Biosorbents for heavy metals removal and their future

Biotechnology Advances 27 (2009) 195–226

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Biotechnology Advances j o u r n a l h o m e p a g e : w w w. e l s e v i e r. c o m / l o c a t e / b i o t e c h a d v

Research review paper

Biosorbents for heavy metals removal and their future Jianlong Wang ⁎, Can Chen Laboratory of Environmental Technology, INET, Tsinghua University, Beijing 100084, PR China

a r t i c l e

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Article history: Received 8 October 2008 Received in revised form 18 November 2008 Accepted 21 November 2008 Available online 6 December 2008 Keywords: Biosorbent Biosorption Heavy metal ions Bacteria Fungi Algae Biomass Kinetics Immobilization Application

a b s t r a c t A vast array of biological materials, especially bacteria, algae, yeasts and fungi have received increasing attention for heavy metal removal and recovery due to their good performance, low cost and large available quantities. The biosorbent, unlike mono functional ion exchange resins, contains variety of functional sites including carboxyl, imidazole, sulphydryl, amino, phosphate, sulfate, thioether, phenol, carbonyl, amide and hydroxyl moieties. Biosorbents are cheaper, more effective alternatives for the removal of metallic elements, especially heavy metals from aqueous solution. In this paper, based on the literatures and our research results, the biosorbents widely used for heavy metal removal were reviewed, mainly focusing on their cellular structure, biosorption performance, their pretreatment, modification, regeneration/reuse, modeling of biosorption (isotherm and kinetic models), the development of novel biosorbents, their evaluation, potential application and future. The pretreatment and modification of biosorbents aiming to improve their sorption capacity was introduced and evaluated. Molecular biotechnology is a potent tool to elucidate the mechanisms at molecular level, and to construct engineered organisms with higher biosorption capacity and selectivity for the objective metal ions. The potential application of biosorption and biosorbents was discussed. Although the biosorption application is facing the great challenge, there are two trends for the development of the biosorption process for metal removal. One trend is to use hybrid technology for pollutants removal, especially using living cells. Another trend is to develop the commercial biosorbents using immobilization technology, and to improve the biosorption process including regeneration/reuse, making the biosorbents just like a kind of ion exchange resin, as well as to exploit the market with great endeavor. © 2008 Elsevier Inc. All rights reserved.

Contents 1. 2.

3. 4.

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . Cell structure: prokaryotes and eukaryotes. . . . . . . . . . . 2.1. Bacterial structure . . . . . . . . . . . . . . . . . . . 2.1.1. Shape and size . . . . . . . . . . . . . . . . 2.1.2. Cell structure . . . . . . . . . . . . . . . . . 2.2. Fungal structure. . . . . . . . . . . . . . . . . . . . 2.2.1. Classification and general characteristics . . . . 2.2.2. Cell wall and its main composite polysaccharide 2.2.3. Cell membrane . . . . . . . . . . . . . . . . 2.2.4. Cytoplasm . . . . . . . . . . . . . . . . . . 2.3. Algae structure . . . . . . . . . . . . . . . . . . . . 2.3.1. Introduction and its classification . . . . . . . 2.3.2. Cell wall of algae . . . . . . . . . . . . . . . 2.4. Functional groups related to the biosorption . . . . . . Bacterial biosorbents . . . . . . . . . . . . . . . . . . . . . Fungal biosorbents . . . . . . . . . . . . . . . . . . . . . . 4.1. Introduction. . . . . . . . . . . . . . . . . . . . . . 4.2. Yeast . . . . . . . . . . . . . . . . . . . . . . . . . 4.3. Filamentous fungi . . . . . . . . . . . . . . . . . . .

⁎ Corresponding author. Tel.: +86 10 62784843; fax: +86 10 62771150. E-mail address: [email protected] (J. Wang). 0734-9750/$ – see front matter © 2008 Elsevier Inc. All rights reserved. doi:10.1016/j.biotechadv.2008.11.002

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4.3.1. Penicillium . . . . . . . . . . . . . . . . . 4.3.2. Aspergillus . . . . . . . . . . . . . . . . . 4.3.3. Other fungi . . . . . . . . . . . . . . . . . 4.4. Selectivity and competitive biosorption by fungi . . . . 4.5. Comparison of fungi and yeast with other biosorbents . 5. Marine algae as biosorbents . . . . . . . . . . . . . . . . . 5.1. Introduction . . . . . . . . . . . . . . . . . . . . . 5.2. Performance. . . . . . . . . . . . . . . . . . . . . 5.3. Comparison of algae with other biosorbents . . . . . . 6. Effect of pre-treatment on biosorption . . . . . . . . . . . . 7. Biosorbent immobilization for bioreactors and regeneration/reuse 8. Modeling of biosorption: isotherm and kinetic models . . . . 8.1. Equilibrium modeling of biosorption . . . . . . . . . 8.2. Kinetic modeling of biosorption in a batch system . . . 9. Biosorbent selection and assessment . . . . . . . . . . . . . 10. Development of novel biosorbents . . . . . . . . . . . . . . 11. Application of biosorption . . . . . . . . . . . . . . . . . . 11.1. Several attempts of the biosorption commercialization 11.2. Application feasibility and consideration. . . . . . . 12. The future of biosorption . . . . . . . . . . . . . . . . . . Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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1. Introduction Biosorption can be defined as the removal of metal or metalloid species, compounds and particulates from solution by biological material (Gadd, 1993). Large quantities of metals can be accumulated by a variety of processes dependent and independent on metabolism. Both living and dead biomass as well as cellular products such as polysaccharides can be used for metal removal. Heavy metal pollution is one of the most important environmental problems today. Various industries produce and discharge wastes containing different heavy metals into the environment, such as mining and smelting of metalliferous, surface finishing industry, energy and fuel production, fertilizer and pesticide industry and application, metallurgy, iron and steel, electroplating, electrolysis, electro-osmosis, leatherworking, photography, electric appliance manufacturing, metal surface treating, aerospace and atomic energy installation etc. Thus, metal as a kind of resource is becoming shortage and also brings about serious environmental pollution, threatening human health and ecosystem. Three kinds of heavy metals are of concern, including toxic metals (such as Hg, Cr, Pb, Zn, Cu, Ni, Cd, As, Co, Sn, etc.), precious metals (such as Pd, Pt, Ag, Au, Ru etc.) and radionuclides (such as U, Th, Ra, Am, etc.) (Wang and Chen, 2006). Methods for removing metal ions from aqueous solution mainly consist of physical, chemical and biological technologies. Conventional methods for removing metal ions from aqueous solution have been suggested, such as chemical precipitation, filtration, ion exchange, electrochemical treatment, membrane technologies, adsorption on activated carbon, evaporation etc. However, chemical precipitation and electrochemical treatment are ineffective, especially when metal ion concentration in aqueous solution is among 1 to 100 mg L− 1, and also produce large quantity of sludge required to treat with great difficulty. Ion exchange, membrane technologies and activated carbon adsorption process are extremely expensive when treating large amount of water and wastewater containing heavy metal in low concentration, they cannot be used at large scale. Volesky (2001) summarized the advantages and disadvantages of those conventional metal removal technologies. In recent years, applying biotechnology in controlling and removing metal pollution has been paid much attention, and gradually becomes hot topic in the field of metal pollution control because of its potential application. Alternative process is biosorption, which utilizes various certain natural materials of biological origin,

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including bacteria, fungi, yeast, algae, etc. These biosorbents possess metal-sequestering property and can be used to decrease the concentration of heavy metal ions in solution from ppm to ppb level. It can effectively sequester dissolved metal ions out of dilute complex solutions with high efficiency and quickly, therefore it is an ideal candidate for the treatment of high volume and low concentration complex wastewaters (Wang and Chen, 2006). The capability of some living microorganisms to accumulate metallic elements have been observed at first from toxicological point of view (Volesky, 1990a,b,c). However, further researches have revealed that inactive/dead microbial biomass can passively bind metal ions via various physicochemical mechanisms. Therefore researches on biosorption have become an active field for the removal of metal ions or organic compounds. Biosorbent behavior for metallic ions is a function of the chemical make-up of the microbial cells of which it consists (Volesky and Holan, 1995). Mechanisms responsible for biosorption, although understood to a limited extent, may be one or combination of ion exchange, complexation, coordination, adsorption, electrostatic interaction, chelation and microprecipitation (Veglio and Beolchini, 1997; Vijayaraghavan and Yun, 2008; Wang and Chen, 2006). A large quantity of materials has been investigated as biosorbents for the removal of metals or organics extensively. The tested biosorbents can be basically classified into the following categories: bacteria (e.g. Bacillus subtillis), fungi (e.g. Rhizopus arrhizus), yeast (e.g., Saccharomyces cerevisiae), algae, industrial wastes (e.g., S. cerevisiae waste biomass from fermentation and food industry), agricultural wastes (e.g. corn core) and other polysaccharide materials, etc. (Vijayaraghavan and Yun, 2008). The role of some groups of microorganisms has been well reviewed, such as bacteria, fungal, yeast, algae, etc. These tested biomasses have been reported to bind a variety of heavy metals to different extents (Gupta et al., 2000). Some potential biomaterials with high metal binding capacity have been identified in part. Some types of biosorbents binding and collecting the majority of heavy metals with no specific priority, while others can even be specific for certain types of metals (Volesky and Holan, 1995). The biosorbent materials among easily available include three groups: algae, fungi, and bacteria, the former two perhaps giving broader choices. Waste materials or by-product biomass from largescale fermentation processes are the source of new family of biosorbents conveniently. In particular, some waste mycelia are available in large quantities for the removal of heavy metals (Kapoor

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and Viraraghavan, 1995; Wang and Chen, 2006). Seaweeds from the oceans produced in copious quantities are another inexpensive source of biomass. Marine algae, especially brown algae such Sargasso seaweed was investigated for metal removal (Davis et al., 2003c). Abundant natural materials, particularly cellulosic nature, have been suggested as potential biosorbents for the removal of heavy metals. For economical reasons, other low-cost biosorbents are of interest recently, such as agricultural wastes (Bailey et al., 1999). The first major challenge for the biosorption field was to select the most promising types of biomass from an extremely large pool of readily available and inexpensive biomaterials (Kratochvil and Volesky, 1998). Although many biological materials can bind heavy metals, only those with sufficiently high metal-binding capacity and selectivity for heavy metals are suitable for use in a full-scale biosorption process. A large number of biomass types have been investigated for their metal binding capability under various conditions. Volesky and Holan (1995) have presented an exhaustive list of microbes and their metal-binding capacities. The published work on testing and evaluating the performance of biosorbents offered a good basis for looking for new and potentially feasible metal biosorbents. Another challenge is that the application of biosorption is facing up with great difficulty (Tsezos, 2001). Great efforts have to be made to improve biosorption process, including immobilization of biomaterials, improvement of regeneration and re-use, optimization of biosorption process etc. In recent 10 years, our lab has attempted to carry out the relevant researches on biosorption phenomena, especially for the removal of metal ions (Chen and Wang, 2007a,b,c,d,e, 2008a,b,c; Liu et al., 2002; Wang et al., 2000, 2001). In this review, an extensive list of biosorbent literature including our research results has been compiled to provide a summary of available information on a wide range of biosorbents for metal removal. The cell structure was introduced first. Then biosorption performances of various biosorbents, including bacteria, filamentous fungi, and marine algae were summarized. Because the different criteria were used by the various authors in searching for suitable material, the results were reported in different units and in different ways, which often make quantitative comparison impossible. As for the biosorbents, it can be easily available biomass, or specially isolated microorganisms, or modified raw biomass to improve its biosorption application properties. It should be noted that comparing results from different sources involve in standardizing the different ways that the sorption capacity may be expressed. The aim of this work is to present the state of the art of biosorbent investigation and to compare results found in the literature. The pretreatment, immobilization, and regeneration/reuse of biosorbents, modeling of biosorption process, biosorbent assessment, as well as the development of novel biosorbents were presented and discussed, their potential application and future were predicted. 2. Cell structure: prokaryotes and eukaryotes A variety of reviews and books of microbiology were devoted to the microbial structure and function (Baron, 1996; Madigan et al., 2000; Moat et al., 2002; Prescott et al., 2002; Remacle, 1990; Talaro and Talaro, 2002; Tortora et al., 2004; Urrutia, 1997). Here we only simply introduce the basic structure necessary for understanding the mechanisms of biosorption. Microbial cells have two fundamentally different types of cells— procaryotic and eukaryotic—and are distributed among several kingdoms or domains. Procaryotic cells have a much simpler and smaller structure than eukaryotic cells and lack a true membrane-delimited nucleus. It generally lacks extensive, complex, internal membrane systems although with a plasma membrane. In contrast, eukaryotic cell have a membrane-enclosed nucleus and many membranous organelles. They are more complex morphologically and are usually larger than procaryotes. Algae, fungi, protozoa, higher plants, and animals are eukaryotic (Prescott et al., 2002). Prokaryotes are

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represented by bacteria and archaea. Most bacteria can be divided into Gram-positive and Gram-negative groups based on their cell wall structure and response to the Gram staining. Most bacteria and yeast are unicellular. Typical bacterial cells range in diameter from 0.5 to 1.0 μm, some wider than 50 μm. Typical eukaryotic cells may be 2 μm to more than 200 μm in diameter. Apart from the above-mentioned differences, procaryotes are simpler functionally in several ways than eukaryotic cells. Eukaryotic cells have mitosis and meiosis, and many complex eukaryotic processes which are absent in procaryotes: phagocytosis and pinocytosis, intracellular digestion, directed cytoplasmic streaming, ameboid movement, and others. The plasma membrane in prokaryotes performs most functions carried out by membranous organelles in eukaryotes. Despite the profound structural and functional differences between prokaryotes and eucaryotes, both cells are similar on the biochemical level. A typical cell of prokaryotes or eukaryotes includes four major components: cell wall, cell membrane, cytoplasm, and nuclear area. Cell wall is a rigid outer layer of the cell membrane, which provides support and protection from osmotic lysis. The chemical composition of the cell wall differs from group to another cell. All fungi, and most bacteria and algae have cell walls. The cell membrane, or plasma membrane, or cytoplasmic membrane, is the critical permeability barrier, with a lipid and protein layer surrounding cytoplasm. It is the boundary between the cell and its environment when lacking cell walls. The membrane is the chief point of contact with the cell's environment and thus is responsible for communication with the outside world. The exact proportions of protein and lipid in the cell membrane vary widely in different group of microorganisms. Eukaryotic plasma membranes usually have a lower proportion of protein than bacterial membranes. Cell membranes are about 5 to 10 nm thickness, and can be only viewed under electron microscope. Lipids in membrane are structurally asymmetric with polar ends (hydrophilic) and nonpolar ends (hydrophobic), usually these asymmetric lipids are phospholipids. One major difference in chemical composition of membrane between eukaryotic and prokaryotic cells is that bacterial membranes, unlike eukaryotic membranes, lack sterols such as cholesterol. Sterols can make up from 5 to 20% of the total lipids of eukaryotic membranes. Sterols are rigid, planar molecules, whereas fatty acids are flexible serving to stabilized its structure and make it less flexible. However, bacterial membranes contain pentacyclic sterol-like molecules called hopanoids. A most widely accepted model for membrane structure is the fluid mosaic model, proposed by S. Jonathan Singer and Garth Nicholson. There are two types of membrane proteins: peripheral proteins and integral proteins. The former are loosely connected to the membrane and can be easily removed, they are soluble in aqueous solutions and make up about 20 to 30% of total membrane protein. The later compose about 70 to 80% of membrane proteins. They are not easily extracted from membranes and are insoluble in aqueous solutions when free of lipids. The integral proteins are also asymmetric (Prescott et al., 2002). Cytoplasm, aqueous fluid of the cell, contains organelles, enzymes, chemicals, in which most cellular metabolic activities occur, e.g. ribosomes. Bacteria do not contain internal membrane-bound organelles, their interior appears morphologically simple. Ribosomes are small particles composed of protein and ribonucleic acid (RNA). Ribosomes are part of the translation apparatus, and the synthesis of cell proteins takes place on these structures. Procaryotic cells occasionally contain inclusions consisting of storage materials, compounds made up of carbon, nitrogen, sulfur, or phosphorus, formed when these nutrients are in excess. Algae have an additional type of organelle: chloroplast. Eukaryotic cells differ most obviously from procaryotic cells, they have a variety of complex membranous organelles in the cytoplasmic matrix and the majority of their genetic materials are within membrane-delimited nuclei. Each organelle has a distinctive structure directly related to specific functions. Nuclear area includes hereditary materials, deoxyribonucleic acid (DNA). For most of cells, but not bacteria, DNA existed within nuclear area. In bacteria,

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Table 1 The major classes of chemical constituents in the walls and envelopes of Gram-positive and Gram-negative bacteria Gram-positive cell walls

Examples

Peptidoglycan Polysaccharides Teichoic acids Ribitol

All species Streptococcus group A, B, C substances

Glycerol

S. aureus B. subtilis Lactobacillus spp B. licheniformis M. lysodeikticus

Teichuronic acids (aminogalacluronic or aminomannuronic acid polymers) Peptidoglycolipids (muramylpeptide– Corynebacterium spp polysaccharide–mycolates) Mycobacterium spp Nocardia spp Glycolipids (“Waxes”) (polysaccharide–mycolates) Gram-negative envelopes LPS (Lipoteichoic acids) All species Lipoprotein E. coli and many enteric bacteria Pseudomonas aeruginosa Porins (major outer membrane proteins) E. coli, Salmonella typhimurium Phospholipids and proteins All species Peptidoglycan Almost all species Source: Salton and Kwan 1996, http://gsbs.utmb.edu/microbook/ch002.htm.

2.1.2.1. Cell wall and Gram-negative cell envelope. Main function of cell wall include: (1) The cell wall gives cell shape and protect it from osmotic lysis; (2) The wall can protects cell from toxic substances (3) The cell wall offers the site of action for several antibiotics. (4) The cell wall is necessary for normal cell division. The major classes of chemical constituents in the walls and envelopes of Gram-positive and Gram-negative bacteria are summarized by Salton and Kwan (http://gsbs.utmb.edu/microbook/ch002. htm), shown in Table 1. By Gram staining technique, the Gram-positive bacteria stained purple, whereas Gram-negative bacteria were colored pink or red. The surface of Gram-negative cells is much more complex chemically and structurally than that of Gram-positive cells. Because of the thicker peptidoglycan layer, the walls of Gram-positive cells are stronger than those of Gram-negative bacteria. Cellular wall shape and strength is primarily due to peptidoglycan, which is a rigid, porous, and amorphous material, the core of which is very similar in all bacteria. Unique features of almost all prokaryotic cells are cell wall peptidoglycan and the specific enzymes involved in its biosynthesis. The amount and exact composition of peptidoglycan only found in cell walls vary among the major bacterial groups. Peptidoglycan is a linear polymer of alternating units of two sugar derivatives, N-acetylglucosamine (NAG) and N-acetylmuramic acid (NAM) (Fig. 1). Peptidoglycan also contain several different amino acids, three of which—D -glutamic acid, D-alanine, and meso-

the genetic materials are localized in a discrete region, the nucleoid, and are not separated from the surrounding cytoplasm by membranes. Prokaryotic cells do not possess true nucleus, the function of the nucleus is performed by a single molecule of DNA. The key difference between eukaryotic and prokaryotic cells is that eukaryotes contain true nuclei. In this review, we will mainly discuss three groups of biomass materials related to metal biosorpion: bacteria (Gram-positive and Gram-negative cells), fungi (filamentous fungi and yeast) and algae. The interface between the microbial cells and its external environment is cell surface. The structure and composition of different cell surfaces can vary considerably, depending on the organism. Due to the importance of the cell surface, especially the cell wall for metal biosorption, the cell surface structures of three groups of microorganisms will be described in detail in term of their metal biosorption performance. 2.1. Bacterial structure 2.1.1. Shape and size Bacteria have simple morphology. The most commonly bacteria present in three basic shapes: spherical or ovoid (coccus), rod (bacillus, with a cylindrical shape), and spiral (spirillum), although there are a great variety of shapes due to differences in genetics and ecology. Bacteria vary in size as much as in shape. For many prokaryotes, the cells remain together in groups or clusters after division (pairs, chains, tetrads, clusters, etc.). Cocci or rods may occur in long chains. The gramnegative organism, Escherichia coli often as typical size of bacteria cell, is about 1.1 to 1.5 μm wide by 2.0 to 6.0 μm long. The smallest bacteria are about 0.3 μm, and a few bacteria become fairly large, e.g. some spirochetes occasionally reach 500 μm in length, and cyanobacterium Oscillatoria is about 7 μm in diameter. Cell size is an important characteristic for an organism. Small size of bacteria is very important because size affects a number of cell biological properties. Small size of bacteria ensures rapid metabolic processes. 2.1.2. Cell structure A “typical” bacterial cell (e.g., E. coli), contains cell wall, cell membrane, cytoplasmic matrix consisting of several constituents, which are not membrane-enclosed: inclusion bodies, ribosomes, and the nucleoid with its genetic material. Some bacteria have special structure, such as flagella, S-layer.

Fig. 1. Peptidoglycan subunit composition. The peptidoglycan subunit of Escherichia coli, most other Gram-negative bacteria, and many Gram-positive bacteria, NAG is Nacetylglucosamine; NAM is N-acetylmuramic acid (NAG with lactic acid attached by an ether linkage). The tetrapeptide side chain is composed of alternating D- and L-amino acids since meso-diaminopimelic acid is connected through its L-carbon. NAM and the tetrapeptide chain attached to it are shown in different shades of color for clarity. Source: Prescott et al., 2002:56.

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Fig. 2. Composition of the cell surfaces of Gram-positive and Gram-negative bacteria. Not all structures shown are found in all organisms. For example, M protein is only used to describe a structure in some of the streptococci. Also, not all organisms have flagella. Source: Moat et al., 2002:3.

diaminopimelic acid—are not found in proteins. N-acetylglucosamine is also the main constituent of chitin. However, the three-dimensional structure differs from the crystalline structure of the chitin. A peptide chain of four or five alternating D- and L-amino acids is connected to the carboxyl group of N-acetylmuramic acid. The disaccharide-peptide units are joined by direct peptide bonds or by short peptides. The carboxyl group of the terminal D-alanine is often connected directly to the amino group of diaminopimelic acid. A common feature of bacterial cell walls is cross-bridging between the peptide chains. There are several types of peptidoglycan, depending on the nature and the localization of the peptide bridge. In a Gram-positive cell, the cross-bridging between adjacent peptides may be close to 100%, such as Staphylococcus aureus. By contrast, the frequency of cross-bridging in E. coli (a Gram-negative organism) may be as low as 30%. The peptidoglycan layer of a Gramnegative cell is generally a single monolayer, composed of phospholipids, lipopolysaccharides, enzymes, and other proteins, including lipoproteins. Fig. 1 showed the peptidoglycan cross-links in a Gramnegative and a Gram-positive cell. Most Gram-negative cell wall peptidoglycans lack the peptide interbridge. This cross-linking results in an enormous peptidoglycan sac which is actually a dense, interconnected network. These sacs are elastic and porous, molecules can penetrate them (Prescott et al., 2002). The Gram-positive cell wall consists of a single 20 to 80 nm thick homogeneous peptidoglycan or murein layer lying outside the plasma membrane. It also contains large amounts of teichoic acids, polymers of glycerol or ribitol joined by phosphate groups (Fig. 2). Peptidoglycan of a Gram-positive cell wall accounts for 40 to 90% of the cell wall materials, containing a peptide interbridge. This peptidoglycan core is usually between 20 and 40 layers thick, and adjacent glycan chains are cross linked through the amino acid stems forming a highly resilient, three-dimensional macromolecule that surrounds the cells. Amino acids such as D-alanine or sugars like glucose are attached to the glycerol and ribitol groups. The teichoic acids are connected to either the peptidoglycan itself by a covalent bond with the six hydroxyl of Nacetylmuramic acid or to plasma membrane lipids (called lipoteichoic acids) (Prescott et al., 2002). Lipoteichoic acids, only present in Grampositive organisms—are synthesized at the membrane surface and may extend through the peptidoglycan layer to the outer surface, are polymers of amphiphitic glycophosphates with the lipophilic glycolipid and anchored in the cytoplasmic membrane. They are antigenic, cytotoxic and adhesins (e.g., Streptococcus pyogenes). Teichoic acids appear to extend to the surface of the peptidoglycan, and, because they are negatively charged, they are helpful to give the Gram-positive cell wall negative charge. The teichuronic acids are free of phosphate and made up of hexuronic acid linear chains. The proportion of teichoic acids and teichuronic acids depends on the

cultural conditions, especially on the phosphate supply. The functions of these molecules are still unclear, but they may be important in maintaining the structure of the wall. Teichoic acids are not present in Gram-negative bacteria. It is proved that the teichoic acids and teichuronic acids participate in metal tripping. Both the phosphoryl groups of the secondary polymers and the carboxyl groups of the peptide chains provide negatively charged sites in the Gram-positive cell wall (Moat et al., 2002; Prescott et al., 2002; Remacle, 1990; Urrutia, 1997). Cell wall teichoic acids are found only in certain Gram-positive bacteria (such as Bacillus spp.), and their structures are illustrated in

Fig. 3. Structures of cell wall teichoic acids. Teichoic acid is a polymer of chemically modified ribitol (A) or glycerol phosphate (B). The nature of the modification (e.g., sugars, amino acids) can define the serotype of the bacteria. Teichoic acid may be covalently attached to the peptidoglycan. Lipoteichoic acid is anchored in the cytoplasm membrane by a covalently attached fatty acid. Source: http://micro.digitalproteus.com/ morphology3.php.

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Fig. 4. Lipopolysaccharide Structure. (A) The lipopolysaccharide from Salmonella. This slightly simplified diagram illustrates one form of the LPS. Abbreviations: Abe, abequose; Gal, galactose; Glc, glucose; GlcN, glucosamine; Hep, heptulose; KDO, 2-keto-3-deoxyoctonate; Man, mannose; NAG, N-acetylglucosamine; P, phosphate; Rha, L-rhamnose. Lipid A is buried in the outer membrane. (B) Molecular model of an Escherichia coli lipopolysaccharide. The lipid A and core polysaccharide are straight; the O side chain is bent at an angle in this model. Source: Prescott et al., 2002:60.

Fig. 3. Teichoic acids are polyol phosphate polymers, with either ribitol or glycerol linked by phosphodiester bonds. Substituent groups on the polyol chains include D-alanine (ester linked), N-acetylglucosamine, N-acetylgalactosamine, and glucose. They are strongly antigenic. These highly negatively charged polymers of the bacterial cell wall can serve as a cation-sequestering mechanism. The Gram-negative cell wall is much more complex than the Grampositive cell, about 30 to 80 nm thick. It is a multilayered structure. It has a 2 to 7 nm peptidoglycan layer surrounded by a 7 to 8 nm thick outer membrane. The peptidoglycan is sandwiched between the plasma membrane and the outer membrane, which is composed of phospholipids, lipopolysaccharides, enzymes, and other proteins, including lipoproteins. The thin peptidoglycan layer next to the plasma membrane may constitute not more than 5 to 10% of the cell wall weight. In E. coli it is about 2 nm thick and contains only one or two layers or sheets of peptidoglycan. Only one type of the peptide bridge occurs between the glycan chains. The space between the outer membrane and the inner membrane is referred to as the periplasmic space, which is the translucent region where various enzymes and proteins located. The peptidoglycan is covalently bound to the outer membrane by lipoproteins. The outer membrane is composed of lipopolysaccharide (LPSs), phospholipids and proteins. The Gram-negative bacteria have various types of complex macromolecular lipopolysaccharide (LPS). LPSs are probably the most unusual constituents of the outer membrane. LPSs structure was illustrated in Figs. 4 and 5. LPSs contain both lipids and carbohydrates, and consist of three parts: (1) lipid A, (2) the core polysaccharide, and (3) the O side chain. The structure of lipid A required for insertion in the outer leaflet of the outer membrane bilayer; a covalently attached core composed of 2-keto-3deoxyoctonic acid (KDO), heptose, ethanolamine, N-acetylglucosamine, glucose, and galactose; and polysaccharide chains linked to the core. The polysaccharide chains constitute the O-antigens of the Gram-negative bacteria, and the individual monosaccharide constituents confer serologic specificity on these components. LPS and phospholipids help confer asymmetry to the outer membrane of the Gram-negative

bacteria, with the hydrophilic polysaccharide chains outermost. Each LPS is held in the outer membrane by relatively weak cohesive forces (ionic and hydrophobic interactions) and can be dissociated from the cell surface with surface-active agents (http://gsbs.utmb.edu/microbook/ch002.htm). The net negative charge of LPSs attributes to the negative surface charge of Gram-negative bacteria. The phosphate groups within LPSs and phospholipids have been proved to be the primary sites for metal interaction. However, only one of the carboxyl groups in LPSs is free to interact with metals (Moat et al., 2002; Prescott et al., 2002; Remacle, 1990; Urrutia, 1997). 2.1.2.2. Capsules and loose slime. Some bacterial cells can produce capsules or slime layer above the bacterial cell wall. They are highly hydrated (N95% water) and loosely arranged polymers of carbohydrates and proteins. Capsules are composed of polysaccharides (high molecular-weight polymers of carbohydrates), and a few consist of proteins or polymers of amino acids called polypeptides (often formed from the D- rather than the L-isomer of an amino acid). The capsule of Streptococcus pneumoniae type III is composed of glucose and glucuronic acid in alternating β-1, 3- and β-1, 4- linkages (Moat et al., 2002):

Bacillus anthracis, the anthrax bacillus, can produce polypeptide capsules composed of D-glutamic acid subunits. Capsule may be thick or thin, rigid or flexible, depending on specific organism. Several different terms can be found to describe the capsule layer, such as slime layer, glycocalyx (defined as the polysaccharide-containing material lying outside the cell), extracellular polysaccharide (EPS). Capsule polymers are usually acidic in nature although capsules can

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Fig. 5. The three major, covalently linked regions that form the typical LPS. Source: Salton and Kwan 1996, http://gsbs.utmb.edu/microbook/ch002.htm.

consist of neutral polysaccharide, charged polysaccharide or charged polypeptide. Capsule arrangement is important to metal binding (Madigan et al., 2000; Moat et al., 2002; Urrutia, 1997). Many prokaryotes contain a cell surface layer composted of a twodimensional array of proteins, or glycoproteins, called S-layers or paracrystalline surface layer. S-layers have a crystalline appearance in p1, p2, p4, p6 symmetry, such as hexagonal (p6) and tetragonal (p4), depending on the number and structure of proteins or glycoproteins subunits of which they are composted. Non-covalent interactions, such as hydrogen bonding, electrostatic attraction, and salt-bridging, are involved in the attachment between neighbouring subunits and the underlying wall. Commonly, divalent metal cations contribute to the correct assembly of the structure. Metals can also be bound after assembly. S-layers are associated with LPSs of Gram-negative or peptidoglycan of a Gram-positive cell (Madigan et al., 2000; Urrutia, 1997). 2.2. Fungal structure 2.2.1. Classification and general characteristics Microscopic fungi include yeasts with spherical budding cells and molds with elongate filamentous hyphae in mycelia. The molds are filamentous fungi, such as Penicillium, Aspergillus, etc. The body or vegetative structure of a fungus is called thallus (pl., thalli), which varies in complexity and size from single cell microscopic yeasts to multicellular molds. A single filament is called a hypha. Hyphae usually grow together, collectively called a mycelium. Classification of fungi was showed in Table 2. Apart from Oomycetes, which are phylogenetically distinct, the other groups of fungi are closely related. Yeasts are unicellular fungi—mainly ascomycetes. Fungi may be grouped into molds or yeasts based on the development of the thallus, which is the body or vegetative structure of a fungus. Yeasts are unicellular fungi. Yeasts reproduce either asexually by budding and transverse division or sexually through spore formation. A mold consists of long, branched, thread-like filaments of cells, the hyphae, which form a tangled mass called a mycelium. Hyphae may be either septate or coenocytic (nonseptate). The mycelium can produce reproductive structures (Prescott et al., 2002). Most fungi are filamentous. The hyphae are typically 5–10 μm wide but may vary from 0.5 μm to 1.00 mm, depending on the various species (Lester and Birkettn, 1999). The mycelium is composed of a complex mass of filaments or hyphae. The hyphae have walls which are composed of cellulose or chitin or both of them. A common cytoplasm exists throughout the hyphae. Thus fungi cellular organization has three types: (1) coenocytic, where the hypha contains a mass of multi-nucleate cytoplasm, also called as aseptate; (2) septate with uni-nucleate protoplasts, where the hypha is divided by crosswalls or

septa, each compartment containing a single nucleus; (3) septate with multi-nucleate protoplasts between the septa. In septate species there is a central pore in the septum connecting the cytoplasm of neighbouring cells and permitting the migration of both cytoplasm and nuclei (Lester and Birkettn, 1999). The yeasts provide an example of a unicellular fungus. Generally yeast cells are larger than bacteria, vary considerably in size. Typical yeast cell is about 2.5 to 10 μm wide by 4.5 to 21 μm long. Yeast cell morphology is commonly spherical to oval shaped and varies, depending on the yeast species, nutrition level, cultural condition. The cells of most microscopic fungi grow in loose associations or colonies. Most yeasts reproduce only as single cell, however some yeasts can form filaments under certain conditions. Some yeasts exhibit sexual reproduction by a process called mating. The colonies of yeasts are much like those of bacteria because they have a soft, uniform texture and appearance. The most important commercial yeasts are the baker's and brewer's yeasts, which are member of the genus Saccharomyces (Madigan et al., 2000). Baker's and brewer's yeasts are eukaryotic cells. They are easily manipulable thus are excellent models for the study of many important problems in eukaryotic biology. S. cerevisiae is a famous model eukaryote for scientific study, and was the first eukaryote to have its genome completely sequenced. S. cerevisiae is a species of budding yeast. “Saccharomyces” derives from Greek, and means “sugar mold”; “cerevisiae” comes from Latin, and means “of beer”. It is perhaps the most useful yeast owing to its use since ancient times in baking and brewing. It is believed that it was originally isolated from the skins of grapes (one can see the yeast as a component of the thin white film on the skins of some dark-colored fruits such as plums; it exists among the waxes of the cuticle). It is one of the most intensively studied eukaryotic model organisms in molecular and cell biology, much like E. coli as the model prokaryote.

Table 2 The classification of fungi Group

Common name

Hyphae

Typical representative

Ascomycetes

Sac fungi

Septate

Basidiomycetes

Club fungi, mushroom

Septate

Zygomycetes

Bread molds

Coenocytic

Oomycetes Deuteromycetes

Water molds Fungi imperfecti

Coenocytic Septate

Neurospora Saccharomyces Morchella Amanita Agaricus Mucor Rhizopus Allomyces Penicillium Aspergillus Candida

Adapted from Madigan et al., 2000:729.

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It is the microorganism behind the most common type of fermentation. S. cerevisiae cells are round to ovoid, 5–10 μm in diameter. It reproduces by a division process known as budding. Our lab has selected the cells of S. cerevisiae to explore the characteristics of metal biosorption and interaction of metal-microbe, and conducted a series of experiments, published some meaningful results (Chen and Wang, 2006, 2007a,b,c,d,e, 2008a,b,c; Wang, 2002a; Wang and Chen, 2006). In general, yeast cells have a cell wall, cytoplasmic membrane, cytoplasm and inclusions, a single nucleus, mitochondria, endoplasmic reticulum, Golgi apparatus, vacuoles, cytoskeleton, and glycocalyx. The yeast has no flagella but do possess most of the other eukaryotic organelles.

Fig. 6. Glycocalyx structure. Cross section through the tip of a fungal cell shows the general structure of the cell wall and other features. Top: photomicrograph. (S, growing tip; CV, coated vesicles; G, Golgi apparatus; M, mitochondrion) Bottom: the cell wall is a thick, rigid structure composed of complex layers of polysaccharides and proteins. From Talaro and Talaro, (2002):127.

2.2.2. Cell wall and its main composite polysaccharide The cell walls of the fungi and algae are rigid and provide structural support and shape, but they are different in chemical composition from procaryotic cell walls. Fungal cell walls are mainly 80–90% polysaccharide, with proteins, lipids, polyphosphates, and inorganic ions, making up the wall-cementing matrix. Chitin is a common constituent of fungal cell walls. Chitin is a strong but flexible nitrogencontaining polysaccharide, consisting of N-acetylglucosamine residues. Two layers were observed in ultrastructural studies of the fungal cell walls (Fig. 6): a thin outer layer consisting of mixed glycans (such as glucans, mannans, or galactans), and a thick inner mcirofibrillar layer of polysaccharide fibers composed of chitin or cellulose with chitin chains in parallel arrangement, sometimes of cellulose chains or

Fig. 7. Structures of cellulose, chitin, glucan and manna. Source for Cellulose: http://www.scientificpsychic.com/fitness/carbohydrates2.html. Source for Chitin: http://www. scientificpsychic.com/fitness/carbohydrates2.html. Source for β-Glucan: http://www.scientificpsychic.com/fitness/glucan.gif. Source for Manna: Davis et al., 2003.

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in certain yeasts, noncellulosic glucan (Remacle, 1990; Talaro and Talaro, 2002). The structures of cellulose, chitin, glucan, manna were shown in Fig. 7. 2.2.3. Cell membrane The cell membrane of eukaryotic cells is a thin, double-layered sheet composed of lipids, such as phospholipids and sterols (averaging about 40% of membrane content) and protein molecules (averaging about 60%). Sterols are different from phospholipids in both structure and behavior. Fluid mosaic model for membrane structure are widely accepted. Cell membrane is a continuous bilayer formed by lipids that are oriented with the polar lipid heads toward outside and the nonpolar heads toward the center of the membrane. Embedded at numerous sites in this bilayer are various sized globular proteins. Some cell membranes are so thin—on the average, just 7 nm thick. Cytoplasmic membranes served as selectively permeable barriers in transport. Unlike procaryotes, eukaryotic cells also contain a number of individual membranebound organelles that are extensive enough to account for 60% to 80% (in volume) (Prescott et al., 2002; Talaro and Talaro, 2002). 2.2.4. Cytoplasm The cytoplasm contains the organelles characteristic of eukaryotic organisms including mitochondria, ribosomes and an extensive endoplasmic reticulum. Vacuoles containing storage materials such as glycogen, lipids and volutin are also present. In a uni-cellular fungus such as Saccharomyces spp., the protoplast is enclosed in a semipermeable membrane, the plasma membrane, which is contained within a rigid cell wall. In filamentous species the protoplasm is concentrated in the tips of the young growing hyphae. The older hyphae are usually metabolically inactive and contain large vacuoles in their cytoplasm. The fungi all lack chlorophyll and are heterotrophic. A mycelium normally develops from the germination of a single reproductive cell or spore. Germination initially results in the production of a single long hypha which subsequently branches and ramifies to form a mass of hyphae which constitutes the mycelium. Cytoplasm is important for living cells to interact with metal ions. After entering into the cell, the metal ions are compartmentalized into different subcellular organelles (e.g. mitochondria, vacuole etc.). Vijver et al. (2004) summarized the metal ion accumulation strategies especially internal compartmentalization strategies. Metal accumula-

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tion strategies for essential and non-essential metal ions may be different. For essential metals, limiting metal uptake or strategies with active excretion, storage in an inert form or excretion of stored metal are the main strategies. For non-essential metals, excretion from the metal excess pool and internal storage without elimination are the major strategies and the metal concentration in the cells will increase with elevating external concentration. They pointed out that the cellular sequestration mechanisms mainly have two types: the formation of distinct inclusion bodies and the binding of metals to heat-stable proteins. The former includes three types of granules: type A, amorphous deposits of calcium phosphates, e.g. Zn; type B, mainly containing acid phosphatase, accumulating e.g. Cd, Cu, Hg and Ag; and type C, excess iron stored in granules as haemosiderin. The latter mechanism mainly relates to a specific metal-binding protein, metallothioneins (MT), which are low molecular weight and cysteine-rich, usually occurring in the animal kingdom, plants, eukaryotic microorganisms or some prokaryotes. MT can be induced by many substances, including heavy metal ions, such as Cd, Cu, Hg, Co, Zn etc. (Vijver et al., 2004). The researches on the role of vacuole detoxification of metal ions showed that vacuole-deficient strain displayed much higher sensitivity and decreased large uptake of Zn, Mn, Co and Ni (Ramsay and Gadd, 1997). However no significant difference in Cd and Cu uptake and the sensitivity to both the metal ions between wild type and mutant of S. cerevisiae was observed. Gharieb and Gadd (1998) found that vacuolar-lacking and -defective mutants of S. cerevisiae display higher sensitivity to chromate and tellurite with the decrease on the cellular content of the each metal, whereas the tolerance to selenite with the increase on the cellular content of Se. Avery and Tobin (1992) also confirmed that Sr2+ accumulated mainly stay in the vacuole of the living yeast cell of S. cerevisiae. 2.3. Algae structure 2.3.1. Introduction and its classification Algae abound in nature in aquatic habitats, freshwater, marine and moist soil. Algae contain chlorophyll and carry out oxygenic photosynthesis. Algae are eukaryotic microorganisms that carry out the process of photosynthesis. In these organisms, as well as in green plants, an additional type of organelle is found: the chloroplase. The chloroplast

Table 3 The properties of major groups of algae Group

Common name

Chrysophyta

Yellow–green and Unicellular golden-brown algae; diatoms)

Euglenophyta Euglenoids

Pyrrhophyta Charophyta Chlorophyta

Dinoflagellates Stoneworts Green algae

Phaeophyta

Brown algae

Rhodophyta

Red algae

Morphology

Unicellular, photosynthetic euglenoid flagellates

Pigments

Typical representative

Carbon reserve materials

Cell walls

Major habitats

Chlorophylls a and c

Navacul

Lipids

Freshwater, Protista (single marine, cell or colonial; soil eukaryotic)

Chlorophylls a and b

Euglena

Pramylon (β-1,2-glucan)

Many have two overlapping components made of silica No wall present

Unicellular to leafy

Chlorophylls a and b

Chlamydomonas Starch (α-1,4-glucan)

Cellulose

Filamentousto leafy, occasionally massive and plantlike Unicellular, filamentous to leafy

Chlorophylls a and c, xanthophylls

Laminaria

Laninarin (β-1,3-glucan), mannitol

Cellulose

Chlorophylls a and d, phycocyanin, phycoerythrin

Polysiphonia

Floridean starch (α-1,4- and Cellulose α-1,6-glucan), fluoridoside (glycerol-galactoside)

Adapted from Madigan et al., 2000:736 and Prescott et al., 2002:572.

Kingdom

Freshwater, Protista a few marine Protista Protista Freshwater, Protista soil, a few marine marine Plantae (multicellular; eukaryotic) Marine

Plantae

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is green and is the site where chlorophyll is localized and where the light-gathering functions involved in photosynthesis occur. Algae have been extensively studied due to their ubiquitous occurrence in nature. The term algae refer to a large and diverse assemblage of eukaryotic organisms that contain chlorophyll and carry out oxygenic photosynthesis. It should be noticed that algae are distinct from cyanobacteria, which are also oxygenic phototrophs, but are eubacteria (true bacteria), and are therefore evolutionarily distinct from algae. Although most algae are of microscopic size and hence are clearly microorganisms, a number of forms are macroscopic, some seaweeds growing to over 100 ft in length (Madigan et al., 1997). Algae are unicellular of colonial, the latter occurring as aggregates of cells. When the cells are arranged end to end, the algae is said to be filamentous. Among the filamentous forms, both unbranched filaments and more intricate branched filamentous forms occur. Most algae contain chlorophyll and are thus green in color. However, a few kinds of common algae are note green but appear brown or red because in addition to chlorophyll, other pigments such as carotenoids are present that mask the green color. Algae cells contain one or more chloroplasts, membranous structures that house the photosynthetic pigments. Several characteristics are used to classify algae, including the nature of the chlorophyll(s) present, the carbon reserve polymers produced, the cell wall structure, and the type of motility. All algae contain chlorophyll a. Some, however, also contain other chlorophylls that differ in minor ways from chlorophylls a. The presence of these additional chlorophylls is characteristic of particular algal groups. The distribution of chlorophylls and other photosynthetic pigments in algae was summarized by Madigan et al. (1997). The algal groups include Chlorophyta (green algae), Euglenophyta (euglenoids, also considered with the protozoa), Chrysophyta (golden-brown algae, diatoms), Phaeophyta (brown algae), Pyrrophyta (dino-flagellates) and Rhodophyta (red algae). One of the key characteristics used in the classification of algal groups is the nature of the reserve polymer synthesized as a result of photosynthesis. Algae of the division Chlorophyta produce starch in a form very similar to that of higher plants. By contrast, algae of other groups produce a variety of reserve substances, some polymeric and some as free monomers. In biosorption, various algae were used and investigated as biosorbents for metal removal. The major groups of algae were listed in Table 3 based on their type of pigments, cell wall, stored food materials, and body plan (Talaro and Talaro, 2002). The nature of the chlorophyll(s), the cell wall chemistry, flagellation, form in which food or assimilatory products of photosynthesis are stored, cell morphology, habitat; reproductive structures; life history patterns, etc., these characteristics can be used for the classification of algae. The important differences between brown algae and other algae are in the storage products they utilize as well as in their cell wall chemistry, shown in Table 3 (Davis et al., 2003c; Madigan et al., 2000; Prescott et al., 2002). The algal cell is surrounded by a thin, rigid cell wall. Some algae have an outer matrix lying outside the cell wall, similar to bacterial capsules. The nucleus has a typical nuclear envelope with pores; within the nucleus there are nucleolus, chromatin, and karyolymph. The chloroplasts have membrane-bound sacs called thylakoids that carry out the light reactions of photosynthesis. These organelles are embedded in the stroma where the dark reactions of carbon dioxide fixation take place. A dense proteinaceous area, the pyrenoid that is associated with synthesis and storage of starch may be present in the chloroplasts. Mitochondrial structure varies greatly in the algae. Some algae (euglenoids) have discoid cristae; some, lamellar cristae (green and red algae); and the remaining, (golden-brown and yellow–green, brown, and diatoms) have tubular cristae (Prescott et al., 2002). 2.3.2. Cell wall of algae Algae show considerable diversity in the structure and chemistry of their cell walls. In many cases the cell wall is composed of a network of cellulose fibrils, but it is usually modified by the addition of other

polysaccharides such as pectin (highly hydrated polygalacturonic acid containing small amounts of the hexose rhamnose), xylans, mannans, alginic acids or fucinic acid. In some algae, the wall is additionally strengthened by the deposition of calcium carbonate; these forms are often called “calcareous” or “coralline” (corallike) algae. Sometimes chitin, a polymer of N-acetylglucosamine, is also present in the cell wall. In euglenoids cell wall is absent. In diatioms, the cell wall is composed of silica, to which protein and polysaccharide are added. Even after the diatom dies and the organic materials have disappeared, the external structure remains, showing that the siliceous component is indeed responsible for the rigidity of the cell. Because of the extreme resistance to decay of these diatom frustules, they remain intact for long periods of time and constitute some of the best algal fossils ever found. Algal cell walls are freely permeable to low molecular-weight constituents such as water, ions, gases, and other nutrients. Their cell walls are essentially impermeable, however, to larger molecules or to macromolecules. Algae cell walls contain pores about 3–5 nm wide to allow pass only low-molecular-weight substances such as water, inorganic ions, gases and other small nutrient substances for metabolism and growth. It is usually made of a multilayered microfibrillar framework generally consisting of cellulose and intersperse with amorphous material (Madigan et al., 2000). The cellulose can be replaced by xylan in the Chlorophyta and Rhodophyta in addition to mannan in the Chlorophyta. The Phaeophyta algal mainly contain alginic acid or alginate (the salt of alginic acid) with a smaller amount of sulfated polysaccharide (fucoidan). The Rhodophyta contains a number of sulfated galactans. Both the Phaeophyta and Rhodophyta are potentially excellent heavy metal biosorbents because two divisions contain the largest amount of amorphous embedding matrix polysaccharides and their well known metal binding ability (Davis et al., 2003c). Cell walls are more complex in algae than in fungi or bacteria, and three groups of algae, i.e., brown, red and green algae, are of interest, and need to be differentiated in those three evolutionary pathways (Kuyicak and Volesky, 1990; Rincon et al., 2005). The cell walls of brown algae (Phaeophyta) generally contain three components: cellulose, the structural support; alginic acid, a polymer of mannuronic and guluronic acids (M and G) and the corresponding salts of sodium, potassium, magnesium and calcium; and sulphated polysaccharides (fucoidan matrix). Red algae (Rhodophyta) also contain cellulose, but their interest in connection with biosorption lies in the presence of sulphated polysaccharides made of galactanes (agar and carragenates). Green algae (Chlorophyta) are mainly cellulose, and a high percentage of the cell wall is proteins bonded to polysaccharides to form glycoproteins (Romera et al., 2006). The Chlorophyta or green algae are an extremely varied division. They have chlorophylls a and b along with specific carotenoids, and store carbohydrates as starch. Many of them have cell walls of cellulose. They can present in unicellular, colonial, filamentous, membranous or sheet-like, and tubular types. Green algae are associated with the land plants and have mitochondria with lamellar cristae (Prescott et al., 2002). Most Rhodophyta or red algae are filamentous and multicellular. The stored food is the carbohydrate called floridean starch (composed of α-1,4 and α-1,6 linked glucose residues). The cell walls of most red algae include a rigid inner part composed of microfibrils and a mucilaginous matrix. The matrix is composed of sulfated polymers of galactose called agar, funori, porphysan, and carrageenan, which are responsible for flexible, slippery texture of the red algae. Agar is used extensively in the laboratory as a culture medium component. Many red algae also deposit calcium carbonate in their cell walls and play an important role in building coral reefs (Prescott et al., 2002). The Phaeophyta or brown algae have been proved to be most effective biosobent for metal removal, based on statistical review among those algae tested in biosorption (Romera et al., 2006). Davis et al. (2003c) summarized the characteristics of brown algae and other

J.L. Wang, C. Chen / Biotechnology Advances 27 (2009) 195–226 Table 4 The ligands present in biological systems and three classes of metals Ligand class

Ligands

Metal classes

I: Ligands preferred to Class A II: Other important ligands III: Ligands preferred to Class B

− F −, O2−, OH−, H2O, CO2− 3 , SO4, 3− ROSO−3, NO−3, HPO2− 4 , PO4 , ROH, RCOO−, CfO, ROR Cl−, Br−, N−3, NO−2, SO2− 3 , NH3, N2, RNH2, R2NH, R3N, fN−, –CO–N– R, O2, O−2,O2− 2 H−, I−, R−, CN−, CO, S2−, RS−, R2S, R3As

Class A: Li, Be, Na, Mg, K, Ca, Sc, Rb, Sr, Y, Cs, Ba, La, Fr, Ra, Ac, Al, Lanthanides, Actinides Borderline ions: Ti, V, Cr, Mn, Fe, Co, Ni, Cu, Zn, Ga, Cd, In, Sn, Sb, As Class B: Rh, Pd, Ag, Lr, Pt, Au, Hg, Tl, Pb, Bi

Source: Nieboer and Richardson, 1980; Pearson, 1963; Remacle, 1990.

algae. The cellular structure and biochemistry were introduced in detail, including cellular structure, storage polysaccharides, cell wall and extracellular polysaccharides (fucoidan and alginic acid). Among thirteen orders in the Phaeophyta; however, only Laminariales and Fucales are important from the viewpoint of biosorption. Laminariales, also called as “kelps”, have many commercial uses (e.g. water holding property for frozen foods, syrups, and frozen deserts; gelling property for instant puddings and dessert gels, or even explosives; emulsifying properties for polishes; stabilizing properties in ceramics, welding rods and cleaners). The well-known algal genus Sargassum belongs to the order Fucales which and have shown good capacity for metal binding. Brown algae are multicellular and occur almost exclusively in the sea. Most of the conspicuous seaweeds that are brown to olive green in color are assigned to this division. The main storage product is laminarin, similar to chrysolaminarin in structure. The algal cell wall, similar to the fungal cell wall in structure, is made of multi-layered microfibrillar framework generally consisting cellulose and interspersed with amorphous material. The algal cell wall is complex, and even more than ten layers can be found in certain kind of algal cell wall. The microfibrils can be organized in parallel or randomly. The amorphous embedding matrix consists of glycoproteins. The cellulous composted 90% of the algal cell wall. The algal cells covered by mucilaginous layers bind metal due to the presence of uronic acids (Remacle, 1990). The schematic cell wall structure of brown algae, and its composition could referees to the review written by Davis et al. (2003c). The cell wall of algae is composed of at least two different layers. The innermost layer consists of a microfibrillar skeleton, and the outer layer is an amorphous embedding matrix, which does not penetrate the fibers, but rather is attached to this layer via hydrogen bonds. The inner layer of brown algae is mainly comprised of the uncharged cellulose polymer (β-1,4-linked unbranched glucan). Two other fibrillar molecules, xylan (principally β-1,3-linked D-xylose) and mannan (β-1,4-linked -linked D-mannose) occur in the red and green algae. Alginate contributes to the strength and flexibility to the cell wall of brown algae. Cellulose remains the principal structural component even if alginate occurs in the inner layer. Fucoidan is present not only in the matrix but also within the inner cell wall. Structures of algal cellulose, xylan, manna, fucoidan and alginate were illustrated in the review (Davis et al., 2003c). The molecular structure of cellulose as a carbohydrate polymer comprises of repeating β-D-glucopyranose units which are covalently linked through acetal functions between the OH group of the C4 and C1 carbon atoms (β-1,4-glucan). Cellulose is a large, linear-chain polymer with a large number of hydroxyl groups (three per anhydroglucose (AGU) unit) and present in the preferred 4C1 conformation. To accommodate the preferred bond angles, every second AGU unit is rotated 180° in the plane. The length of the polymeric cellulose chain depends on the number of constituent AGU units (degree of polymerisation, DP) and varies with the origin and treatment of the cellulose raw material. Cellulose has a ribbon shape allowing it to twist and bend in the direction out of the plane, thus making the

205

molecule moderately flexible. There is a relatively strong interaction between neighbouring cellulose molecules in dry fibres due to the presence of the hydroxyl (–OH) groups, which stick out from the chain and form intermolecular hydrogen bonds. Regenerated fibres from cellulose contain 250–500 repeating units per chain. Cellulose is hydrophilicity, chirality and degradability. Chemical reactivity is largely due to the high donor reactivity of the OH groups (O'Connell et al., 2008). 2.4. Functional groups related to the biosorption According to the metal classification by Pearson (1963) as well as by Nieboer and Richardson (1980), metal affinity for ligands is supposed and illustrated in Table 4 (Remacle, 1990). The symbol R represents an alkyl radical such as CH2−, CH3CH2−, etc. Class A metal ions preferred to bind the ligands of I through oxygen. Class B metal ions show high affinity for III types of ligands, but also form strong binding with the ligands with II types of ligands. Borderline metal ions could bind these three types of ligands with different preferences.

Table 5 The representative functional groups and classes of organic compounds in biomass

Source: Talaro and Talaro, 2002:38.

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J.L. Wang, C. Chen / Biotechnology Advances 27 (2009) 195–226 Table 6 (continued)

Table 6 Bacterial biomass used for metal removal (mg g− 1) Metal ions

Bacteria species

Biosorption capacity

References

Pb Pb

Bacillus sp. Bacillus firmus

92.3 467

Pb Pb Pb Pb Pb Pb Pb Zn Zn

Corynebacterium glutamicum Enterobacter sp. Pseudomonas aeruginosa Pseudomonas aeruginosa Pseudomonas putida Pseudomonas putida Streptomyces rimosus Streptomyces rimosus Bacillus firmus

567.7 50.9 79.5 0.7 270.4 56.2 135.0 30 418

Zn

Aphanothece halophytica

133.0

Zn Zn Zn Zn Zn

Pseudomonas putida Pseudomonas putida Streptomyces rimosus Streptomyces rimosus Streptoverticillium cinnamoneum

6.9 17.7 30.0 80.0 21.3

Zn Zn Cu

Thiobacillus ferrooxidans Thiobacillus ferrooxidans Bacillus firmus

82.6 172.4 381

Cu Cu Cu Cu Cu Cu Cu Cu Cu Cu Cu Cu Cu Cu Cd Cd Cd Cd Cd Cd Cd Cd Cd Cd Fe(III) Cr(IV) Cr(IV) Cr(IV) Cr(IV) Cr(IV) Cr(IV) Cr(IV) Cr(IV) Cr(IV) Cr(IV) Fe Ni

Bacillus sp. Bacillus subtilis Enterobacter sp. Micrococcus luteus Pseudomonas aeruginosa Pseudomonas cepacia Pseudomonas putida Pseudomonas putida Pseudomonas putida Pseudomonas stutzeri Sphaerotilus natans Sphaerotilus natans Streptomyces coelicolor Thiobacillus ferrooxidans a Ochrobactrum anthropi Sphingomonas paucimobilis Aeromonas caviae Enterobacter sp. Pseudomonas aeruginosa Pseudomonas putida Pseudomonas sp. Staphylococcus xylosus Streptomyces pimprina Streptomyces rimosus Streptomyces rimosus Bacillus coagulans Bacillus megaterium Zoogloea ramigera Aeromonas caviae Bacillus coagulans Bacillus licheniformis Bacillus megaterium Bacillus thuringiensis Pseudomonas sp. Staphylococcus xylosus Bacillus sp. Bacillus thuringiensis Streptomyces rimosus Desulfovibrio desulfuricans Desulfovibrio fructosivorans Desulfovibrio vulgaris Desulfovibrio desulfuricans Desulfovibrio fructosivorans Desulfovibrio vulgaris Arthrobacter nicotianae Bacillus licheniformis Bacillus megaterium Bacillus subtilis Corynebacterium equi Corynebacterium glutamicum

16.3 20.8 32.5 33.5 23.1 65.3 6.6 96.9 15.8 22.9 60 5.4 66.7 39.8 – – 155.3 46.2 42.4 8.0 278.0 250.0 30.4 64.9 122.0 39.9 30.7 2 284.4 39.9 69.4 30.7 83.3 95.0 143.0

Tunali et al. (2006) Salehizadeh and Shojaosadati (2003) Choi and Yun (2004) Lu et al. (2006) Chang et al. (1997) Lin and Lai (2006) Uslu and Tanyol (2006) Pardo et al. (2003) Selatnia et al. (2004c) Mameri et al. (1999) Salehizadeh and Shojaosadati (2003) Incharoensakdi and Kitjaharn (2002) Pardo et al. (2003) Chen et al. (2005) Mameri et al. (1999) Mameri et al. (1999) Puranik and Paknikar (1997) Celaya et al. (2000) Liu et al. (2004) Salehizadeh and Shojaosadati (2003) Tunali et al. (2006) Nakajima et al. (2001) Lu et al. (2006) Nakajima et al. (2001) Chang et al. (1997) Savvaidis et al. (2003) Pardo et al. (2003) Uslu and Tanyol (2006) Chen et al. (2005) Nakajima et al. (2001) Beolchini et al. (2006) Beolchini et al. (2006) Ozturk et al. (2004) Liu et al. (2004) Ozdemir et al. (2003) Tangaromsuk et al. (2002) Loukidou et al. (2004) Lu et al. (2006) Chang et al. (1997) Pardo et al. (2003) Ziagova et al. (2007) Ziagova et al. (2007) Puranik et al. (1995) Selatnia et al. (2004a) Selatnia et al. (2004b) Srinath et al. (2002) Srinath et al. (2002) Nourbakhsh et al. (1994) Loukidou et al. (2004) Srinath et al. (2002) Zhou et al. (2007) Srinath et al. (2002) Sahin and Ozturk (2005) Ziagova et al. (2007) Ziagova et al. (2007) Volesky and Holan (1995) Ozturk (2007) Selatnia et al. (2004d) de Vargas et al. (2004) de Vargas et al. (2004) de Vargas et al. (2004) de Vargas et al. (2004) de Vargas et al. (2004) de Vargas et al. (2004) Nakajima and Tsuruta (2004) Nakajima and Tsuruta (2004) Nakajima and Tsuruta (2004) Nakajima and Tsuruta (2004) Nakajima and Tsuruta (2004) Nakajima and Tsuruta (2004)

Pd

Pt

U U U U U U

45.9 32.6 128.2 119.8 106.3 62.5 32.3 40.1 68.8 45.9 37.8 52.4 21.4 5.9

Metal ions

Bacteria species

Biosorption capacity

References

U U U Th Th Th Th Th Th Th Th

Micrococcus luteus Nocardia erythropolis Zoogloea ramigera Arthrobacter nicotianae Bacillus licheniformis Bacillus megaterium Bacillus subtilis Corynebacterium equi Corynebacterium glutamicum Micrococcus luteus Zoogloea ramigera

38.8 51.2 49.7 75.9 66.1 74.0 71.9 46.9 36.2 77.0 67.8

Nakajima and Tsuruta (2004) Nakajima and Tsuruta (2004) Nakajima and Tsuruta (2004) Nakajima and Tsuruta (2004) Nakajima and Tsuruta (2004) Nakajima and Tsuruta (2004) Nakajima and Tsuruta (2004) Nakajima and Tsuruta (2004) Nakajima and Tsuruta (2004) Nakajima and Tsuruta (2004) Nakajima and Tsuruta (2004)

According to the Hard and Soft Acid Base Principle (HSAB principle), hard ions which bind F− strongly, such as Na+, Ca2+, Mg2+ 2+ − could form stable bonds with OH−, HPO2− 4 , CO3 , R–COO and fCfO, which are oxygen-containing ligands. Contrast to hard ions, soft ions, for example, heavy metal ions such as Hg2+ and Pb2+ form strong bond with CN−. R–S−, –SH−, NH−2 and imidazol, which are groups containing nitrogen and sulfur atoms. Borderline or intermediate metal ions such as Zn2+ and Co2+ are less toxic. Hard ions mainly show ionic nature of binding, whereas soft ions binding exhibit a more covalent degree (Nieboer and Richardson, 1980; Pearson, 1963; Remacle, 1990). Metal biosorption by biomass mainly depend on the components on the cell, especially through cell surface and the spatial structure of the cell wall. Peptidoglycan, teichoic acids and lipoteichoic acids are all important chemical components of bacterial surface structures. Various polysaccharides, including cellulose, chitin, alginate, glycan, etc. existed in fungi or algae cell walls, have been proved to play a very important role in metal binding. Various proteins are also proved to involve in metal binding for certain kinds of biomasses. Some functional groups have been found to bind metal ions, especially carboxyl group. There are some evidence to confirm that the O-, N-, S-, or P-containing groups participate directly in binding a certain metals. Some active sites involved in the metal uptake are determined by using techniques of titration, infra-red and Raman spectroscopy, electron dispersive spectroscopy (EDS), X-ray photoelectron spectroscopy (XPS), electron microscopy (scanning and/or transmission), nuclear magnetic resonance (NMR), X-ray diffraction analysis (XRD), XAFS (X-ray absorption fine structure spectroscopy) etc. The most important of these groups are summarized by Volesky (2007), including Carbonyl (ketone), Carboxyl, Sulfhydryl (thiol), Sulfonate, Thioether, Amine, Secondary amine, Amide, Imine, Imidazole, Phosphonate, Phosphodiester. The relevant structural formula, pKa, HSAB classification, ligand atom, as well as occurrence in selected biomolecules were offered. Table 5 offers a representative functional groups and classes of organic compounds in biomass. The symbol R is shorthand for residue, and its placement in a formula indicates that what is attached at that site varies from one compound to another, according to Talaro and Talaro (2002). 3. Bacterial biosorbents Bacteria are the most abundant and versatile of microorganisms and constitute a significant fraction of the entire living terrestrial biomass of ~ 1018 g (Mann, 1990). Early 1980, some microorganisms were found to accumulate metallic elements with high capacity (Vijayaraghavan and Yun, 2008). Some marine microorganisms enriched Pb and Cd by factors of 1.7 × 105 and 1.0 × 105 respectively, relative to the aqueous solute concentration of these elements in ocean waters (Mann, 1990). Bacteria were used as biosorbents because of their small size, their ubiquity, their ability to grow under controlled conditions, and their resilience to a wide range of environmental

J.L. Wang, C. Chen / Biotechnology Advances 27 (2009) 195–226

situations (Urrutia, 1997). Bacteria species such as Bacillus, Pseudomonas, Streptomyces, Escherichia, Micrococcus, etc, have been tested for uptake metals or organics. Table 6 summarizes some of the important results of metal biosorption using bacterial biomasses, according to some published references (Ahluwalia and Goyal, 2007; Vijayaraghavan and Yun, 2008). Metal uptake capacity is not necessarily to reach the maximum values in the application. Some uptake values were experimental uptake, and some were predicted by the Langmuir model. Table 6 also provides the basic information to evaluate the possibility of using bacterial biomass for the removal of metal ions. Bacteria may either possess the capacity for biosorption of many elements or, alternatively, depending on the species, may be element specific. It is likely that, in the future, microorganisms will be tailored for a specific element or a group of elements, using recombinant DNA technology which is based on genetic modification using endorestrictive nucleases (Mann, 1990). 4. Fungal biosorbents 4.1. Introduction Although fungi are a large and diverse group of eukaryotic microorganisms, three groups of fungi have major practical importance: the molds, yeasts and mushrooms. Filamentous fungi and yeasts have been observed in many instances to bind metallic elements. Fungi are ubiquitous in natural environments and important in industrial processes. A range of morphologies are found, from unicellular yeasts to polymorphic and filamentous fungi, many of which have complex macroscopic fruiting bodies. Their most important roles are as decomposers of organic materials, with concomitant nutrients cycling, as pathogens and symbionts of animals and plants, and as spoilage organisms of natural and synthetic materials, e.g. wood, paint, leather, food and fabrics. They are also utilized as producers of economically important substances, e.g. ethanol, citric acid, antibiotics, polysaccharides, enzymes and vitamins (Gadd, 1993). The importance of metallic ions to fungal and yeast metabolism has been known for a long time (Gadd, 1993). The presence of heavy metals affects the metabolic activities of fungal and yeast cultures, and can affect commercial fermentation processes, which created interest in relating the behavior of fungi to the presence of heavy metals. The results from such studies led to a concept of using fungi and yeasts for the removal of toxic metals (such as lead and cadmium) from wastewater and recovery of precious metals (such as gold and silver) from process waters (Kapoor and Viraraghavan, 1997a). Both living and dead fungal cells possess a remarkable ability for taking up toxic and precious metals. In the field of biosorption, the molds and yeast are of interests and many researches are reported and reviewed. The molds are filamentous fungi. The yeasts are unicellular fungi and most of them are classified with the Ascomycetes. The most important commercial yeasts are the baker's and brewer's yeasts, which are members of the genus Saccharomyces. The original habitats of these yeasts were undoubtedly fruits and fruit juices, but the commercial yeasts of today are probably quite different from wild strains because they have been greatly improved through the years by careful selection and genetic manipulation eukaryotic cells, and they are thus excellent models for the study of many important problems in eukaryotic biology. Yeast cells are much larger than bacterial cells and can be distinguished microscopically from bacteria by their size and by the obvious presence of internal cell structures, such as the nucleus (Madigan et al., 1997). Fungi and yeasts are easy to grow, produce high yields of biomass and can be manipulated genetically and morphologically. The fungal organisms are widely used in a variety of large-scale industrial

207

fermentation processes. For example, strains of Aspergillus are used in the production of ferrichrome, kojic acid, gallic acid, itaconic acid, citric acid and enzymes like amylases, glucose isomerase, pectinase, lipases and glucanases; while S. cerevisiae is used in the food and beverage industries. The biomass can be cheaply and easily procured in rather substantial quantities, also as a by-product from the established industrial fermentation processes, for the biosorption of heavy metals and radio nuclides, which made the fungi of primary interest as a raw material serving as a basis for formulating suitable biosorbents. The use of biomass as an adsorbent for heavy-metal pollution control can generate revenue for industries presently wasting the biomass and at same time ease the burden of disposal costs associated with the waste biomass produced. Alternatively, the biomass can also be grown using unsophisticated fermentation techniques and inexpensive growth media (Kapoor and Viraraghavan, 1995). It is not a priority from the economical point of view to use the waste biomass, but the fungal cultures are also amenable to genetic and morpholocial manipulations which may result in better raw biosorbents material (Volesky, 1990a). This section will review and summarize the removal of heavy metals and radio nuclides by filamentous fungi (such as Penicillium sp., Aspergillus sp., Mucor sp., Rhizopus sp.) and yeast (Saccharomyces spp.) from aqueous solutions. 4.2. Yeast The yeast biomass has been successfully used as biosorbent for removal of Ag, Au, Cd, Co, Cr, Cu, Ni, Pb, U, Th and Zn from aqueous solution. Yeasts of genera Saccharomyces, Candida, Pichia are efficient biosorbents for heavy metal ions. Most of yeasts can sorb a wide range of metal ions or be strictly specific in respect of only one metal ion. S. cerevisiae as biosorbents is of special interest (Podgorskii et al., 2004). A number of literatures have proved that S. cerevisiae can remove toxic metals, recover precious metals and clean radionuclides from aqueous solutions to various extents. The advantages of S. cerevisiae as biosorbents in metal biosorption, the forms of S. cerevisiae in biosorption research, biosorptive capacity of S. cerevisiae, the selectivity and competitive biosorption by S. cerevisiae were depicted in detail by Wang and Chen (2006). Table 7 presents some data on the biosorptive capacities of the yeast (in various forms) for different metal ions reported in literatures. Based on data presented in Table 7, the magnitude order of metal uptake capacity by S. cerevisiae can be estimated as the followings: for Lead, biosorptive capacity by S. cerevisiae is in the order of 2–3, above tenth and less than 300 mg Pb/g dry weight biomass; for copper, in the order of 1–2, less than 20 mg Cu/g dry weight yeast; for zinc, in the order of 1–2, usually less than 30 mg Zn/g dry weight; for cadmium, in the order of 2–3, usually above 10 but less than 100 mg Cd/g dry mass; for mercury, in the order of 2; for chromium and nickel, usually in the order of 1, seldom more than 40 mg/g dry mass; for precious metals, such as Ag, Pt, Pd, in the order of 2, around 50 mg/g dry weight yeast. Biosorptive capacity of radionuclide uranium by S. cerevisiae is usually between 150 and 300 mg U/g dry weight biomass. It should be noted that comparing results from different literatures involves in standardizing the different ways the sorption capacity may be expressed. At same time, metal uptake, q, should be compared in almost the same equilibrium concentration of metals in solution for the purpose of evaluating performance of the biomaterial (Kratochvil and Volesky, 1998). In particular, there is no standard measurement of dry weight of biomass, i.e. no standard of dry temperature and dry hours when drying biomass. Park et al. (2003) obtained the dry-cell weight by drying cells at 70 °C until the weight of the cells became constant. Ozer and Ozer (2003) dried the yeast at 100 °C for 24 h. Obviously, the numeric value of dry weight of biomass obtained in different drying conditions is sure to be different. Hence, attention should be paid to these conditions when comparing the different results.

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J.L. Wang, C. Chen / Biotechnology Advances 27 (2009) 195–226

Table 7 Biosorption by Saccharomyces cerevisiae (mg g− 1) Metal ions

Source or form of biosorbents

Biosorption capacitya

References

Pb Pb Pb Pb Pb Cu Cu Cu Cu Cu Cu Zn Zn Zn Zn Zn Zn Cd Cd Cd Cd Cd Cd Cd Hg Co Ni Ni Ni Ni Cr(VI) Cr(VI) Cr(VI) Fe Pd Pt Ag Ag 241 Am U U

Free cells Immobilized cells in a sol–gel matrix Whiskey distillery spent wash, lyophilized Lab cultivated, then dried at 100 °C Ethanol treated waste baker's yeast Adapted and growing cells Waste yeast from fermentation industry and then autoclaved at 120 °C Free cells Whiskey distillery spent wash lyophilized immobilized cells on sepiolite Waste yeast from brewery, formaldehyde cross-linked cells in column bioreactors Waste yeast from fermentation industry and then autoclaved at 120 °C Free cells Immobilized cells in a sol–gel matrix Whiskey distillery spent wash, lyophilized Immobilized cells on sepiolite Formaldehyde cross-linked cells in column bioreactors Deactivated protonated yeast from yeast co. Free cell suspended in solution Lab culture Free cell suspended in solution Lab culture Immobilized cells on sepiolite Waste yeast from brewery, formaldehyde cross-linked cells in column bioreactors Ethanol treated waste baker's yeast Non-living and resting cells from aerobic culture Free cells Free cells Waste yeast from fermentation industry and then autoclaved at 120 °C Free cells Lab cultivated, then dried at 100 °C Deactivated protonated yeast from yeast co. oven at 80 °C for 24 h Lab cultivated, dehydrated at 30 °C, 15% of cell humidity; 80.5% of the viability As a by-product from brewery, formaldehyde cross-linked cells in fixed-bed column Lab cultivated, then dried at 100 °C Whiskey distillery spent wash, lyophilized Immobilized cells of waste yeast Immobilized cells of waste yeast Whiskey distillery spent wash lyophilized Industrial strain, then lab cultivated and freeze-dried Lab cultivated, free cell Whiskey distillery spent wash lyophilized Beer yeast, 8.75 mmol UO2+ 2 /g yeast Washed and unwashed non-viable spent yeast from a company in Greece

79.2 41.9 189 270.3 17.5 2.04–9.05 4.93 6.4 5.7 4.7 8.1 3.45–1.95 23.4 35.3 16.9 8.37 7.1 9.91–86.3 35.5–58.4 14.3–20.0 10.9 14 15.6 70 64.2 9.9 1.47 8 46.3 11.4 About 5.5 6.3 32.6 16.8 40.6 44 59 41.7 7.45–1880.0b 180 2082.5c 360–150 150 63

Al-Saraj et al. (1999) Al-Saraj et al. (1999) Bustard and McHale (1998) Ozer and Ozer (2003) Goksungur et al. (2005) Donmez and Aksu, (1999) Bakkaloglu et al. (1998) Al-Saraj et al. (1999) Bustard and McHale (1998) Bag et al. (1999a) Zhao and Duncan (1997) Bakkaloglu et al. (1998) Al-Saraj et al. (1999) Al-Saraj et al. (1999) Bustard and McHale (1998) Bag et al. (1999a) Zhao and Duncan (1997) Vasudevan et al. (2003) Park et al. (2003) Park et al. (2003) Bag et al. (1999a) Zhao and Duncan (1997) Goksungur et al. (2005) Volesky et al. (1993) Al-Saraj et al. (1999) Al-Saraj et al. (1999) Bakkaloglu et al. (1998) Al-Saraj et al. (1999) Ozer and Ozer (2003) Padmavathy et al. (2003) Rapoport and Muter (1995) Zhao and Duncan (1998) Ozer and Ozer (2003) Bustard and McHale (1998) Xie et al. (2003a) Xie et al. (2003b) Bustard and McHale (1998) Simmons and Singleton (1996) Liu et al. (2002) Bustard and McHale (1998) Popa et al. (2003) Riordan et al. (1997) Tsezos (1997) Tsezos (1997)

U Th a b c

Metal sorption is not necessarily maximum. Unit: μg U g− 1. −1 The value calculated by converting the data 8.75 mmol UO2+ yeast. 2 g

4.3. Filamentous fungi This section will review the removal of heavy metal ions and radionuclides by filamentous fungi (such as Penicillium spp., Aspergillus spp., Rhizopus spp. and white rot fungi) from aqueous solutions. Different species of Penicillium, under some circumstances, also Aspergillus, have been reported as good biosorbents of metal ions. The genus Rhizopus, such as R. arrhizus and Rhizopus javanicus, has been discovered to owe the relatively good-sequestering properties (Volesky, 1990a). Table 8 summarizes some of the important results of metal biosorption using fungal biomasses. 4.3.1. Penicillium Penicillium can remove a variety of heavy metal ions from aqueous solutions, such as Cu, Au, Zn, Cd, Mn, U and Th, see Table 9. Penicillium italicum (Mendil et al., 2008), Penicillium spinulosum, Penicillium oxalicum (Svecova et al., 2006) Penicillium austurianum (Awofolu et al., 2006), Penicillium verrucosum (Cabuk et al., 2005), Penicillium purpurogenum (Say et al., 2003a), Penicillium canescens (Say et al., 2003b), Penicillium griseofulvum (Shah et al., 1999), P. austurianum (Rostami and Joodaki, 2002), Penicillium chrysogenum, etc. were

Table 8 Biosorption by fungal biomass (mg g− 1) Species of fungi

Metal ions

References

Aspergillus niger, Mucor rouxii, Rhizopus arrhizus (living cells) Penicillium spp. (living cells)

Au

Kapoor and Viraraghavan (1997a)

Ag Cu

Cd Pb Penicillium, Aspergillus, Trichoderma, Rhizopus, Mucor, Pb Saccharomyces, Fusarium (living cells) Cu Cd Zn Aspergillus, Penicillium, Rhizopus, Saccharomyces, Th Trichoderma, Mucor, Rhizopus (living cells) U Sr Cs La Phanerochaete chryosporium (living cells) Cd Pb Cu

Kapoor and Viraraghavan (1997a)

Kapoor and Viraraghavan (1997a)

Kapoor and Viraraghavan (1997a)

Day et al. (2001)

J.L. Wang, C. Chen / Biotechnology Advances 27 (2009) 195–226 Table 9 (continued)

Table 9 Biosorption by Penicillium sp. (mg g− 1) Species

Metal ions

Biosorption capacity

References

Penicillium canescens Penicillium canescens Penicillium canescens Penicillium canescens Penicillium chrysogenum Penicillium chrysogenum Penicillium chrysogenum Penicillium chrysogenum Penicillium chrysogenum Penicillium chrysogenum Penicillium chrysogenum Penicillium chrysogenum (surface imprinted) Penicillium chrysogenum (waste biomass) Penicillium chrysogenum Penicillium chrysogenum (modified) Penicillium chrysogenum (modified) Penicillium chrysogenum (modified) Penicillium chrysogenum (modified) Penicillium chrysogenum (modified) Penicillium chrysogenum (modified) Penicillium chrysogenum (raw) Penicillium chrysogenum (raw) Penicillium chrysogenum (raw) Penicillium chrysogenum (Alkaline pretreatment) Penicillium chrysogenum (Alkaline pretreatment) Penicillium chrysogenum (Alkaline pretreatment) Penicillium chrysogenum Penicillium chrysogenum Penicillium chrysogenum Penicillium chrysogenum Penicillium chrysogenum Penicillium chrysogenum Penicillium chrysogenum

Cd Pb Hg As(III) Cd Cu Pb Cd Cd Th Zn Ni

102.7 213.2 54.8 26.4 11 9 116 56 39 – 6.5 82.5

Say et al. (2003b) Say et al. (2003b) Say et al. (2003b) Say et al. (2003b) Niu et al. (1993) Niu et al. (1993) Niu et al. (1993) Holan and Volesky (1995) Fourest et al. (1994) Gadd and White (1992) Niu et al. (1993) Su et al. (2006)

Ni

56.2

Su et al. (2006)

Cr(VI) Cd

– 210.2

Park et al. (2005) Deng and Ting (2005b)

Cu

108.3

Deng and Ting (2005b)

Cu

92

Deng and Ting (2005a)

Pb

204

Deng and Ting (2005a)

Ni

55

Deng and Ting (2005a)

Ni

260

Tan et al. (2004)

Cr(III) Ni Zn Cr(III)

18.6 13.2 6.8 27.2

Tan and Tan and Tan and Tan and

Ni

19.2

Tan and Cheng (2003)

Zn

25.5

Tan and Cheng (2003)

Cd Pb Cd Zn Cu Pb Th

56 96 21.5 13 11.7 116 150

Penicillium chrysogenum

Th

142

Penicillium chrysogenum

Pb

116

Penicillium chrysogenum

U

70

Penicillium digitatum

Ni, Zn, Cd, Pb

–

Penicillium digitatum

Cd

3.5

Holan and Volesky (1995) Skowronski et al. (2001) Skowronski et al. (2001) Skowronski et al. (2001) Skowronski et al. (2001) Niu et al. (1993) Veglio and Beolchini (1997) Kapoor and Viraraghavan (1995) Kapoor and Viraraghavan (1995) Kapoor and Viraraghavan (1995) Kapoor and Viraraghavan (1995) Veglio and Beolchini (1997)

Pb Cu

5.5 20.47

Cu Cu, Th, Zn

1.51 –

Penicillium italicum

Cu

0.4–2

Penicillium italicum

Zn

0.2

Penicillium notatum

Cu

80

Penicillium notatum

Zn

23

Penicillium notatum

Cd

5.0

Penicillium janthinellum

U

52.7

Penicillium purpurogenum Penicillium purpurogenum

Cr(VI) Cd

36.5 110.4

Penicillium griseofulvum (immobilized) Penicillium griseofulvum (free) Penicillium italicum

209

Cheng Cheng Cheng Cheng

(2003) (2003) (2003) (2003)

Shah et al. (1999) Shah et al. (1999) Ahluwalia and Goyal (2007) Ahluwalia and Goyal (2007) Ahluwalia and Goyal (2007) Kapoor and Viraraghavan (1995) Kapoor and Viraraghavan (1995) Kapoor and Viraraghavan (1995) Kapoor and Viraraghavan (1995) Say et al. (2004) Say et al. (2003a) (continued on next page)

Species

Metal ions

Biosorption capacity

References

Penicillium purpurogenum Penicillium purpurogenum Penicillium purpurogenum Penicillium simplicissimum

Pb Hg As Pb Cu Cd

252.8 70.4 35.6 298.01 207.68 1.5

Say et al. (2003a) Say et al. (2003a) Say et al. (2003a) Xu et al. (2008)

Cd

0.4

Cu

2.4

Cu

3.6

Zn

1.3

Zn

0.2

Cd Al

84.5 50

Penicillium sp.

Sn Pb U

60 5.0 1.4

Penicillium spp.

Pb

6.0

Penicillium spp.

Cu

3

Penicillium spp.

Cd

3

Penicillium spp.

U

165

Penicillium spp.

Sr

75

Penicillium sp.

Nd

178

Penicillium spinulosum (Non-growing) Penicillium spinulosum (Growing, mid-linear phase) Penicillium spinulosum (Non-growing) Penicillium spinulosum (Growing, lag period) Penicillium spinulosum (Non-growing) Penicillium spinulosum (Growing, mid-linear phase) Penicillium spinulosum Penicillium sp.

Kapoor and Viraraghavan (1995) Kapoor and Viraraghavan (1995) Kapoor and Viraraghavan (1995) Kapoor and Viraraghavan (1995) Kapoor and Viraraghavan (1995) Kapoor and Viraraghavan (1995) Gabriel et al. (1996) Kapoor and Viraraghavan (1995)

Kapoor and Viraraghavan (1995) Kapoor and Viraraghavan (1997a) Kapoor and Viraraghavan (1997a) Kapoor and Viraraghavan (1997a) Kapoor and Viraraghavan (1997a) Kapoor and Viraraghavan (1997a) Palmieri et al. (2000)

reported to adsorb various metals. For example, P. chrysogenum can extract gold from a cyanide solution. However, the biosorption capacity was not encouraging (Vieira and Volesky, 2000). P. spinulosum was reported to be capable of removing Cu, Au, Zn, Cd, Mn (Kapoor and Viraraghavan, 1995). Among these Penicillium sp., P. chrysogenum was studied most. The P. chrysogenum, a semi-known strains Hyphomycetes gang door Hyphomycetes Head (Cong stems Species) CONG stems Branch Penicillium spores of fungi. Classified asymmetry Penicillium group, cashmere-like Penicillium Asian group, the middle P. chrysogenum and it is typical of penicillin-producing bacteria. Fungi have smooth surface, 150–350 μm long, 3 to 3.5 μm wide, 2–3 branches, they are brush sticks asymmetry, ranging from the length of the vice sticks, based on the growing stems and small stems. Conidia is oval, (2–4) μm × (2.8–3.5) μm. They grow faster, round, tight cashmere-like or slightly tempered, blue and green (white edge), a radial grooving on the surface, often yellow-colored droplets exudative. Bright yellow colony back to a dark brown and yellow-soluble spread to the medium. They are widely distributed in the air, soil and organic matters on biodeterioration. Penicillinum is famous for organics production, which can produce organic acids, such as glucose acid, citric acid, as well as glucose oxidase (http:// www.chemyq.com/En/xz/xz4/39623ajqia.htm). P. chrysogenum exhibited preferential sorption orders: Pb2+ N Cu2+ N Zn2+ N Cd2+ N Ni2+ N Co2+ (Puranik and Paknikar, 1999). For non-living P. chrysogenum: Pb2+ N Cd2+ N Cu2+ N Zn2+ N As3+. P. canescens exhibited the same sorption orders: Pb(II) N Cd(II) N Hg(II) N As(III) at non-competitive conditions or competitive conditions. At non-competitive conditions, metal uptake capacity of P. canescens were 26.4 mg/g for As(III), 54.8 mg/g for Hg(II), 102.7 mg/g for Cd(II) and 213.2 mg/g for Pb(II), respectively. However, competitive adsorption capacity for the heavy metal ions were 2.0 mg/g for As(III), 5.8 mg/g for Hg(II), 11.7 mg/g for Cd(II) and

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32.1 mg/g for Pb(II), respectively, when the initial concentration of the metal ions was 50 mg L− 1. The species of Pencillium biosorption seems to be only sorbing well for uranium and lead (Volesky and Holan, 1995). However, the genera Rhizopus and Penicillium have already been studied as potential biomass for the removal of heavy metals from aqueous solutions (Kapoor et al., 1999). 4.3.2. Aspergillus Aspergillus niger is an important microorganism in biotechnological applications (Bapat et al., 2003). It has been used to produce extracellular enzymes such as glucoamylas, pectinase, acidic lipase, feruloyl esterase, and xylanase and organic acids such as gluconic acid and citric acid. Citric acid and several enzymes produced by A. niger are considered GRAS (generally regarded as safe) by the United States Food and Drug Administration. In addition, A. niger is also used in biotransformation of ferrulic acid, progesterone, diperpenoid, isosteviol, terpene, linaloo, gereniol, nirol, and citral. In the last two decades, A. niger has been developed as an important transformation

host to overexpress food enzymes. A. niger is also ecologically important in biodegradation of toxic chemicals such as hexadecane, treatment of waste beet molasses and olive mill waste, and bioconversion of wastewater sludge. Waste biomass of A. niger from fermentative industry, is used to remove hazardous heavy metal ions, such as cadmium, lead, chromium, and copper from aqueous solution. As it produces organic acids, A. niger can be used to bioleach metals from mining ores. Table 10 showed that various metal ions could be removed by A. niger. Fungus A. niger 405 showed a good affinity for binding Cu2+, Zn2+ and 2+ Ni ions in single composition system, while in multi-component solution it occurred only for copper and zinc (Filipovic-Kovacevic et al., 2000). A waste fungal biomass containing killed cells of A. niger was efficiently used for the removal of toxic metal ions such as nickel, calcium, iron and chromium from aqueous solution. The adsorption capacity for various metal ions could be arranged as Ca N Cr (III) N Ni N Fe N Cr (VI) (Natarajan et al., 1999).

Table 10 Biosorption by Aspergillus sp. (mg g− 1) Species Aspergillus Aspergillus Aspergillus Aspergillus Aspergillus Aspergillus Aspergillus Aspergillus Aspergillus Aspergillus Aspergillus Aspergillus Aspergillus Aspergillus Aspergillus Aspergillus Aspergillus Aspergillus Aspergillus Aspergillus Aspergillus Aspergillus Aspergillus Aspergillus Aspergillus Aspergillus Aspergillus Aspergillus Aspergillus Aspergillus Aspergillus Aspergillus Aspergillus Aspergillus Aspergillus Aspergillus Aspergillus Aspergillus Aspergillus Aspergillus Aspergillus Aspergillus Aspergillus Aspergillus Aspergillus Aspergillus Aspergillus Aspergillus Aspergillus Aspergillus Aspergillus Aspergillus

niger (pretreated with NaOH) niger (pretreated with NaOH) niger (pretreated with NaOH) niger (pretreated with NaOH) niger (growing) niger (growing) niger (spore) niger (hyphae) niger niger niger niger niger niger niger niger niger niger niger niger niger niger niger niger niger (live) niger (live) niger (live) niger (live) niger (NaOH pretreated) niger (NaOH pretreated) niger (NaOH pretreated) niger (NaOH pretreated) niger niger niger (attached to wheat bran) niger niger niger carbonarius flavus flavus fumigatus fumigatus nidulans terreus (mycelial waste) terreus terreus (immobilized in polyurethane foam) terreus (immobilized in polyurethane foam) terreus (immobilized in polyurethane foam) terreus awamori oryzae

Metal ions

Biosorption capacity (mg/g)

References

Cu Pb Cu Pb Cu Pb

28.7 32.6 25.5 28.9 15.6 34.4 7.2–142.4 MBq/g 5.2–106.5 MBq/g 93 –

Dursun (2006) Dursun (2006) Dursun (2003) Dursun (2003) Dursun et al. (2003a) Dursun et al. (2003a) Yang et al. (2004) Yang et al. (2004) Spanelova et al. (2003) Karunasagar et al. (2003) Goyal et al. (2003) Dursun et al. (2003b) Basumajumdar et al. (2003) Barros et al. (2003) Rajendran et al. (2002) Magyarosy et al. (2002) Bhattacharyya et al. (2002) Price et al. (2001) Bag et al. (2001) Bag et al. (1999b) Filipovic-Kovacevic et al. (2000) Rosa et al. (1999) Natarajan et al. (1999) Lyalikova-Medvedeva and Khijniak (1999) Kapoor et al. (1999) Kapoor et al. (1999) Kapoor et al. (1999) Kapoor et al. (1999) Kapoor et al. (1999) Kapoor et al. (1999) Kapoor et al. (1999) Kapoor et al. (1999) Gomes et al. (1999) Kapoor and Viraraghavan (1997b) Modak et al. (1996)

241 241

Am Am

Pb Hg2+, CH3Hg+ Cr(VI), Fe(III) Cu(II) Cd Cd Ni Ni Ph, Cd, Ni, Cr Cu, Zn Fe(II), Fe(III) Cu, Zn, Fe, Ni, Cd Cu, Zn, Ni, Cr(VI) Free Cd and complexed Cd Ni, Ca, Fe, Cr Tc, U, Am, Ce, Cs, Eu, Pa, Sb Pb Cd Cu Ni Pb Cd Cu Ni Cyano-metal complexes (Au, Ag. Cu, Fe, Zn) Pb, Cd, Cu Cu, Zn Cd, Cu, Zn, Ni, Co Ag Th Cu, Cr U, Th Au, Ag, Cu U Au, Ag, Cu Zn Cu Cd Fe Cr Ni Cu Cu Cu, Cd, Zn

9.53 – – – –

2.25 1.31 0.75 1.75 7.24 3.43 2.66 0.96

160–180 164.5 96.5 19.6 224

Akthar et al. (1995) Gadd and White (1992) Alasheh and Duvnjak (1995) Hafez et al. (1997) Gomes and Linardi (1996) Bhainsa and D'Souza (1999) Gomes and Linardi (1996) Zhou (1999) Gulati et al. (2002) Massaccesi et al. (2002) Dias et al. (2002) Dias et al. (2002) Dias et al. (2002) Gulati et al. (1999) Tsekova et al. (2000) Vianna et al. (2000)

J.L. Wang, C. Chen / Biotechnology Advances 27 (2009) 195–226

Non-living waste biomass consisting of A. niger attached to wheat bran was used as a biosorbent for the removal of copper and zinc from aqueous solution. The biosorption of copper and zinc conformed to the Langmuir isotherm. The binding capacity of the biomass for copper was found to be higher than that for zinc. The metal uptake capacity, expressed in milligrams per gram of biomass, was found to be dependent upon the following factors: the initial metal concentration (with the uptake capacity decreasing with increasing initial concentration), the biomass loading (with the uptake capacity decreasing with increasing biomass loading) and pH (with the uptake capacity increasing with increasing pH in the range of 1.5 to 6.0). The metal uptake capacity was significantly affected in the presence of the co-existed ions. The uptake capacity of copper decreased in the presence of zinc and vice versa. The decrease in metal uptake capacity was dependent on the concentration of metal ions in the two-component aqueous solution. The effect of copper on zinc uptake was more pronounced than the effect of zinc on copper uptake (Modak et al., 1996). 4.3.3. Other fungi The cell wall of R. arrhizus involves a high content of chitin. The ability of chitin to complex metal ions has been confirmed (Dursun et al., 2003b). Viable R. arrhizus and A. niger could remove Cu(II) with the maximum specific uptake capacity of 10.76 and 9.53 mg g− 1 at 75 mg L− 1 of initial Cu(II) concentration (Dursun et al., 2003b). Of the six species of inactivated fungal mycelia, R. arrhizus, Mucor racemosus, Mycotypha africana, Aspergillus nidulans, A. niger and Schizosaccharomyces pombe, R. arrhizus exhibited the highest capacity (qmax = 213 μmol g− 1). Further experiments with different cellular fractions of R. arrhizus showed that Zn was predominantly bound to cell-wall chitin and chitosan (qmax = 312 μmol g− 1). R. arrhizus were reported to adsorb Th (Gadd and White, 1992), Pb (Naja et al., 2005), Ph, Cd, Ni, Cr (Bhattacharyya et al., 2002). Brady and Tobin (1995) investigated the freeze-dried R. arrhizus biomass for its potential to adsorb the hard metal ion Sr2+ and the borderline metal ions Mn2+, Zn2+, Cd2+, Cu2+, and Pb2+ from aqueous solutions. Biosorption of metal ions, such as Li+, Ag+, Pb2+, Cd2+, Ni2+, Zn2+, Cu2+, 2+ Sr , Fe2+, Fe3+, Al3+ by Rhizopus nigricans biomass was studied, with the maximum biosorption capacity for the individual metal ions were in the range from 160 to 460 μmol g− 1 (Kogej and Pavko, 2001). The live and dead white-rot fungus Trametes versicolor entrapped in Ca-alginate beads were able to adsorb Cd(II). The maximum experimental biosorption capacity was 102.3 ± 3.2 and 120.6 ± 3.8 mg g− 1, respectively (Arica et al., 2001). A white rot fungus species Lentinus sajorcaju biomass was entrapped into alginate gel via a liquid curing method in the presence of Ca(II) ions. The maximum experimental biosorption capacity for entrapped live and dead fungal mycelia of L. sajurcaju were found to be 104.8 ± 2.7 mg Cd(II) g− 1 and 123.5 ± 4.3 mg Cd(II) g− 1, respectively (Bayramoglu et al., 2002). 4.4. Selectivity and competitive biosorption by fungi Native fungal biomass, such as Absidia orchidis, P. chrysogenum, R. arrhizus, R. nigricans, and modified spruce sawdust (Picea engelmanii) was used to adsorb heavy metal ions, the results indicated that the biosorption capacity of these fungal biomasses was in the following order: Pb N Cd N Ni (Holan and Volesky, 1995). P. canescens at competitive or noncompetitive conditions exhibited the same preferential order: Pb(II) N Cd(II) N Hg(II) N As(III). At noncompetitive conditions, the sorption capacity was 26.4 mg/g for As (III), 54.8 mg/g for Hg(II), 102.7 mg/g for Cd(II) and 213.2 mg/g for Pb (II), respectively. The competitive adsorption capacity for the heavy metal ions were 2.0 mg/g for As(III), 5.8 mg/g for Hg(II), 11.7 mg/g for Cd(II) and 32.1 mg/g for Pb(II), respectively, when the initial concentration of the metal ions was 50 mg L− 1(Say et al., 2003b). Sag (2001) compared the biosorption performance of heavy metal ions by various free and immobilized fungal cells in different reactor

211

systems. Although the results from the different authors cannot be compared directly, some qualitative conclusions can be draw from these data, the order of sorption capacity was as follows: Cd N Co N Cr N Au ≈ Cu N Fe N Ni N Th N U N Pb N Hg N Zn. Aspergillus seems to have better sorption capacity for Au, Co, Th, Zn. Penicillium is excellent biosorbent for Cd, Fe, Pb, Th, U, Zn. As seen from Tables 9 and 10, Cu(II) is one of the most studied metal ions due to its biological functions: it is an essential micronutrient for most living organisms but is toxic when in excess. A wide variety of free- and immobilized-, treated- and untreated-fungal biomasses have been used for Cu biosorption in different reactor systems and a wide range of capacities observed, with the uptake capacity from 1.015 mmol g− 1 for Ganoderma lucidum to 0.012 mmol g− 1 for A. oryzae. The Cu(II) biosorption capacity of R. arrhizus has been found to be 0.301, 0.353, 0.738, 0.754 mmol g− 1, respectively, in batch stirred tank reactor (BSTR), continuous-flow stirred-tank (CFST) contactor, batch stirred-tank reactors in series (BSTRS) (three reactor was used in series), packed column (or fixed bed) reactor (PCR), which were operated at exactly same conditions (Sag, 2001). The selectivity and competitive biosorption by S. cerevisiae could refer to our previous review paper (Wang and Chen, 2006). 4.5. Comparison of fungi and yeast with other biosorbents We introduced some studies and results of biosorption of heavy metals by S. cerevisiae (Wang and Chen, 2006). Table 11 represents a part of comparative results of metal uptake capacity between S. cerevisiae and other biosorbents. Bakkaloglu et al. (1998) compared the various types of waste biomass including bacteria (S. rimosus), yeast (S. cerevisiae), fungi (P. chrysogenum), activated sludge as well as marine algae (F. vesiculosus and A. nodosum) for removal of zinc, copper and nickel ions, especially their removal efficiency in the biosorption, sedimentation and desorption stages. The results showed that S. cerevisiae has the mediocre efficiency for one- or multi-metal biosorption systems. By comparing the index qmax obtained by the Langmuir equation with seven types of waste biomass, taking lead ion as example, Kogej and Pavko (2001) indicated that the lead uptake capacity of S. cerevisiae is in the middle in comparison with other six biosorbents. Vianna et al. (2000) studied the capability for the adsorption of Cu, Cd and Zn by three kinds of waste biomass from fermentation industries, that is, Bacillus lentus, Aspergillus oryzae and S. cerevisiae. The results showed that protonated B. lentus had the highest sorption capacity for Cu and Cd, followed by protonated A. oryzae and S. cerevisiae biomass. Donmez and Aksu (1999) studied the copper ion bioaccumulation by adapted and growing cells of S. cerevisiae, Kluyceromyces marxianus, S. pombe and Candida sp. They found that the biosorptive capacity for Cu2+ decreased in the following

Table 11 The comparison of different biosorbents with Saccharomyces cerevisiae (mg g− 1) Metal ions

Biosorptive capacity (mg metal/g dry weight biomass)

References

Zn

A.nodosum (25.6) N P. chrysogenum N (19.2) N F. vesiculosus (17.3) N Activated sludge(9.7) N S. rimosus(6.63) N Saccharomyces cerevisiae (3.45) S. rimosus(9.07) N P. chrysogenum(8.62) N F. vesiculosus (7.37) N Activated sluge(5.54) N Saccharomyces cerevisiae (4.93) N A.nodosum(4.89) F. vesiculosus(2.85) N S. rimosus(1.63) N Saccharomyces cerevisiae(1.47) N A. nodosum(1.11) Phanerochaete chrysosporium(419.4) N R. nigricans(403.2) N M. purpurea(279.5) N S. cerevisiae(211.2) N A. terreus(201.1) N M. inyoensis(159.2) N Streptomyces clavulgerus(140.2) Protonated biomass: Bacillus lentus (≈30) N Aspergillus oryzae N S. cerevisiae (b 5) Growing cells: S. cerevisiae (7.11) N K. Marxianus (6.44) N Candida sp. (4.80) N S. pombe (1.27).

Bakkaloglu et al. (1998)

Cu

Ni Pb

Cd, Cu Cu

Bakkaloglu et al. (1998) Bakkaloglu et al. (1998) Kogej and Pavko (2001) Vianna et al. (2000) Donmez and Aksu (1999)

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order: S. cerevisiae (7.11) N K. Marxianus (6.44) N Candida sp. (4.80) N S. pombe (1.27). However, Candida sp. and K. marxianus have been found to be more efficient than S. cerevisiae and S. pombe in heavy metal resistance and copper(II) bioaccumulation at higher copper (II) concentrations. Compared with the excellent biosorbent of fungi Rhizopus for lead, cadmium, copper, zinc, and uranium, the common yeast S. cerevisiae is regarded as a ‘mediocre’ metal biosorbent (Volesky, 1994). The biosorption capacity of cadmium by S. cerevisiae was observed to be higher in comparison with that of other adsorbents such as aluminum oxide, activated carbon, and activated charcoal (Kapoor and Viraraghavan, 1997a). In spite of the mediocre metal uptake capacity comparing with other fungi biosorbents, S. cerevisiae is a unique biomaterial in biosorption research and application. It has long been and continues to be paid much attention. The metal uptake capacity of Cr(VI) is found to decrease in the order R. nigricans N R. arrhizus N A. oryzae N A. niger (Bai and Abraham, 1998). Three by-products of fermentation, containing the biomass of B. lentus, A. oryzae or S. cerevisiae were tested for the capacity to absorb Cu, Cd and Zn (Vianna et al., 2000). The composition of the three biomasses was first determined and showed high contents of ashes in both B. lentus and A. oryzae biomass and high amounts of lipids in the bacterial biomass. Metal ion binding experiments were performed by contact of 0.1 g of biomass (protonated for all the metal tests and not protonated only for the Cd test) with 50 mL of solution containing each of the metal ions in the concentration range from 10 to 500 mg/ mL, at pH 4.5, 3.5 and 2.5. The final metal ion concentrations were determined using a plasma absorption spectrometer, and the metal removal levels for isotherm plots were determined using the Langmuir model. The results showed that the protonated biomass of B. lentus had the best sorption capacity for Cu and Cd, followed by protonated A. oryzae and S. cerevisiae biomass. The sorption of Zn was low for all tested biomasses, as also was the binding of all metals at acidic pH (2.5 and 3.5). A significant increase in Cd sorption was obtained using non-protonated biomass from B. lentus and A. oryzae (Vianna et al., 2000). 5. Marine algae as biosorbents 5.1. Introduction Algae are of special interest in search for and the development of new biosorbents materials due to their high sorption capacity and their ready availability in practically unlimited quantities in the seas and oceans (Kuyicak and Volesky, 1990; Rincon et al., 2005). However, there are few publications on biosorption with algae as compared to those using other biomass (mainly fungi and bacteria), and there is still fewer for multi metallic systems (Romera et al., 2006). The topic is relatively novel, with exponential growth of interest throughout the scientific community in the last few years. According to the statistic review on biosorption, algae have been less used as biosorbent material than other kinds of biomass, especially fungi and bacteria (15.31% in the former case and 84.69% in the second) (Romera et al., 2006). 5.2. Performance From the published literatures, brown algae among the three groups of algae (red, green, brown algae) received the most attention. Higher uptake capacity has been found for brown algae than for red and green algae (Brinza et al., 2007). The reason seems to be that they offer better sorption than red or green algae (Romera et al., 2006). Researchers have employed mainly brown algae treated in different ways to improve their sorption capacity (Romera et al., 2006). Volesky and his colleagues have performed many researches on brown algae biosorption characteristics, especially Sargassum sp. (Davis et al.,

2003a,b,c, 2004; Diniz and Volesky, 2005; Volesky et al., 2003; Yun and Volesky, 2003). A review of the biochemistry of heavy metal biosorption by brown algae was published (Davis et al., 2003c). Brinza et al. (2007) reviewed some marine micro and macro algal species as biosorbents for heavy metal ions. The micro algae mentioned in the review include Chlamydomonas reinhardtii, Chlorella salina, Chlorella sorokiniana, Chlorella vulgaris, Chlorella miniata, Chlorococcum sp, Cyclotella cryptica, Lyngbya taylorii, Phaeodactylum tricornutum, Porphyridium purpureum, Scenedesmus abundans, Scenedesmus quadricauda, Scenedesmus subspicatus, Spirogyra sp., Spirulina platensis, Stichococcus bacillaris and Stigeoclonium tenue. The macro algae mentioned in the review include Ascophyllum nodosum, Ascophyllum sp., Cladophora crispata, Cladophora fascicularis, Codium fragile, Colpomenia sinuosa, Corallina officinalis, Ecklonia sp., Fucus vesiculosus, Fucus ceranoides, Fucus serratus, Fucus spiralis, Gracilaria fischeri, Gracilaria sp., F. spiralis, G. fischeri, Gracilaria sp., Jania rubrens, Laminaria digitata, Laminaria japonica, Laurencia obtuse, Padina pavonia, Padina sp., Palmaria palmata, Petalonia fascia, Pilayella littoralis, Porphyra columbina, Sargassum asperifolium, Sargassum hemiphyllum, Sargassum hystrix, Sargassum natans, Sargassum sp., Sargassum sp., Sargassum vulgaris, Sargassum kjellmanianum, Turbinaria conoides, Ulva fascia, Ulva reticulata, Ulva sp. These algae were reported to be able to adsorb one or more heavy metal ions, including K, Mg, Ca, Fe, Sr, Co, Cu, Mn, Ni, V, Zn, As, Cd, Mo, Pb, Se, Al, with good metal uptake capacity (Brinza et al., 2007). Chojnacka et al. (2005) reported the biosorption performance of Cr3+, Cd2+ and Cu2+ ions by blue–green algae Spirulina sp. Nayak et al. (2003) studied the biosorption of heavy metals and toxic radionuclides by three genera of algae from different taxonomic groups, including Hg-197, Tl-198, Tl199, Tl-200, Tl-201, Pb-199, Pb-200, Pb-201, Bi-204 and Po-204, Po205 radionuclides. Thirty freeze-dried strains of algae were examined to adsorb cadmium, lead, nickel, and zinc from aqueous solution (Klimmek et al., 2001). The screening batch adsorption experiments were carried out

Table 12 The maximum biosorption capacity (qmax) for 30 algae strains (unit: mmol g− 1) Biomass

Pb (0.4)a

Cd (0.1)a

Ni (0.1)a

Zn (0.1)a

S. hofmani L. taylorii A. densus K. spiculiformis V. dichotoma C. kessleri M. species N. parmeloides S. maxima C. vulgaris G. longicauda R. spiculiforme A. hantzschii S. platensis P. tricornutum M. aeroginosa P. purpureum T. species G. verrucosa C. species A. cylindrica S. laxissima G. planctonica S. species P. species A. africanum E. magnus D. salina A. inaequealis D. bioculata

0.85 0.84 0.8 0.71 0.7 0.55 0.54 0.5 0.49 0.46 0.44 0.4 0.39 0.38 0.36 0.35 0.33 0.3 0.24 0.23 0.22 0.22 0.21 0.19 0.19 0.18 0.16 0.1 0.1 0.02

0.33 0.32 0.24 0.34 0.28 0.24 0.25 0.23 0.27 0.29 0.27 0.25 0.27 0.29 0.23 0.23 0.18 0.13 0.15 0.2 0.14 0.22 0.06 0.24 0.17 0.17 0.09 0.07 0.08 0.05

0.17 0.43 0.26 0.28 0.37 0.12 0.2 0.22 0.12 0.31 0.2 0.26 0.25 0.4 0.19 0.21 0.2 0.26 0.13 0.17 0.14 0.13 0.11 0.09 0.18 0.15 0.12 0.06 0.12 0.05

0.37 0.37 0.23 0.42 0.42 0.14 0.24 0.24 0.23 0.18 0.28 0.25 0.11 0.27 0.37 0.23 0.25 0.19 0.24 0.16 0.1 0.11 0.18 0.07 0.36 0.11 0.17 0.06 0.1 0.04

Source: Klimmek et al., 2001. a In parentheses is the initial concentration of the particular metal ions.

J.L. Wang, C. Chen / Biotechnology Advances 27 (2009) 195–226

with the same initial concentration for each metal. The initial concentrations where the surface of C. vulgaris was saturated with the particular metal were selected for the screening. The use of saturating conditions for a screening investigation was necessary because the uptake capacity otherwise would not be comparable. The initial concentrations for the screening investigations were determined to be 400 mg L− 1 for lead and 100 mg L− 1 for the other three metals. The maximum capacity (qmax) according to the Langmuir model was used to screen these 30 algae. A wide range of the values of qmax between the different strains of algae and between the four metals can be observed. The results were shown in Table 12, which offered the qmax for 30 algae strains (Klimmek et al., 2001). The cyanophyceae, L. taylorii exhibited high uptake capacity for four metal ions (qmax: mmol g− 1): Pb (1.47), Ni (0.65), Zn (0.49) and Cd

Table 13 The sorption parameters in monometallic systems for un-pretreated algal biomass Algae

Metal ions

qmax (mmol g− 1)

Ascophyllum nodosum (B) Ascophyllum nodosum Ascophyllum nodosum Chaetomorha linum (G) Chlorella miniata (G) Chlorella miniata Chlorella vulgaris (G) Chlorella vulgaris Chlorella vulgaris Chlorella vulgaris Chlorella vulgaris Chlorella vulgaris Chlorella vulgaris Cladophora glomerata (G) Chondrus crispus (R) Chondrus crispus Codium fragile (G) Codium taylori (G) Codium taylori Corallina officinalis (R) Fucus vesiculosus (B) Fucus vesiculosus Fucus vesiculosus Galaxaura marginata (R) Galaxaura marginata Gracilaria corticata (R) Gracilaria edulis (R) Gracilaria Salicornia (R) Padina sp.(B) Padina gymnospora (B) Padina gymnospora Padina tetrastomatica (B) Padina tetrastomatica Polysiphonia violacea (R) Porphira columbina (R) Sargassum sp. (B) Sargassum sp. Sargassum sp. Sargassum baccularia (B) Sargassum fluitans (B) Sargassum fluitans Sargassum hystrix (B) Sargassum natans (B) Sargassum natans Sargassum natans Sargassum siliquosum (M) Sargassum vulgare (M) Sargassum vulgare Scenedesmus obliquus (G) Scenedesmus obliquus Scenedesmus obliquus Ulva lactuca (G) Undaria pinnatifida (B)

Cd Ni Pb Cd Cu Ni Cd Ni Pb Zn Cr(VI) Cu Fe(III) Pb Ni Pb Cd Ni Pb Cd Cd Ni Pb Ni Pb Pb Cd Cd Cd Ni Pb Pb Cd Pb Cd Cd Cr(VI) Cu Cd Ni Pb Pb Cd Ni Pb Cd Ni Pb Cu Ni Cr(VI) Pb Pb

0.338~1.913 1.346~2.316 1.313~2.307 0.48 0.366 0.237 0.30 0.205~1.017 0.47 0.37 0.534~1.525 0.254~0.758 0.439 0.355 0.443 0.941 0.0827 0.099 1.815 0.2642 0.649 0.392 1.105~2.896 0.187 0.121 0.2017~0.2605 0.24 0.16 0.53 0.170 0.314 1.049 0.53 0.4923 0.4048 1.40 1.30~1.3257 1.08 0.74 0.409 1.594 1.3755 1.174 0.409 1.1487~1.221 0.73 0.085 1.100 0.524 0.5145 1.131 0.61 1.945

Source: Romera et al., 2006. (B): Brown alga; (G): Green alga; (R): Red alga.

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Table 14 The average value of qmax (mmol g− 1 biomass) for each metal ion in monometallic systems without pretreatment Metal ions

Brown alga

Red alga

Green alga

Average value

Cd Ni Zn Cu Pb

0.930 0.865 0.676 1.017 1.239

0.260 0.272

0.598 0.515 0.370 0.504 0.813

0.812 0.734 0.213 0.909 1.127

0.651

Source: Romera et al., 2006.

(0.37). The modified biosorbent of L. taylorli by phosphorylation improved the metal binding ability and achieved the values of qmax: Pb (3.08), Ni (2.79), Zn (2.60) and Cd (2.52). The selectivity remained quite similar to the unmodified algae (Klimmek et al., 2001). Based on the statistical analysis using biosorption data of 37 different algae (20 brown algae, 9 red algae and 8 green algae) from 214 references collected, a statistical review of biosorption of algae in the form of dead biomass were given by Romera et al. (2006). The available data of maximum sorption capacity (qmax) and biomass-metal affinity (b) of the Langmuir equation for Cd2+, Cu2+, Ni2+, Pb2+ and Zn2+ were listed in the review. Brown algae stand out as very good biosorbents for heavy metals. The information available in connection with multimetallic systems is very poor. Algae achieve values of qmax were close to 1 mmol/g for copper and lead and smaller for the other metals. Metal recovery performance was worse for nickel and zinc, but the number of samples for zinc was very small. Algae present a high affinity for Pb, followed by cadmium, copper, nickel and zinc, all of which present very similar values. The best performer for metal biosorption by brown algae is lead (Romera et al., 2006). Based on the some reviews and relevant articles, some values of sorption capacity were listed in Table 13. 5.3. Comparison of algae with other biosorbents Romera et al. (2006) summarized the results achieved with brown algae, green algae, and red algae. It was found that the average sorption capacity of red algae was lower. Table 14 offered the average qmax values for each metal in monometallic systems by algae. When taking average values, these atypical values must be discarded, otherwise the mean will not be representative of the whole set of algae. The differences may be due to both the experimental conditions of each work and the chemical composition of the corresponding cell walls. Baran et al. (2005) reported that the maximum sorption capacity of Halimeda tuna, Sargassum vulgare, Pterocladia capillacea, Hypnea musciformis, Laurencia papillosa for Cr6+ were 2.3, 33.0, 6.6, 4.7 and 5.3 mg g− 1, respectively. The results showed that S. vulgare was suitable for removing chromium from aqueous solution. Five different brown seaweeds, Bifurcaria bifurcata, Saccorhiza polyschides, A. nodosum, Laminaria ochroleuca and Pelvetia caniculata were studied and their ability to remove cadmium from aqueous solution were between 64 and 95 mg g− 1 (Lodeiro et al., 2005). Taking Cu(II) as an example, the uptake capacity (expressed as qmax values) by various algal species were (qmax: mmol Cu/g): A. nodosum (Brown algae: 0.99), Caulerpa lentillifera (Green macroalgae: 0.13), C. vulgaris (Green microalgae: 0.67, 1.40), Durvillaea potatorum (Brown algae: 1.30), Ecklonia radiate (Brown algae: 1.11), Glacillaria sp. (Red macroalgae: 0.59), Padina sp. (Brown algae: 0.80, 1.14), Sargassum filipendula (Brown algae: 0.98), Sargassum fluitans (Brown macroalgae: 0.80, 0.96), Sargassum sp.(Brown algae: 0.99, 1.48), S. vulgare (Brown algae: 0.93). Spirulina sp., (Blue green algae: 0.004), Ulothrix zonata (Green macroalgae: 2.77), Ulva sp. (Green macroalgae: 0.75) (Brinza et al., 2007). The results were not able to be compared directly due to the data from the various authors' reports.

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Murphy et al. (2007) also studied several dried biomass of the marine macroalgae, F. spiralis and Fucus uesiculosus (brown), Ulva spp. (comprising Ulva linza, Ulva compressa and Ulva intestinalis) and Ulva lactuca (green), P. palmata and Polysiphonia lanosa (red), in terms of their Cu(II) biosorption performance. Ulva spp. performed extremely efficiently in sequestering copper ions (0.326 mmol g− 1), maybe due to its high uronic acid content. Zhou et al. (1998) investigated the sorption and desorption of Cu and Cd by macroalgae and microalgae, the experimental results showed that S. platensis had the highest capacity for Cd, followed by Nannochloropsis oculata, P. tricornutum, Platymonas cordifolia and Chaetoceros minutissimus among those five microalgae tested. Lee et al. (2000) investigated the screening of hexavalent chromium biosorbent from marine algae, they compared chromate adsorption capacity of 48 species of red, brown, or green marine algae from the east coast of Korea. A red marine alga, Pachymeniopsis sp. was identified as a highly chromate-selective biosorbent with high adsorption capacity of 225 mg/g. The alga also showed high selectivity for chromate and its adsorption capacity for other heavy metal ions such as cadmium and manganese was relatively low. Matsunaga et al. (1999) investigated the screening of marine microalgae for bioremediation of cadmium-polluted seawater, the results indicated that twenty four strains out of 191 marine microalgal strains exhibited cadmium (Cd) resistance. These strains were tested for their Cd removal ability in growth media containing 50 μM Cd. Six strains out of 19 green algae and one out of five cyanobacteria removed more than 10% of total Cd from the medium. The marine green alga Chlorella sp. NKG16014 showed the highest removal capacity, the removal efficiency of Cd achieved 48.7%. The removal of Cd by NKG16014 was further quantitatively evaluated by measuring the amount of cell adsorption and intracellular accumulation. After 12 days incubation, 67% of the removed Cd was accumulated intracellularly and 25% of the Cd removed was adsorbed on the algal cell surface. The maximum Cd adsorption was estimated to be 37.0 mg Cd g− 1 using the Langmuir sorption model. The Cd removal by freeze-dried NKG16014 cells was also determined. Cd was more quickly adsorbed by dried cells than by living cells, with a qmax of 91.0 mg Cd g− 1. The metal uptake capacity by the non-living, dried marine brown algae decreased in the following sequence: U. pinnatifida N H. fusiformis N S. fulvellum (Nayak et al., 2003). The affinity and selectivity of algae for metal ions were of interest. The microalgae C. reinhardtii showed the affinity order as follows: Pb(II) N Hg(II) N Cd(II). The maximum biosorption capacity of microalgae for Hg(II), Cd(II) and Pb(II) ions were 72.2 ± 0.67, 42.6 ± 0.54 and 96.3 ± 0.86 mg g− 1 dry biomass, respectively (Tuzun et al., 2005). The affinity of metal ions for the red algae P. palmata was found to decrease in the order: Pb 2+ N Co 2+ N Cu 2+ N Ni 2+ (Prasher et al., 2004). The selectivity for the following four metal ions was: Ca N Mg N Cd N K for Laminaria sp.; Cd N Ca N Mg N K for Durvillaea sp.; Ca N Cd N K N Mg for Ecklonia sp.; Mg N Cd N K NCa for Hormosira sp. And by ion exchange model: Ca N Mg N Cd N K for Laminaria sp.; Cd N Mg N Ca N K for Durvillaea sp.; Ca N Cd N K N Mg for Ecklonia sp.; Mg N Cd N K NCa for Hormosira sp. (Figueira et al., 2000). The general affinity sequence of Pb N Cu N Cd N Zn N Ni for Padina sp. was observed (Sheng et al., 2004). The biomass of non-living dried marine brown algae U. pinnatifida, H. fusiformis, and S. fulvellum, harvested in the sea near Cheju Island, Korea were studied for their sorption ability for copper, zinc, and lead. The metal uptake capacity by biosorbent decreased in the following sequence: U. pinnatifida NH. fusiformisN S. fulvellum. The maximum metal uptake capacity of U. pinnatifida for Cu2+, Pb2+, and Zn2+ in the single component metal solution was 2.58, 2.6, and 2.08 meq g− 1, respectively, in the pH range of 5.3–4.4. The metal uptake capacity by biosorbent in the mixed metal solution system decreased greatly in comparison with single component metal uptake system (Lee et al., 2002).

Batch equilibrium sorption experiments were used for screening the cost-effective marine algal biomass harvested from the Gulf of Persian. Biosorption of lead by eight brown, green and red marine algae was investigated. Three species of brown algae, namely S. hystrix, S. natans and P. pavonia, can remove lead most efficiently from aqueous solution, respectively (Jalali et al., 2002). Rincon et al. (2005) investigated the biosorption of heavy metals by chemically-activated alga F. vesiculosus, they compared brown algae and other sorbents, the results was summarized in Table 15. 6. Effect of pre-treatment on biosorption As the biosorption process involves in mainly cell surface sequestration, the modification of cell wall can greatly alter the binding of metal ions. A number of methods have been employed for cell wall modification of microbial cells in order to enhance the metal binding capacity of biomass and to elucidate the mechanism of biosorption. The physical treatments include heating/boiling, freezing/thawing, drying and lyophilization. The various chemical treatments used for biomass modification include washing the biomass with detergents, cross-linking with organic solvents, and alkali or acid treatment. The pretreatments could modify the surface characteristics/groups either by removing or masking the groups or by exposing more metalbinding sites (Vieira and Volesky, 2000). Yeast cells killed by extreme chemical and physical conditions may also show very different properties for metal accumulating, compared with the original yeast (Lu and Wilkins, 1996). Now various pretreatment methods were reported to deal with the cells of S. cerevisiae. Physical methods include vacuum and freeze-drying, boiling or heating, autoclaving, mechanical disruption. Chemical methods include treatment with various organic and inorganic compounds, such as acid and caustic, methanol, formaldehyde, etc. Some methods are found to improve metal biosorption to some extent. Alkali treatment of fungal has been shown to increase significantly the metal uptake capacity, whereas acid treatment of biomass almost has no influence on metal biosorption (Kapoor and Viraraghavan, 1995; Wang, 2002a). S. cerevisiae were modified by methanol, formaldehyde and glutaraldehyde respectively, and then used for Cu2+ removal. The results showed that esterification of carboxyl and methylation of amino groups present in the cell wall significantly decreased the biosorption capacity of copper, which suggests that both carboxylic and amine groups play an important role in biosorption of copper. However, glutaraldehyde-treated biomass almost retained the original biosorption capacity (Wang, 2002a). Due to the important role of cell wall for metal biosorption by nonviable cells, metal biosorption may be enhanced by heat or chemical sterilization or by crushing. Thus degraded cells would offer a larger available surface area and expose the intracellular components and more surface binding sites because of the destruction of the cell membranes (Errasquin and Vazquez, 2003).

Table 15 The value of qmax (mmol g− 1) for different sorbents Sorbents

Cu

Pb

Cr

Ni

Natural zeolite Activated charcoal powder Pseudomonas aeruginosa (bacteria) Rhizopus arrhizus (fungus) Activated charcoal granular Ion exchange resin Fucus vesiculosus

– – 0.29 0.25 0.03 – 0.97

0.18 0.10 0.33 0.50 0.15 1.37 1.04

– – – 0.27 0..07 0.59 1.12

– – – – – – 0.08

Source: Rincon et al., 2005.

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The biosorption of cadmium and lead ions from synthetic aqueous solutions using yeast biomass was investigated (Goksungur et al., 2005). The waste baker's yeast cells were treated by caustic, ethanol and heat methods, and the highest metal uptake capacity for Ca2+ and Pb2+ were obtained by ethanol treated yeast cells. However, Suh and Kim (2000) gave the different results on pretreatment. The equilibrium uptake capacity of lead (in mg Pb2+ g− 1) decreased in the order: original cell (260) N5 times autoclaved cell for 15 min (150)N grinded cell after drying (100)N autoclaved cell for 5 min (30). Brown alga F. vesiculosus for the removal of copper, cadmium, lead and nickel was investigated. Metal sorption yields were modified using different kinds of pretreatment reagents: HCl, CaCl2, formaldehyde, Na2CO3 and NaOH. The Langmuir isotherm was applied to both the nontreated and all treated biomass tests. Calcium chloride was the only chemical that improved the maximum sorption capacity of the biomass (Rincon et al., 2005). Pretreatment of Mucor rouxii biomass with detergent and alkali chemicals such as NaOH, Na2CO3, and NaHCO3 were investigated for the biosorption of Pb2+, Cd2+, Ni2+ and Zn2+ (Yan and Viraraghavan, 2000). Different alkaline treatments were also studied (1 M NaOH/ 20 °C/24 h and 10 M NaOH/107 °C/6 h) (Spanelova et al., 2003). The effect of pretreatment of A. niger biomass on biosorption of lead, cadmium, copper and nickel was studied. Pretreatment of live A. niger biomass using sodium hydroxide, formaldehyde, dimethyl sulphoxide and detergent resulted in significant improvement in biosorption of lead, cadmium and copper in comparison with live A. niger cells. Pretreatment of A. niger reduced biosorption of nickel, compared with live cells (Kapoor and Viraraghavan, 1998). Some modifications can be introduced either during the growth of a microorganism or in the pre-grown biomass because the condition in which microorganisms grow affects its cell components or surface phenol type, which in turn affects its biosorption potential (Vianna et al., 2000). Variation in growth conditions possibly brings about changes in composition of the cell surface, thereby affecting metal biosorption characteristics of the biomass (Mehta and Gaur, 2005). Some work has been done on the effect of cultural conditions of cells on their biosorptive capacity, such as the effect of glucose, cysteine, glucose, ammonium sulphate, phosphate, ammonium chloride, C-, N-, P-, S-, Mg- and K-limited conditions, which could refer to the review (Wang and Chen, 2006). For example, Mapolelo and Torto (2004) reported that the pretreatment of the S. cerevisiae by using 10–20 mmol L− 1 glucose increased the removal efficiency by 30–40% for Cd2+, Cr3+, Cu2+, Pb2+ and Zn2+, but by using 60 mmol L− 1 glucose decreased almost 50% removal for Cr6+. The mechanism for Cr6+ uptake may differ from other metal ions. Stoll and Duncan (1996) investigated the uptake of Cu2+, Cr6+ Cd2+, Ni2+ and Zn2+ from electroplating effluent by living cells of S. cerevisiae. The results showed that pretreatment of the yeast cells with glucose increased the amount of metal removed, while direct addition of glucose to the yeast-effluent solution had no effect on the amount of metal accumulated. Dostalek et al. (2004) investigated biosorption of Cd2+, Cu2+ and Ag+ ions by C-, N-, P-, S-, Mg- and K-limited cells of S. cerevisiae. The binding capacity of yeast cells for cadmium decreases in the order: K-limited≥Mg-limited≌ C-limitedN N-limited≌S-limitedN P-limited. For Ag+ ions: P-limited N K-limitedN C-limited ≥ N-limited ≌ Mg-limited N S-limited. For copper ion: K-limited N Mg-limited ≥ Climited N N-limited ≌ P-limited N S-limited. Addition of L-cysteine into the growth medium increased the biosorption capacity for silver, protein and sulphydryl group content of the freeze-dried and viable yeast cells, although the increase of concentration of L-cysteine (from 1 to 5 mmol L− 1) decreased the cell numbers in comparison with the control test without L-cysteine (Simmons and Singleton, 1996). 7. Biosorbent immobilization for bioreactors and regeneration/reuse The costs of biosorbent preparation must also be taken into account. To date, the majority of research conducted has focused on

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the use of granulized biosorbents packed in columns, resembling ionexchange resins. Although cell entrapment imparts mechanical strength and resistance to chemical and microbial degradation upon the biosorbents, the costs of immobilizing agent cannot be ignored. Free cells are not suitable for use in a column in that due to their low density and size they tend to plug the bed, resulting in large drops in pressure. Support matrices suitable for biomass immobilization include alginate, polyacrylamide, polyvinyl alcohol, polysulfone, silica gel, cellulose and glutaraldehyde (Wang, 2002b). For industrial application of biosorption, it is important to utilize an appropriate immobilization technique to prepare commercial biosorbents which retain the ability of microbial biomass to adsorb metal(s) during the continuous treatment process. The free microbial cells generally are basically small particles, with low density, poor mechanical strength and little rigidity, which may come up with the solid–liquid separation problems, possible biomass swelling, inability to regenerate/reuse and development of high pressure drop in the column mode in real application. Excessive hydrostatic pressures are required to generate suitable flow rates in a fixed or expanded bed reactor. High pressures can cause disintegration of free biomass. These problems can be avoided by the use of immobilized cell systems. The immobilization of the biomass in solid structures would create a biosorbent material with the right size, mechanical strength, rigidity and porosity necessary for use in practical processes. The immobilized materials can be used in a manner similar to ion exchange resins and activated carbons such as adsorption–desorption cycles (recovery of the adsorbed metal, reactivated and re-use of the biomass) (Veglio and Beolchini, 1997). The author introduces the microbial immobilization techniques in a monograph (Wang, 2002b). Immobilization technique is one of the key elements for the practical application of biosorption, especially by dead biomass. Various kinds of immobilized S. cerevisiae have been studied with different support materials, which can be used in practical biosorption (Veglio and Beolchini, 1997). A number of matrices have been employed for immobilization of cells. Important immobilization matrices used in biosorbent immobilization include sodium or calcium alginate, polysulfone, polyacrylamide, polyurethane, silica (Vijayaraghavan and Yun, 2008). The polymeric matrix determines the mechanical strength and chemical resistance of the final biosorbent particle to be utilized for successive sorption–desorption cycles so it is very important to choose the immobilization matrix. Fluidized beds of Ca-entrapped cells of C. vulgaris and S. platensis were successfully used to recover gold from a simulated gold-bearing process solution containing AuCl4, CuCl2, FeCl2 and ZnCl2 (Vieira and Volesky, 2000). P. maltophilia cells immobilized with polyacrylamide gel also have a high ability for gold biosorption. The gold adsorbed on the immobilized cells is easily desorbed with 0.1 M thiourea solution. The immobilized P maltophilia cells can be used repeatedly in biosorption–desorption cycles (Tsuruta, 2004). Basidiospores of P. chryosporium were immobilized into Ca-alginate beads via entrapment for the removal of Hg(II) and Cd(II) ions from aqueous solution in the concentrations range of 30–500 mg L− 1. The alginate-fungus beads could be regenerated using 10 mM HCl, up to 97% recovery. The biosorbents were reused in three biosorption–desorption cycles with negligible decrease in biosorption capacity (Kacar et al., 2002). Another important matrix is silica. The silica immobilized product is mechanically strong and exhibits excellent flow characteristics. T. versicolor mycelia were immobilized in carboxymethylcellulose (CMC) to form beads via entrapment, and then the beads containing immobilized fungus spores were incubated at 30 degrees C for 3 days to attain uniform growth on the bead surface. After incubation, the live and heat inactivated immobilized fungus on the CMC beads were used for the biosorption of Cu2+, Pb2+ and Zn2+ ions. Plain CMC beads were used as a control system. The maximum biosorption capacities

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for both immobilized live and heat inactivated T. versicolor were 1.51 and 1.84 mmol Cu2+, 0.85 and 1.11 mmol Pb2+ and 1.33 and 1.67 mmol Zn2+ per g of dry biosorbents, respectively. The CMC beads with the immobilized fungus can be regenerated using 10 mM HCl, with up to 97% recovery of the metal ions; the biosorbents reused up to five biosorption–desorption cycles without any major loss in the biosorption capacity (Bayramoglu et al., 2003). The entire biosorption process for metal removal include sorption followed by desorption, i.e., to concentrate the solute. Biotechnological exploitation of biosorption technology for removal of heavy metal(s) depends on the efficiency of the regeneration of biosorbent after metal desorption. It is important to regenerate the biosorbents especially the biomass preparation/generation is costly. Therefore non-destructive recovery by mild and cheap desorbing agents is desirable for regeneration of biomass and reuse in multiple cycles. Appropriate eluants are necessary to attain the above-mentioned objective, which strongly depends on the type of biosorbent and the mechanism of biosorption. Also, the eluant must meet the following requirements: (i) non-damaging to the biomass, (ii) less costly, (iii) environmental friendly and (iv) effective (Vijayaraghavan and Yun, 2008). Acidic and alkaline condition were used for desorption. The eluants such as CaCl2 with HCl, HCl with EDTA, NaOH were reported (Vijayaraghavan and Yun, 2008). Desorption data showed that nearly 99% of the Cr (VI) adsorbed on Mucor hiemalis could be desorbed using 0.1 N NaOH. The cyclic use of a batch of M. hiemalis repeatedly after desorption was studied, the results showed that it retain its activity up to five cycles of sorption and desorption (Tewari et al., 2005). Desorption with nitric acid showed the high elution efficiency and preservation of biosorptive properties for heavy metal ions (Cr3+, Cd2+, Cu2+) by blue–green algae Spirulina sp. (Chojnacka et al., 2005). The efficiency of desorption is often expressed by the S/L ratio, i.e. solid to liquid ratio. The solid represents the solid sorbent (in mg dry wt) and the liquid represents the amount of eluant applied (in ml). High values of S/L are desirable for complete elution and to make the process more economical. Sometimes metal-selective elution is desirable and it is dependent on metal sequestration mechanism. Dilute mineral acids, EDTA, carbonates and bicarbonates, NH4OH, KHCO3, KCN have been used to remove metal(s) from the loaded biomass (Vieira and Volesky, 2000). To date, less attention has been paid to investigate the regeneration ability of the biosorbent, more relevant work is necessary for future biosorption application. Immobilization of biosorbents is a key aspect for the purpose of biosorption application. It is important to decrease the cost of immobilization and consequently distribution, regeneration and reuse of biosorbents (Tsezos, 2001). Although continuous process for metal removal by immobilized cells has been realized at lab scale, there is still long way to go for biosorption commercialization. Selection of good and cheap support materials for biosorbent immobilization, improvement of reuse methods, and enhancement of properties of immobilized biosorbents such as porous ratio, mechanical intensity and chemical stability, these are also important factors for application. However, immobilization of biosorbents will probably bring about at least two practical problems: mass transfer limitation and additional process cost (Vijayaraghavan and Yun, 2008). As we pointed out that the industrial application of biosorption with immobilized dead cells have been performed for some pilot plants of biosorption, but the cost for preparation of the required biosorbents with waste biomass was too expensive by immobilization techniques and by various pre-treatment processes. Process of regeneration and re-use on-line is complex and expensive. The co-existed ions and organic compounds in solution made matters even more difficult and more complex for real effluents (Wang and Chen, 2006). When developing the immobilization and regeneration technology for biosorption application, the above-mentioned problems should be taken into account.

Fig. 8. Schematic diagram of processing different types of microbial biomass into usable biosorbents. Source: Vieira and Volesky, 2000.

A schematic diagram for processing different types of microbial biomass into usable biosorption materials is shown in Fig. 8 (Vieira and Volesky, 2000). 8. Modeling of biosorption: isotherm and kinetic models Assessment of a solid–liquid sorption system is usually based on two types of investigations: equilibrium batch sorption tests and dynamic continuous-flow sorption studies (Volesky and Holan, 1995). Yu and Neretnieks (1990) reviewed the model isotherms for singlecomponent adsorption. Some authors gave a description of the modeling of biosorption in detail (Aksu, 2005; Kratochvil and Volesky, 1998; Pagnanelli et al., 2002; Veglio and Beolchini, 1997; Volesky, 2003). Volesky, in the book entitled “sorption and biosorption” (http://www. Biosorption.mcgill.ca), also offered a detailed introduction to biosorption equilibrium and kinetics, e.g. single-sorbate isotherms, multi-sorbate sorption equilibrium (the multi-component Langmuir models with considering electrostatic binding, the effect of pH, surface complex model, the Donnan model with considering ionic strength, the Wilson model for ion exchange etc.), biosorption batch dynamics (mass transfer model for biosorption rate), dynamic continuous-flow reactor/contactor systems for modeling column performance including equilibrium column model, mass transfer model and derivation of mass transfer model. Aksu (2005) described the kinetic modeling for biosorption in a continuous system. Volesky (2003) summarized biosorption dynamics. 8.1. Equilibrium modeling of biosorption Equilibrium isotherm models are usually classified into the empirical equations and the mechanistic models. The mechanistic models are based on mechanism of metal ion biosorption, which are able not only to represent but also to explain and predict the experimental behavior (Pagnanelli et al., 2002; Volesky, 2003). Some empirical models for single solute systems are listed in Table 16. The Langmuir model (L type, based on monolayer adsorption of solute) and the Freundlich model (F type, developed for heterogeneous surfaces) are the most widely accepted and used in literatures. The BET model describes the multi-layer adsorption at the adsorbent surface and assumes that the Langmuir isotherm applies to each layer. These models can provide information of metaluptake capacity and difference in metal uptake between various species (Kapoor and Viraraghavan 1995; Pagnanelli et al., 2002; Volesky and Holan 1995). These empirical models do not reflect any mechanisms of sorbate uptake and hardly have a meaningful physical interpretation for biosorption. Volesky and Holan (1995) pointed out that the results from the empirical models cannot be extrapolated, and no predictive

J.L. Wang, C. Chen / Biotechnology Advances 27 (2009) 195–226 Table 16 Frequently used single-component adsorption models Isotherm types

Equations

Langmuir

qe =

Freundlich

qe = KF Ce

Langmuir– Freundlich

qe =

qmax bCe 1=n 1 + bCe

BET model (multilayer sorption)

qe =

BQ 0 Ce ðCs −Ce Þ½1 + ðB−1ÞCe =Cs 

Redlich– Peterson

qe =

KRP Ce 1 + aRP Ceβ

Radke– Prausnitz

qe =

arCep a + rCep−1

qmax bCe 1 + bCe

1=n

1=n

distribution qe = Kd Ce coefficients model

Nomenclature

References

qe is equilibrium metal sorption capacity; Ce is equilibrium solute concentration in solution; qmax and b are Langmuir constants related to maximum sorption capacity (monolayer capacity) and bonding energy of adsorption (or “affinity”), respectively KF is a biosorption equilibrium constant, representative of the sorption capacity; and n is a constant indicative of biosorption intensity Assuming that the surface is homogeneous, but that the sorption is a cooperative process due to adsorbate–adsorbate interactions. Cs is the saturation concentration of the adsorbed component; B a constant indicating the energy of interaction between the solute and the adsorbent surface, and Q0 is a constant indicating the amount of solute adsorbed forming a complete monolayer KRP, aRP, and β are the Redlich– Peterson parameters. The exponent β lies between 0 and 1. For β = 1 the model converts to the Langmuir form. a, r, and p are related model constants

Langmuir (1918)

Kd is distribution coefficient

Freundlich (1906)

Sips (1948)

Brunauer et al. (1938)

Redlich and Peterson (1959) Radke and Prausnitz (1972) Aksu (2005)

conclusions can be drawn for systems operating under different conditions. Both simple basic models (the Langmuir model and the Freundlich model) also do not incorporate the effects of any external variable environmental factors, although they are capable of describing many biosorption isotherms in most cases. The mechanistic conclusions from the good fit of the models alone should be avoided. Moreover, biosorption isotherms may exhibit an irregular pattern due to the complex nature of both the biosorbents and its varied multiple active sites, as well as the complex solution chemistry of some metallic compounds (Kapoor and Viraraghavan, 1995; Volesky and Holan, 1995; Kim et al., 1998). To describe two- or multi-metal ions biosorption system, various extended Langmuir models (also called competitive Langmuir model) or Freundlich type models have been developed (Aksu et al., 1997; Chong and Volesky, 1995; Pagnanelli et al., 2002; Volesky, 2003). These empirical models hardly reflect the sorption mechanism.

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Volesky and his colleagues carried out a series of work on modeling biosorption, considering metal biosorption mechanisms involving ion exchange and/or complexation. These models considered the sorbate speciation in solution, pH and even electrostatic attraction (Chong and Volesky, 1995; Figueira et al., 2000; Schiewer, 1999; Schiewer and Volesky, 1996, 1997a,b; Schiewer and Wong, 2000; Yang and Volesky, 1999). Based on the mechanism of ion exchange between protons in the biomass and hydrolyzed uranium ion species, they developed a mathematical model for predicting biosorption isotherm of uranium at different pH values (Yang and Volesky, 1999). Real wastewaters commonly contain a mixture of metal ions. Thus, multi-metal biosorption models have been developed, and some of them are listed in Table 17. The Surface Complexation Model (SCM) based on the concept of surface charge generated from the amphoteric surface sites are capable of explaining the reaction with sorbing cationic or anionic species to form surface complexes (Volesky, 2003). 8.2. Kinetic modeling of biosorption in a batch system Numerous kinetic models have been suggested to describe the reaction order of adsorption systems based on solution concentration. Kinetic models based on the capacity of the adsorbent have also been presented, such as the Lagergren's first-order equation and Ho's second-order expression (Ho, 2006). The first-order equation of Lagergren (Lagergren, 1898) and the pseudo second-order equation are the most widely used kinetic models to describe the biosorption process, they are listed in Table 18. The pseudo second-order equation fitted the data very well in a large quantity of literature for biosorption (Ho, 2006; Ho and McKay, 1999). Ho (2006) gave a review on the application of second-order kinetic models to adsorption systems, including an earlier adsorption rate equation based on the solid capacity for a system of liquids and solids, the Elovich equation for adsorption of gases onto a solid, and applying a second-order rate equation for gas/solid and solution/solid adsorption systems, a second-order rate expression for ion exchange reactions, and a pseudo-second-order expression. Kinetics studies and dynamic continuous-flow investigations, offering information on the rate of the sorption metal uptake, together with the hydrodynamic parameters, are very important for biosorption process design (Volesky and Holan, 1995). However, biosorption kinetics studies are insufficient according to literature published so far. 9. Biosorbent selection and assessment How to select the suitable biosorbent among a large quantity of biomass tested? The selection of a proper sorbent for a given separation is a complex problem. The predominant scientific basis for sorbent selection is the equilibrium isotherm. Diffusion rate is generally secondary in importance. From the viewpoint of practical application, availability and economy is a major factor to be taken into account for selecting the biomass for clean-up purposes (Vieira and

Table 17 Frequently used multi-component adsorption models Isotherm types Langmuir (multi-component)

Equations qei =

bi qmaxi Cei N

1 + Σ bi C ei i= 1

aC

1=ni

i ei Combined qei = N 1=n 1 + Σ bi Cei i Langmuir–Freundlich i= 1 KRPi Cei Competitive qe = N βi 1 + Σ aRPi Cei Redlich–Peterson model i= 1 Y 1 i = Σ IAST: Ideal Adsorbed 0 qt qi Solution Theory

Nomenclature

References

Cei and qei are the unadsorbed concentration of each component at equilibrium and the adsorbed quantity of each Langmuir (1918) component per g of dried biomass at equilibrium, respectively. bi and qmaxi are derived from the corresponding individual Langmuir isotherm equations. ai,bi, phase concentration of a single adsorbed component in equations. Sips (1948) KRPi, aRPi, and βi are the Redlich–Peterson parameters derived from the corresponding individual Redlich–Peterson isotherm equations. Yi is the solute concentration of component i in the solid phase. q0i is the phase concentration of a single adsorbed component in equations with C0i

Bellot and Condoret (1993) Radke and Prausnitz (1972)

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Table 18 First-order equation of Lagergren and the pseudo second-order equation Kinetic models

Differential equations

Integral equations

First-order rate expression of Lagergren

dqt = k ðq −q Þ t 1 e dt

k1 Lagergren t logðqe −qt Þ = log qe − 2:303 (1898) v1 = k1 qe v1 = k1qe where q is the amount of adsorbed pollutant on the biosorbent at time t; k1 is the rate constant of Lagergren first-order biosorption; v1 is the initial sorption rate. qt = 1 t + t Ho and qe k 2 q2 e McKay v2 = k2q2e (1999) where k2 is the rate constant of second-order biosorption; v2 is the initial adsorption rate.

Pseudo second- dqt = k2 ðqe −qt Þ2 dt order equation

References

Volesky, 2000). Correct assessment of the metal-binding capacity of some types of biomass is also very important. How to evaluate the sorption performance for a certain biosorbent? How to evaluate the experimental results reported by researchers from different backgrounds? Volesky and his colleagues discussed the related questions (Kratochvil and Volesky, 1998; Volesky and Holan, 1995). Two types of investigations could help to examine a solid–liquid sorption system: (a) equilibrium batch sorption tests and (b) dynamic continuous-flow sorption studies. The Langmuir model and the Freundlich model (Table 16) are two widely accepted equilibrium adsorption isotherm models for single solute systems. qmax is the maximum sorption capacity corresponding to complete monolayer coverage (in mmol g− 1), Ce (in mmol L− 1) is the equilibrium solute concentration, and b is the equilibrium constant related to the energy of sorption (or “affinity”) (in L mmol− 1), KF and n are the Freundlich constants related to the adsorption capacity and intensity of the biosorbent, respectively. These parameters from the models could be used for comparing the biosorbents performances. The evaluation of sorption systems is based on the classical sorption isotherm derived from equilibrium batch contact experiments under the same environmental conditions (e.g. pH, temperature, ionic strength). A quantitative comparison of two different sorption systems can only be made at the same equilibrium (final, residual) concentration. Thus comparison at low equilibrium concentration Cf (e.g., 10 mg L− 1) and another at high equilibrium concentration Cf (e.g., 200 mg L− 1) are made in some biosorption screens, as an example, shown in Fig. 9 (Kratochvil and Volesky, 1998). Biosorption performance in terms of metal uptake capacity can be judged at the same (selected: e.g. 10 and/or 200 mg L− 1) equilibrium (final) metal concentration. Comparison of qmax is also useful. The Langmuir isotherm model incorporates two easily interpretable constants: qmax and b. Low values of b are reflected in the steep initial slope of a sorption isotherm, indicating a desirable high affinity. Thus, for ‘good’ sorbents in general, one is looking for a high qmax and a steep initial sorption isotherm slope (i.e. low b) (Kratochvil and Volesky, 1998). Any other comparison may carry an inherent error. The comparison of sorbent performance based on ‘% removal’ (percent of metal removal) is an often-used criterion encountered in the literature. However, it does not indicate the concentration range, and could lead to outright misleading conclusions on the relative sorption performance (Kratochvil and Volesky, 1998). The authors strengthened that, “even if all experimental parameters are given, this criterion can only result in a qualitative, and relative comparison (better or worse performance) that is adequate only for material screening purposes. Any figures given are essentially misleading because they lead to inadvertent and erroneous comparative calculations. The presence of other ions in solution can complicate the evaluation of the sorption system to a large degree, depending on the way the new solute species

interact with the sorbent and with the original one. Knowledge on these aspects may not be readily available. Appropriate and meaningful evaluation of a sorbent system with three or more metallic ions becomes even more complicated, if not impossible for all practical purposes.” ‘% removal’ can only serve the purpose of crude orientation, such as a qualitative comparison, often used for quick and very approximate screening of (bio)sorbent materials (Kratochvil and Volesky, 1998). To obtain the laboratory equilibrium sorption data, enough time must be allowed for the sorption system to reach equilibrium (Wang and Chen, 2006). A simple preliminary sorption kinetics test should be performed to determine the exposure time necessary for the given sorbent particles to reach the equilibrium state (characterized by unchanging sorbate concentration in the solution) by using timebased analyses (Volesky and Holan, 1995). The evaluation of equilibrium sorption performance needs to be supplemented by process-oriented studies of its kinetics and eventually by dynamic continuous-flow tests. The sorption rate of the metal uptake, together with the hydrodynamic parameters, determines the size of the contact equipment. These key process parameters could be used for comparison, for process design, and for scale-up purposes (Volesky and Holan, 1995). 10. Development of novel biosorbents Routinely lots of biosorbents, such as bacteria, fungi and algae are discovered and distinguished by trial and experiments. Some easily available biomass in their native state or after simple processing have been tested for their biosorption performance, in particular the biowaste generated as a by-product of large-scale industrial fermentation, olive mill solid residues, activated sludge from sewage treatment plants, biosolids, aquatic macrophytes, and other plant derived materials (Ahluwalia and Goyal, 2007). Bailey et al. (1999) introduced some low-cost sorbents, including biomaterials abundant in nature, or by-product or waste material from another industry, such as bark and other tannin-rich materials, lignin, chitosan and sea-food processing wastes, dead biomass and rice hulls, alginate from seaweed, peat moss, moss, bone gelatin beads, leaf mould, modified wool or modified cotton. As above-mentioned, chemical modification methods could increase/activate the binding sites on the biomass surface, they include pretreatment, binding site enhancement, binding site modification and polymerization (Vijayaraghavan and Yun, 2008). For example, the grafting of long polymer chains onto the biomass surface through direct grafting or polymerization of a monomer could introduce functional groups onto the surface of biomass. Deng and Ting (2005b) modified P. chrysogenum by graft polymerization of acrylic acid (AAc) on the surface of ozone-pretreated biomass. The sorption capacity for copper and cadmium increased significantly as a large number of carboxyl groups were present on the biomass surface,

Fig. 9. Comparison the performance of two biosorbents. Source: Kratochvil and Volesky, 1998.

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especially when the carboxylic acid group was converted to carboxylate ions using NaOH. Another method for developing novel biosorbent is genetic engineering technology which has the potential to improve or redesign microorganisms, to enhance the selectivity as well as the accumulating properties of the cells. Molecular biotechnology, a potent tool to elucidate the mechanism at molecular level, and to construct engineered organism with higher sorption capacity and specificity for objective metal ions, should be considered and applied in future. Many genes on metal-uptake or detoxification or tolerance have been identified (Rosen, 2002). For example, the S. cerevisiae Arr4p plays an important role in the tolerance of metal ions, such as As3+, As5+, Co2+, Cr3+, Cu2+, VO 3− 4 (Shen et al., 2003). Higher organisms produce cysteine-rich peptides, such as glutathione (GSH), phytochelatins (PCs) and metallothioneins (MTs) which could bind metal ions (Cd, Cu, Hg etc.). These peptides usually occurred in the animal kingdom, plants, eukaryotic microorganisms or some prokaryotes. MT, a specific metal-binding protein, can be induced by many substances, including heavy metal ions, such as Cd, Cu, Hg, Co, Zn etc. (Vijver et al., 2004). However, MT in S. cerevisiae can only be induced by Cu, hence called Cu–MT. Much attention has been paid to MT recently because of the potential application in metal removal. In addition to MT, other cellular thiols influencing the sensitivity to toxic metals include glutathione (GSH), phytochelatins (`cadystins (γ-Glu-Cys)nGly), labile sulfide (Gharieb and Gadd, 2004; Perego and Howell, 1997). Tripeptide glutathione (GSH) is a typical low molecular weight cellular thiol and functions as a storage form of endogenous sulfur and nitrogen as well as detoxification of metal ions. GSH in S. cerevisiae may account for 1% of the cell dry weight (Gharieb and Gadd, 2004). Based on the understanding of metal uptake mechanism, engineered technologies, including the cell surface display technology, have been used to improve the performance of biomass in metal removal from aqueous solution (Bae et al., 2003; Kuroda and Ueda, 2003; Kuroda et al., 2002). Kuroda et al. (2002) have constructed a cell surface-engineered yeast S. cerevisiae which displays histidine hexapeptide, the engineered yeast can chelate copper ion, and possesses the property of the self-aggregation, indicating the potential application for bioremediation of heavy metal pollution. Expression of MTs or PCs on the cell surface could dramatically increase the whole-cell accumulation of metal ions. Bae et al. (2003) reported that the metalloregulatory protein MerR, which exhibits high affinity and selectivity toward mercury, was exploited for the construction of microbial biosorbents specific for mercury removal. Whole-cell sorbents were constructed with MerR genetically engineered onto the surface of E. coli cells by using an ice nucleation protein anchor. The presence of surface-exposed MerR on the engineered strains enabled six-fold higher sorption capacity for Hg2+ biosorption than that found in the wild-type JM109 cells. Hg2+ binding via MerR was very specific, with no observable decline even in the presence of 100-fold excess Cd2+ and Zn2+. The Hg2+ binding property of the whole-cell sorbents was also insensitive to different ionic strengths, pH, and the presence of metal chelators. Bae et al. (2003) suggest that the microbial biosorbents overexpressing metalloregulatory proteins may be used similarly for the cleanup of other important heavy metals. Another attractive alternative strategy is to develop organisms harboring synthetic genes encoding protein analogs of PCs with the general structure (Glu-Cys)nGly (ECs) (Bae et al., 2000). A gene fusion system consisting of the signal sequence and the first nine amino acids of lipoprotein (Lpp) joined to a transmembrane domain from outer membrane protein A (OmpA) has been used successfully to anchor a variety of proteins and enzymes onto the cell surface (Richins et al., 1997). Bae et al. (2000) constructed the recombinant E. coli strains that anchor and display functional synthetic phytochelatins ranging from 8–20 cysteines (EC8, EC11, and EC20) onto the cell surface using this Lpp–OmpA fusion system. Synthetic genes encoding for several metal-

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chelating phytochelatin analogs (Glu-Cys)(n)Gly (EC8 (n = 8), EC11 (n = 11), and EC20 (n = 20)) were synthesized by Bae et al. (2000), linked to a lpp–ompA fusion gene, and displayed on the surface of E. coli. For comparison, EC20 was also expressed periplasmically as a fusion with the maltose-binding protein (MBP-EC20). Purified MBPEC20 was shown to accumulate more Cd2+ per peptide than typical mammalian metallothioneins with a stoichiometry of 10 Cd2+/peptide. Cells displaying synthetic phytochelatins exhibited chain-length dependent increase in metal accumulation. For example, 18 nmol of Cd2+/mg dry cells were accumulated by cells displaying EC8, whereas cells exhibiting EC20 accumulated a maximum of 60 nmol of Cd2+/mg dry cells. Moreover, cells with surface-expressed EC20 accumulated twice the amount of Cd2+ as cells expressing EC20 periplasmically. The ability to genetically engineer ECs with precisely defined chain length could provide an attractive strategy for developing high-affinity biosorbents suitable for heavy metal removal (Bae et al., 2000). Kambe-Honjoh et al. (2000) investigated the molecular breeding of yeast with higher metal-adsorption capacity by expressing the histidine-repeat insertion in the protein anchored to the cell wall. The genetic and protein engineering as the latest tools is possible to create “artificial’ protein polymers with fundamentally new molecular organization. The novel protein-based nano-biomaterials with both metal-binding and tunable properties for heavy metal removal is summarized by Kostal et al. (2005). Several different strategies for the selective removal of heavy metals such as cadmium and mercury are highlighted. 11. Application of biosorption A large amount of researches on metal biosorption have been published to elucidate the principles of this effective metal-concentration phenomenon during the past 30 years. Biosorption is regarded as a potential cost-effective biotechnology for the treatment of high volume low-concentration complex wastewaters containing heavy metal(s) (Wang and Chen, 2006). Some efficient natural biosorbents have been identified that require little modification in their preparation. There have been few investigations on determining the compatibility of the biosorbent for real industrial effluents. However, several attempts to scale-up the biosorption process or to commercialize the process based on experiences from conventional sorption operations have not been successful so far. The biosorption has not been applied yet, while it seems that biosorption could hardly have any competition in many types of large-scale environmental metal removal applications (Volesky and Naja, 2005) (http://biosorption. mcgill.ca/publication/BVibs05.pdf). 11.1. Several attempts of the biosorption commercialization Some commercial biosorbents were reported. In the early 1980s, the first patents appeared, claiming the use of specific microbial biomass types as biosorbents for wastewater treatment (Tsezos, 2001). In the early 1990s, other biomaterials were developed and commercialized, including AlgaSORB™ (C. vulgaris), AMT-BIOCLAIM™ (Bacillus biomass) (MRA), Bio-fix, etc., prepared by immobilization technology (Garnham, 1997; Veglio and Beolchini, 1997; Volesky, 1990c). The immobilization of the microbial biomass seems indispensable for biosorption application, and also can make use of traditional chemical engineering reactor configurations, such as upflow or downflow packed bed reactors, fluidized bed reactors. In the early 1990s, some enterprises in North America were mentioned in developing the biosorption system. B. V. SORBEX, Inc. in Montreal, Canada, have produced a series of biosorbents based on different types of biomaterial, including the algae S. natans, A. nodosum, Halimeda opuntia, Palmyra pamata, Chondrus crispus and C. vulgaris. The biosorbent was effective over a range of pH values and solution conditions, and can biosorb a wide range of metal

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ions. The metal biosorption was not affected by calcium or magnesium, it was also not affected by organics, and can be regenerated easily (Volesky, 1990c). Advance Mineral Technologies Inc. In Golden, Colorado, developed a broad-range metal-removal biosorbent based on Bacillus sp, but it stopped in late 1988 (Volesky, 1990c). AlgaSORB™ was produced by Bio-recovery Systems Inc. in Las Cruces, New Mexico. The biosorbent based on immobilised Chlorella (a freshwater alga) in silica or polyacrylamide gels. It can efficiently remove metal ions from dilute solution of 1 to 100 mg L− 1, thus may reduce the concentration to below 1 mg L− 1 or lower. The heavy metal biosorption was not affected by light metals such as Ca and Mg. The biosorbent resembles an ion-exchange resin and can undergo more than 100 biosorption–desorption cycles (Garnham, 1997; Kuyucak, 1990). AMT-BIOCLAIM™ (Visa Tech Ltd.) comprises of Bacillus subtilis. It was treated with strong caustic solution, washed with water, and immobilized as porous balls onto polyethyleneimine and glutaraldehyde, which can efficiently remove metal ions (Brierley, 1990; Garnham, 1997; Veglio and Beolchini, 1997; Vijayaraghavan and Yun, 2008). Brierley (1990) introduced the production and application of this kind of Bacillus-based biosorbent. AMT-BIOCLAIM™ based on Bacillus biomass can accumulate 2.90 mmol Pb g− 1, 2.39 mmol Cu g− 1, 2.09 mmol Zn g− 1, 1.90 mmol Cd g− 1 or 0.8 mmol Ag g− 1 metal cations with high efficiency of more than 99% from dilute solutions (Kuyucak, 1990). It is non-selective and metal(s) can be stripped using H2SO4, NaOH or complexing agents, and the granules can be regenerated for repeated use (Gupta et al., 2000). AMT-BIOCLAIMTM is able to accumulate gold, cadmium and zinc from cyanide solutions, and is therefore suitable for metal-finishing operations (Atkinson et al., 1998). The biosorbent BIO-FIX is made up of a variety of biomasses, including Sphagnum peat moss, algae, yeast, bacteria, and/or aquatic flora immobilized in high density polysulfone. This biosorbent is selective for toxic heavy metals over that of alkaline earth metals (Vijayaraghavan and Yun, 2008). U. S. Bureau of Mines (Golden, Colorado) produced the granular Bio-fix, which has been tested extensively for the treatment of acid mine waste (Garnham, 1997). The results showed the Zn binding to the biosorbent BIO-FIX is about 4fold higher than the ion exchange resins. The metal affinity followed: Al3+ N Cd2+ N Zn2+ N Mn2+, and a much lower affinity for Mg2+ and Ca2+. Metal(s) can be eluted using HCl or HNO3, and the biosorbent can be used for more than 120 extraction–elution cycles (Gupta et al., 2000). The type of these systems employed is dependent on the amount of flow to be processed, its composition, its continuity, and the regeneration conditions. From the process of application point of view, the design and operation of the biosorption are similar to the established technologies for ion exchange resin or activated carbon adsorption (Volesky, 1990c). In these systems, pre-treatment of a liquor may be required in some cases, depending on the suspendedsolids removal prior to biosorption (Volesky, 1990c). All the commercial biosorption enterprises, including both Biorecovery Systems and B. V. Sorbet, offer small “canisters” as flowthrough fixed-bed systems, as well as large-scale fluidized-bed, pulsed-bed systems, multi-element large-scale treatment schemes capable of handling flows in excess of 100 m3 d− 1 (Volesky, 1990c). Kuyucak (1990) investigated the treatment of wastewater in the flow rate ranging from 3.8 to 30 L/min using 79 kg of MRA, the result showed that the fluidized-bed contactors would offer optimum removal process using large amount of MRA. The performance of the several biosorbents were summarized by Volesky (1990c), the major features are as follows: high versatility for wide-range of operational conditions, metal selectivity and not influenced by alkaline earth and common light metals, independent of concentration (for ≤10 ppm or ≥100 ppm), high tolerance to organics, and convenient and effective regeneration (Volesky, 1990c). Immobilized R. arrhizus biomass was tested for recovery of uranium from an ore bioleaching solution (Veglio and Beolchini, 1997).

Two other commercialized biosorbents include ‘MetaGeneR’ and “RAHCO Bio-Beads”. They are effective to remove metal ions from electroplating or mining waste streams. Information related to their industrial application is still limited although the extensive laboratory and field trials were carried out (Atkinson et al., 1998). Metal biosorption by synthetic or biosynthetic chemicals was also investigated. For example, a kind of mercury-binding synthetic biosorbent, called Vitrokele™ 573, was prepared and used for mercury removal. This biosorbent is an insoluble composition comprising Hgbinding groups in particular cysteine, convalently fixed to the surface of a suitable insoluble carrier. The basic formula of the group is carrierR-Cys, where Cys is a cysteine residue, and R is a hydrocarbon chain (Huber et al., 1990). The batch and column tests demonstrated that mercury was efficiently removed from solution containing high concentration of sulfate and chloride. The biosorbent could be reused over multiple cycles (Huber et al., 1990). Another Vitrokele™ product was iron-binding synthetic biosorbent. The common groups binding iron are hydroxamates and phenolate–catecholates, usually found in siderophore (Huber et al., 1990). The catecholate type Vitrokele™ was tested in a column containing 600 μM radioactive iron, cobalt, sodium and cadmium. The Vitrokele™ showed good affinity for Fe, but poor affinity for Co and no affinity for Na or Cd. Unlike the commercial ion exchange resins, the Vitrokele™ could remove trace amounts of iron from artificial seawater in the presence of high concentration of other cations. It was not interfered by other cations and was not saturated quickly (Huber et al., 1990). Biosorption of metal ions and organics from industrial wastewater on full-scale was mainly focused on the biosorbent of peat during the past decades (Wase et al., 1997). Some peat on-site wastewater treatment systems for ion removal were operated in Maine, Alaska, Canada, and Ireland. The peat was regarded as utilizable and disposable. With the emphasis on using readily renewable biosorbents, peat-involving systems become much more engineered and much more specific, such as membrane-media extraction process developed by Harrison Western Environmental Services Inc. of Lakewood, Colorado. The process used peat moss capsules and was able to effectively treat As, Cd, Pb, Ni, Se and other metals from several type of wastewater, including electroplating rinsewater, pulp and paper mill discharge, municipal wastewater and acid mine drainage. In order to meet the renewable demand, another alternative is to take a pure component in a load-regeneration cycle system. The cellulosic sago waste was more effective than peat for Pb removal (Wase et al., 1997). Peat was regarded as the most successful and the rigorously scrutinized biosorbent in its natural state or in a modified form. Designs for large-scale peat-sorption processes are also available for application. However, the supply of peat is finite, and probably not the best biomaterial resource for commercialization. Thus, the development of other forms of biosorbents is essential (Forster and Wase, 1997; Wase et al., 1997). Three types of biomasses, including algae, fungi and waste biomass were suggested as potential biosorbents after predicting the future for biosorption application (Forster and Wase, 1997). 11.2. Application feasibility and consideration Although there are above-mentioned attempts to biosorption application or commercialization, Tsezos (2001), as well as Volesky and Naja (2005) pointed out that these attempts have failed to obtain successful commercial application. Obviously, biosorption application is facing with great challenges, although biosorption processes seem to have the following advantages: (1) versatility and flexibility for a wide range of applications; (2) robustness; (3) selectivity for heavy metals over alkaline earth metals; (4) ability to reduce metal concentration to very low level such as drinking water standards in some cases; (5) cost-effectiveness compared to alternative processes (Garnham, 1997).

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Volesky and Naja (2005) analyzed the feasibility of biosorption process in detail. They are optimistic on the biosorption future on a stage-wise approach. The assessment of the competing technologies (precipitation, reverse osmosis, ion exchange, bio-reduction), assessment of the market size, as well as assessment of cost of new biosorbents, all these should be considered with highest priority at the early stage in evaluation of the commercial potential and feasibility of application of the new technology based on the family of new biosorbent products (Volesky and Naja, 2005). After analysis, Volesky and coworkers proposed the following views: (1) Huge markets already exist for cheap biosorbents, because a large amount of heavy metal is released into waters from various polluting industries, and also because ion exchange ion is expensive. (2) The partnership approach is advisable for demand of innovative process ventures, i.e., a solid capitalization. Identification of potential synergies and partners appears to critical considering biosorption as a direct competitor of ion exchange resin. A handful of huge transnational companies controlling the ion exchange resin market are difficult in operative decision making. Dynamic consulting companies are not capital-rich entities although in an excellent position to acquire and push new process technologies into the marketplace. Pioneering and propagation of innovative biosorption process is not appealing mining and ore processing companies although they appear to be excellent “clients” for innovative clean-up technologies. The above-mentioned aspects make the wide industrial application of biosorption difficult despite of its excellent performance from the R&D angle. (3) Application of biosorption to treat the simulated AMD liquid waste, ready for demonstration tests, as an example, was introduced. From viewpoint of Volesky and coworkers, the enormous potential of biosorption application and its strong economic and technical advantages opens considerable market opportunities that can actually be quantified through a responsible market analysis (Volesky and Naja, 2005). Of course, there is still a lot of work required to do prior to the actual launching of the biosorption technology venture (Volesky, 2007). Kuyucak (1990) discussed the feasibility of biosorbents application. Metal situation, the cost of biosorbents, the capacity and selectivity, the fate of exhausted biosorbent, all these should be considered. He compared biosorption with the several existing technology, including evaporation and reverse osmosis techniques, membrane processes, precipitation and classification techniques, activated carbon and ion exchange resin. The biosorption exhibited some extraordinary properties as follows: (1) selective at low metal concentration; (2) low affinity for Ca and Mg; (3) effective over a broad range of conditions, including pH (3 to 9), temperature (4 to 90 °C); (4) meet the regulation; (5) low capital investment and low operation cost; (6) converting pollutant metals to a metal product, thus eliminating the cost and liability to dispose of toxic sludge. However, the fate of exhausted biosorbent in fact remains relatively unanswered (Vijayaraghavan and Yun, 2008). Precipitation and electrowinning procedures were supposed to recover metals from concentrated solution. However, the final disposal of the material should be addressed. Landfill or incineration still has their problems (Vijayaraghavan and Yun, 2008). Atkinson et al. (1998) think that the feasibility of a potential biosorbent for inorganics removal from industrial effluents should be considered. The biosorption needs to effectively compete both on a cost and performance basis with existing methods before industry accept and implement it. These factors include: (1) the effluent characteristics, such as volume, type of contaminant and competitive ions, solution chemistry, pH and temperature adjustment; (2) biomass characteristics, such as availability, mechanical stability, capacity, efficiency and metal selectivity of the biosorbent, ease of recovery and regenerative properties of the biomass, contaminant specificity and reaction kinetics, and immunity from interference by other effluent components or operating conditions; (3) process characteristics, such as capital and operating costs, economic and performance equivalence to existing chemical and physical processes, batch/continuous and

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land space requirements. In fact, proper and cheap immobilization techniques are vital for biosorption application, determining the design and type of process to be employed (batch/continuous). Kapoor and Viraraghavan (1997a) proposed several factors affecting the application of a biosorbent in practice: (1) the biosorptive capacity; (2) the availability of the biosorbent; (3) the cost of the biosorbent; (4) the ease of regeneration and subsequent use of the biosorbent; and (5) the ease with which the biosorbent can be used in various reactor configurations. Vijayaraghavan and Yun (2008) also offered some important features required for the successful application of biosorption technology to real situations. Kratochvil and Volesky (1998) strengthened and pointed out that the limited understanding of the metal biosorption mechanisms has hindered the application of biosorption. Selection of industrial effluents for pilot testing has remained largely intuitive. Therefore, exploring the mechanism of metal uptake by dead biomass was a real challenge for the field of biosorption. Cost is a major factor for application of biosorbent systems. The overall economics of the biosorbent was influenced mainly by the cost of procuring/growing the biomass and the cost of immobilization process. The cost of commercialized biosorbents must be considerably lower than ion-exchange resins, activated carbon and other agents. Bulk production costs of specifically cultured algae and fungi are in the order of £2000– £10000/tonne. The commercially supplied, dried seaweed cost in the order of £200–£300/tonne. Waste biomass including agricultural wastes will be expected considerable cheaper than this (Edyvean et al., 1997). Kuyucak (1990) discussed the cost of biosorbents and the economic assessment of biosorption process. Harvesting and drying are the major costs from marine algal biomass types. Usually the immobilization of biomass is simple and inexpensive, thus the source of raw biomass was the final cost of a biosorbent. The regeneration, kinetics, biosorption performance, and the like are all important factors for the cost of a biosorbent process. Although the full costs of an algal-based biosorption metal recovery system are not well documented, Garnham (1997) described some authors' work on the costs assessment. The cost assessment of two biosorption processes, alkaline precipitation and ion-exchange for treating electroplating waste (a total metal concentration was 60 mg L− 1, including nickel, cadmium, chromium and zinc), with a flow rate of 50000 gal/day, five days a week (1 gal = 4.5 L). It was found that the capital equipment price included metal removal, biosorbent regeneration and metal recovery systems, AMT-Bioclaim process based on B. subtilis exhibited a 50% saving over alkaline precipitation and a 28% saving over ion-exchange. The cost of the Bio-fix process (partially based on algal biomass) was comparable with lime precipitation. The result showed that the costs of both processes were similar per 1000 gal of waste treated, but the recovered metals from the biofix could offer some income (Garnham, 1997). Some pilot installations and a few commercial scale units constructed in the USA and in Canada, not only confirmed the applicability of biosorption as the basis for recovery process, but also helped people to realize the limitations of the industrial application of biosorption. There is absence of a reliable supply of waste microbial biomass suitable for biosorption application. Fermentation industry was reluctant or unable to secure a steady supply of waste microbial biomass as an inexpensive raw material. Furthermore, the immobilized biomass distribution, regeneration, recycling and re-use made the above issues even more complex and more difficult (Tsezos, 2001). 12. The future of biosorption Biosorption application is facing to great challenge, some investigators proposed several suggestion. Volesky and Naja (2005) think that the failure of the process commercialization is due to mainly nontechnical pitfalls involved in commercialization of technological

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innovations. As solid capitalization is required for innovative process ventures, partnership approach is perhaps advisable. However, the choice of partners appears to be critical. For the future of biosorption, there are two trends of biosorption development for metal removal. One trend is to use hybrid technology for pollutants removal (Tsezos, 2001), especially using living cells. Another trend is to develop good commercial biosorbents just like a kind of ion exchange resin, and to exploit the market with great endeavor (Volesky, 2007). The difficulties existing for biosorption application urge people to consider applying the hybrid technology which comprise of various processes to treat real effluents. Various biotechnology-based processes, such as biosorption, bioreduction and bioprecipitation were suggested. Consequently, application of living cells rather than dead cells for biosorption has gained attention again (Malik, 2004). The above-mentioned bioprocesses along with other non-biotechnology based processes, for example, chemical precipitation, flotation, electrochemical processes, membrane technology, may also be helpful for treating wastewater in large-scale, even for simultaneous removal of organic substances and heavy metal ions in solution. Some examples have been reported (Brady et al., 1994; Riordan et al., 1997; Thomas and Macaskie, 1996). All these processes may even possibly be realized in a single reactor, hence the corresponding novel reactors should be designed (Tsezos, 2001). Malik (2004) advised to use growing microbes as a feasible alternative to pure biosorptive removal of metal contaminants from complex industrial effluents. Tsezos (2001) suggested a hybrid technology either intra-biotechnological or inter-technological, making use of a combination of various processes, including biosorption. Biosorption is a desirable component in the design of flow sheets because the biosorption can effectively sequester dissolved metals out of dilute complex solutions in high efficiency and rapid intrinsic kinetics. These characteristics make biosorption an ideal candidate for the treatment of high volume low concentration complex waste waters (Tsezos, 2001). Biosorption appears to be suitable as secondary or polishing applications for metal removal from dilute waste streams, which would be competitive with ion-exchange resin based on final cost-beneficial analysis, and the greatest use for biosorption may be in modular system for small companies, e.g. for specific treatment (Edyvean et al., 1997). Another trend requires the improvement of biomaterials immobilization, as well as the optimization of the parameters of biosorption process and physicochemical conditions, including reuse and recycling. The mechanisms involved in biosorption or metal–microbe interactions should be further studied with great efforts (Wang and Chen, 2006). Market factor for successful application of biosorption should be considered. From Volesky's viewpoint (Volesky, 2007), the applications of certain types of biosorption are on the horizon, when the knowledge of biosorption is adequate, inviting the “new technology” enterprise ventures and presenting new and quite different challenges. Volesky (2007) thought that metals are only the “tip of the iceberg”. He pointed out a completely different type of biosorption, focusing on the purification and recovery of high-value proteins, steroids, pharmaceuticals and drugs like digoxin or vinblastin, not for environmentally oriented low-cost biosorption but for the product recovery of the high-priced pharmaceuticals. For example, antibodies as a biosorbent for locking and thus extracting, recovering and purifying the one desirable target molecule out of the mixture. The sources and type of biosorbent play a major role in determining the overall cost of the biosorbent material. If the biomass needs to be specifically cultured for this purpose, manufacturers will incorporate maintenance and production expenses in the total cost, as well as a commercial fee. These costs can be minimal where certain biomass types such as photo-autotrophic algae (e.g., Chlorella and Oscillatoria spp.) can be successfully grown for large-scale commercial use due to their minimal growth requirements (water, sunlight and CO2). Marine algae such as S. fluitans and A. nodosum have shown

biosorptive potential although the costs of harvesting the biomass may prove inhibitory to its application. Many industrial wastebiomass types have been investigated for their biosorptive potential. These include the yeasts, S. cerevisiae from the food and beverage industry and Candida albicans, a clinical isolate; the moulds, R. arrhizus from the food industry, P. chrysogenum from antibiotic manufacturers and A. niger from citric acid and industrial enzyme producers; the bacteria, Bacillus spp., utilized in amino acid and antibiotic fermentations and Streptomyces noursei from the pharmaceutical industry. These potential biosorbents can usually be obtained relatively free of charge from the respective producers since they already present disposal problems to them. The only costs incurred should be those of drying, if required, and transport. These low-cost biosorbents will make the process highly economical and competitive particularly for environmental applications in detoxifying effluents of e.g. — metal-plating and metal-finishing operations; — mining and ore processing operations; — metal processing, battery and accumulator manufacturing operations; — thermal power generation (coal-fired plants in particular); — nuclear power generation (etc.). The researchers of various types of scientific background, from engineering to biochemistry, working together, will make a significant contribution to elucidating the biosorption mechanisms. Interdisciplinary efforts are mandatory and represent quite a challenge. The optimization of specific biosorption process applications has to be done in conjunction with industrial users/clients and requires specific process engineering expertise and a serious development capital commitment. A variety of investigation demonstrated that biosorption is a useful alternative to the conventional systems for the removal of heavy metal ions from aqueous solution. The development of biosorption process requires further investigation in the direction of modeling, of regeneration and immobilization of biosorbents, and of treating the real industrial wastewater. Acknowledgements The authors would like to acknowledge the financial support from the National Natural Science Foundation of China (Grant Nos. 50830302; 50808111; 50278045), China Postdoctoral Science Foundation funded project (Grant No. 20080430350), special fund of State Key Joint Laboratory of Environment Simulation and Pollution Control (Grant No. 08K05ESPCT) and the Basic Research Fund of Tsinghua University (Grant No. JC2002054). References Ahluwalia SS, Goyal D. Microbial and plant derived biomass for removal of heavy metals from wastewater. Bioresour Technol 2007;98:2243–57. Aksu Z. Application of biosorption for the removal of organic pollutants: a review. Process Biochem 2005;40:997-1026. Aksu Z, Acikel U, Kutsal T. Application of multicomponent adsorption isotherms to simultaneous biosorption of iron(III) and chromium(VI) on C. vulgaris. J Chem Technol Biotechnol 1997;70:368–78. Akthar N, Sastry S, Mohan M. Biosorption of silver ions by processed Aspergillus niger biomass. Biotechnol Lett 1995;17:551–6. Al-Saraj M, Abdel-Latif MS, El-Nahal I, Baraka R. Bioaccumulation of some hazardous metals by sol–gel entrapped microorganisms. J Non-Cryst Solids 1999;248:137–40. Alasheh S, Duvnjak Z. Adsorption of copper and chromium by Aspergillus carbonarius. Biotechnol Prog 1995;11:638–42. Arica MY, Kacar Y, Genc O. Entrapment of white-rot fungus Trametes versicolor in Caalginate beads: preparation and biosorption kinetic analysis for cadmium removal from an aqueous solution. Bioresour Technol 2001;80:121–9. Atkinson BW, Bux F, Kasan HC. Considerations for application of biosorption technology to remediate metal-contaminated industrial effluents. Water Sa 1998;24:129–35. Avery SV, Tobin JM. Mechanisms of strontium uptake by laboratory and brewing strains of Saccharomyces cerevisiae. Appl Environ Microbiol 1992;58:3883–9. Awofolu OR, Okonkwo JO, Roux van der Merwe R, Badenhorst J, Jordaan E. A new approach to chemical modification protocols of Aspergillus niger and sorption of lead ion by fungal species. Electron J Biotechnol 2006;9:340–8. Bae W, Chen W, Mulchandani A, Mehra RK. Enhanced bioaccumulation of heavy metals by bacterial cells displaying synthetic phytochelatins. Biotechnol Bioeng 2000;70:518–24.

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