Potential of Fungal Laccase in Decolorization of Synthetic Dyes

CHAPTER 7

Potential of Fungal Laccase in Decolorization of Synthetic Dyes Abha Mishra, Sudhir Kumar, Aditi Bhatnagar Biomolecular Engg Laboratory, School of Biochemical Engineering, Indian Institute of Technology (BHU), Varanasi, Uttar Pradesh, India Laccase (E.C. 1.10.3.2, p-benzenediol: oxygen oxidoreductases) is an oxidoreductase able to catalyze the oxidation of various aromatic compounds (particularly phenolic compound) with the reduction of oxygen to water (Chawachart et al., 2004). Laccases are predominantly present in fungi and higher plants (Messerschmidt and Huber, 1990) and also in a lower proportion in insects and bacteria. Yoshida in 1883 reported first about the enzyme from the Japanese lacquer tree Rhus vernicifera, exudates from which the name laccase was derived (Levine, 1965; Thurston, 1994). In 1896, Bertrand and Laborde demonstrated the presence of laccases in fungi. Since then, the presence of laccase was shown in Ascomycetes, Deuteromycetes, and Basidiomycetes, and white-rot fungi found to be involved in the lignin metabolism (Thurston, 1994). Laccase redox potential (450e800 mV) is reported to be lower than other ligninolytic peroxidases (>1 V); it was initially presumed that laccases would only be able to oxidize phenolic substrates (Kersten et al., 1990). However, the oxidation of substrates can be enhanced by mediator-involved reaction mechanism. Mediators often used for increasing laccase activity are of low molecular weight compounds and in some cases, unstable and highly reactive cationic radicals, have an ability to oxidize variety of substrate before returning to their original state. Finally, laccase transfer electron to oxygen to form water (Mc Guirl and Dooley, 1999). More than 100 fungal laccases have been purified and characterized and the threedimensional structure of fungal and bacterial laccases have been reported such as Trametes versicolor (Bertrand et al., 2002), Pycnoporus cinnabarinus (Antorini et al., 2002), Melanocarpus albomyces (Hakulinen et al., 2002), Rigidoporus lignosus (Garavaglia et al., 2004), Coprinus cinereus (in a copper Type 2-depleted form) (Ducros et al., 1998), and CotA laccase from Bacillus subtilis (Enguita et al., 2003), Lentinus (Panus) tigrinus (Ferraroni et al., 2007), Thielavia arenaria(Kallio et al., 2011), Coriolopsis caperata (Glazunova et al., 2015), and Aspergillus niger (Ferraroni et al., 2017), etc. Microbial Wastewater Treatment. https://doi.org/10.1016/B978-0-12-816809-7.00007-5 Copyright © 2019 Elsevier Inc. All rights reserved.

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128 Chapter 7 The class of enzyme which reduces dioxygen to water and especially multicopper oxidase family (the only enzyme not in this class being cytochrome-c oxidase, a heme/copper containing enzyme) were identified as laccase. The basic nature of laccase is a polyphenol oxidase, which means it can oxidize a phenolic substrate and can initiate a polymerization reaction. Laccases vary greatly with respect to their degree of glycosylation, molecular weight and kinetic properties depending on their sources. The laccase reaction mechanism may be explained as the reduction of molecular oxygen by different organic compounds to water and no formation of hydrogen peroxide (Yaropolov et al., 1994). Laccases exhibit a high affinity for oxygen as their electron acceptor, but have a low affinity for their reducing substrates (Fernandez-Sanchez et al., 2002). It also catalyzes the oxidation of mono- and polyphenolic substrates and aromatic amines by removal of a single electron, to form a free radical or removing hydrogen atom from their hydroxyl group (Yaropolov et al., 1994). Burke and Cairney (2002) proposed that laccase action is mediated by (1) type-1 copper reduction by the reducing substrate, (2) internal electron transfer from type 1 copper to type 2 and type 3 copper trinuclear cluster, (3) molecular oxygen reduction to water at type-2 and type-3 copper atoms. The catalytic mechanism of action of laccase gaining considerable attention and several researchers worked on interaction of laccase with its various substrates by crystallography and X-ray diffraction studies (Ducros et al., 1998; Antorini et al., 2002; Bertrand et al., 2002; Piontek et al., 2002; Ferraroni et al., 2017). The fungal laccase molecule usually contains four copper (Cu) atoms, although some of them contain only three Cu atoms in its structure. Laccase has a molecular mass from about 50e100 kDa and its optimum pH is in the range of 3.0e5.0 (Heinzkill et al., 1998). Laccases can be polymeric, and the enzymatically active form can be a monomer, dimer, trimer or tetramer. The lignin degrading enzymes are laccase, oxidises phenolic compounds to phenoxy radicals; lignin peroxidase, which catalyzes the oxidation of both phenolic and nonphenolic units, manganese-dependent peroxidase (Baldrian, 2006). Ligninolytic enzymes found to be extracellular in nature (Johansson, 1999) but there are reports on intracellular laccases in fungi e.g., Neurospora crassa was found to contain intracellular as well as extracellular laccases (Kunamneni, 2007). Yaropolov et al. (1994) explained the lignin decomposition by laccases and the polymerization of lignin oxidation products, but this function could be the characteristic of the ligninolytic fungi as evident from the work of different researchers such as Botryospheria sp. From Ascomycete (Barbosa et al., 1996); Pleurotus ostreatus (Bollag and Leonowicz, 1984; Ardon et al., 1996; Palmieri et al., 1993); Trameters hirsuta (Bollag and Leonowicz, 1984; Rogalski et al., 1991); Phlebia radiate(Niku-Paavola et al.1990); Coriolus hirsutus (Gindilis et al., 1988); Agaricus bisporus(Wood, 1980); Pleurotus spp. (Prasad et al., 2005) etc. from Basidiomycete, from Deuteromycete such as Botrytis cineres (Bollag and Leonowicz, 1984); Rhizoctonia praticola (Bollag and Leonowicz, 1984; Xu et al., 1998);

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Trichoderma sp (Assavanig et al., 1992); Myceliophthora thermophila (Xu, 1996); Rhizoctonia solani (Wahleithener et al., 1996; Xu et al., 1996); Pycnoporus sanguineus (Herna´ndez et al.,2017) etc. The role of laccases in lignin degradation has been demonstrated by laccase mutants of Pycnoporus cinnabarinus by Eggert et al. (1997). Plants laccase involved in lignification, whereas fungal laccase are involved in many cellular processes, such as sporulation, pigment production, delignification, fruiting body formation and plant pathogenesis (Brijwani, 2010; Knezevic et al., 2016). The laccasemediated lignin degradation is an oxidative reaction with the loss of one electron from the phenolic hydroxyl groups of lignin which in turn produces phenoxy radicals, this further lead to cleavage of lignin side chains, specifically alkyl chains. Laccases are important in fungi in fruiting body formation. It was observed that laccase activity increased during the formation of fruiting bodies, which indicates a possible function in their evolution. Laccase synthesis was observed to be a principal factor in growth and development of rhizomorphs in Armillaria mellea, it was observed that the growth of rhizomorph formation was decreased on addition of laccase inhibitors. Laccase have also been reported to confer virulence property to the fungus Botyritis cinerea and the host plant was unaffected by the fungus when laccase was inhibited in the growing culture on addition of some suppressor (Gianfreda et al. 1999). Virulence property was also reported in Heterobasidion annosum where laccase concentration was proportional to the aggressiveness of the root pathogen (Johannsson et al., 1999). Laccase was also reported to be involved in melanin biosynthesis (Dijkstra and Walker, 1991), sclerotization in insects (Barrett, 1987) and in the formation of humus (Stevenson, 1994).

1. Laccase Production Studies Many scientists are working in the field of laccase production under submerged fermentation (SmF) and solid-state fermentation using different microorganisms, raw materials(substrate) and other physio-chemical parameters at different scales. Dominguez et al. (2001) designed a rotating drum reactor (RDR) for ligninolytic enzymes production under SSF conditions. This bioreactor was able to operate in batch and continuous mode. Bohmer et al. (2006) elaborated on the temporary immersion RITA-System (Recipient a Immersion Temporaire Automatique) as a bioreactor for laccase production by white-rot fungi and its application to synthetic dye decolorization. Songulashvili et al. (2015) worked on submerged fermentation in a 120-L scale stirred bioreactor with white rot fungus Cerrena unicolor C-139 in the presence of wheat bran as a lignocellulosic substrate for laccase production. Successive micro- and ultrafiltration (5 kDa) of fermented broth a liquid concentrate with 22,203,176 units of laccase was reported. Couto et al. (2003) worked on bioreactor configurations such as immersion, expanded bed and tray with

130 Chapter 7 different agitation systems (mechanical, pneumatic and static, respectively) for laccase production by T. versicolor under SSF conditions using an inert (nylon sponge) and a noninert (barley bran) support. They found that the tray configuration with barley bran as support-substrate led to the highest laccase activities. Couto et al. (2006) compared two bioreactor configurations immersion and tray for laccase production by T. hirsuta using grape seeds as support-substrate and found that much higher laccase activities in the tray bioreactor. Also, there are reports on much high laccase production in tray bioreactor for T. hirsuta on ground orange peelings (Rosales et al., 2007). Couto (2018) discussed the cost-efficient production of laccase enzymes by solid-state fermentation (SSF) using organic wastes as support-substrates. The pretreatment of corn stalk lead to the disruption of the compact lignocellulosic structure, which increases the surface area and soluble compounds for the utilization by Trametes versicolor, it was also reported by Adenkunle et al. (2017) that this process of pretreatment released high level of the phenolic compounds which are considered to be inducers of laccase. Laccase production by the steam-exploded corn stalk (SCS) was 2.1-fold greater than that from the raw corn stalk. The organic solid wastes (food wastes) are high in moisture and rich in carbon. Most of the wastes are directly incinerated with other combustible wastes and residual ash is disposed of in landfills. Agricultural products such as corn, potato and wheat containing large amounts of starchy substrate have been preferred as raw materials for fermentation (Hofvendahl and Hahn-Ha¨gerdal, 1997). It is expected that food wastes, which are supplied constantly at lower costs and are rich in carbohydrate, could be suitable renewable resources in substitution of agricultural products. The microorganisms need supply of various nutrients in media such as naturally occurring organic nitrogen for growth. These nutrients can be selected from a number of materials including yeast extracts, polypeptones, meat extracts, defatted soybeans, defatted soybean hydrolysates (HVP), corn steep liquors (CSL), cotton seed meals, peanut meals, pharmamedia, distiller’s solubles, livestock bloods, butchery wastes, casein hydrolysates. Nutrients used in the culture media in commercial fermentation should be low in cost, abundant in supply without seasonal irregularities, stable in quality. Only HVP, CSL and yeast extracts among the above listed nutrients meet the above requirements (Frondosa et al., 2011). Commercial application of enzyme may be enhanced by searching less expensive substrates, as opposed to a chemically defined medium (Berka et al., 1997; Yaver et al., 1999; Papinutti et al., 2003). The use of agricultural wastes such as cotton stalk extract (Ardon et al., 1996; Castillo et al., 1997), corn straw extracts (Crestini et al., 1996) and potato waste (Trojanowski et al., 1995) for production studies have yielded significant quantities of laccase. Agrowaste such as sugar cane baggase (Perumal and Kalaichelvan, 1996) and olive oil mill wastewater (Sanjust et al., 1991) have also been investigated as potential nutrient sources for the production laccase. The use of industrial effluents gives not only an economical growth medium but has the ability to use for bioremediation of the.

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Laccases, are inducible or constitutively expressed as reported by Bollag and Leonowicz (1984) and Yaver et al. (1996). The constitutive or noninducible group, do not react to dissolved compounds that exhibit properties similar to their substrates, and furthermore no inducer producing significant improvements in their yield. Single inducers may not induce the desired response of laccase production, and a mixture of inducers may be required for the enhanced activity (Marbach et al., 1985). Most of these compounds have some similarity with lignin molecules or other phenolic chemicals (Farnet et al., 1999). Veratryl (3,4-Dimethoxybenzyl) alcohol is an aromatic compound and important in lignin synthesis and degradation. Many white-rot fungi was reported with enhanced laccase production on addition of veratryl alcohol in fermentation media (Barbosa et al., 1996). Ethanol was found to trigger laccase production indirectly and affect the growth rate (Lee et al., 1999). Various recognition sites may present on the promoter region of laccase genes that could be specific for heavy metals and xenobiotics (Sannia et al., 2001). Their presence in the medium may affect the recognition sites and induces laccase production. The inducers may increase specific laccase concentration or induce the production of new isoforms of the enzyme. Action of inducers vary with different fungus or fungal strain (Eggert et al., 1996). They found that the xylidene addition had a significant effect on laccase production. On addition of 10 mM xylidine after 24 h of cultivation gave the highest induction with nine-fold increase of lacasse activity. On the contrary at higher concentrations the xylidene has inhibitory nature, probably due to toxicity. Laccase offers protection to the fungus against toxic phenolic monomers of polyphenols. Lee et al. (1999) investigated the inducing effect of alcohols on the laccase production by Trametes versicolor. The enhanced laccase activity was comparable to those obtained using 2,5-xylidine and veratryl alcohol (Mansur et al., 1997). The addition of ethanol to the cultivation medium was found to cause a reduction in melanin formation. The monomers, when not polymerized to melanin, then acted as inducers for laccase production (Lee et al., 1999). Ethanol can act as an indirect inducer of laccase activity and offers a very economical way to enhance laccase production. Lu et al. (1996) found hyphal branching and the expression and secretion of laccase have strong chemistry. The cellobiose can induce profuse branching in certain Pycnoporus species and consequently increases laccase activity. The addition of cellobiose and lignin can increase the activity of extracellular laccases without an increase in total protein concentration (Garzillo et al., 1998). The addition of low concentrations of copper to the cultivation media of laccase producing fungi stimulates its production (Assavanig et al., 1992). Palmieri et al. (2000) found that the 50 times increase of laccase activity in the presence of 150 mM copper sulfate to the cultivation media as compared to a synthetic basal medium. Syringaldazine was used as substrate by Cordi et al. (2007) to study pH (3.0e8.0) effect on laccase activity. Isoenzymes of laccase such as L1 acts in acidic range, at optimum pH 4.0 but optimum pH for L2 was 5.0. Laccase enzyme of Trametes versicolor function optimally at

132 Chapter 7 pH 3.0 at 50
C (Han et al., 2005). Purified laccase of Stereum ostrea functions optimally at temperature 40
C and pH 6.0 (Valeriano et al., 2009). Mishra and Kumar (2009) reported Kinetic studies of laccase enzyme of Coriolus versicolor MTCC138 in an expensive culture medium which was having strong ability to decolorize synthetic dyes. Cyanobacterial biomass of water bloom, groundnut shell (GNS) and dye effluent was used as culture medium for laccase enzyme production by Coriolus versicolor. Laccase production was found to be 10.15  2.21 U/mL with groundnut shell and cyanobacterial bloom in a ratio of 9:1 (dry weight basis) in SmF at initial pH 5.0 and 28  2
C temperature. The half-life of the enzyme was found to be 74 min at 60
C (Mishra and Kumar, 2009). L1 (isoenzyme of laccase) was stable at 60
C with 100% activity on 20 min incubation whereas at 70
C residual activity was found to be 47% whereas L2 isozyme retained only 28.1% of initial activity after 20 min incubation at 60
C (Cordi et al.,2007). D’Souza-Ticlo et al. (2009) extracted three laccases LI, LII and LII of different molecular masse from mangrove (Cerrena unicolor) and studied for optimization of physical parameters such as pH and temperature and it was found that the optimum pH was 3.0 and 70
C temperature in all the three cases. The crystal structures of laccases help in designing new laccases with better substrate specificity/affinity, catalytic efficiency, and/or stability. Bertrand et al. (2002) identified two amino acid residues, a histidine that coordinates the copper acting as the first electron acceptor and an aspartate that conserved among fungal laccases interacts with the amino group of 2,5-xylidine. Different amino acid residues that make hydrophobic interactions with the aromatic ring of the substrate are being studied and explored for site directed mutagenesis to improve the properties of laccase such as specific activity and optimal pH (Ducros et al., 1998). Xu et al. (1998) were studied the use of site directed mutagenesis for potentially important laccase amino acids (Xu et al., 1998). Laccase genes, named lac3 and lac4, encoding proteins of 547 and 532-amino acids preceded by 28 and 16-residue signal peptides, respectively, were cloned from the edible basidiomycete Coprinus comatus by Gu et al. (2014). Both the genes showed 70% identity but homology with other fungal laccases at protein level were very low (less than 58%). Pichia pastoris was taken as expression system for these laccase isoenzymes by fusing an additional 10 amino acids (Thr-Pro-Phe-Pro-Pro-Phe-Asn-Thr-Asn-Ser) tag at N-terminus. The laccase activity increased from undetectable level to 689 and 1465 IU/L for Lac3 and Lac4, respectively (Gu et al., 2014). Higher decolorization efficiency was exhibited by Lac3 than Lac4 on various synthetic dyes. The very moderate synergistic decolorization by two laccases was noticed for triphenylmethane dyes but not for anthraquinone and azo dyes. Anions such as halides, azide, cyanide and hydroxide bind to the type 2 and 3 copper atoms of laccases which disrupts the electron transfer system, resulting in enzyme inhibition (Gianfreda et al., 1999). The inhibition by hydroxide generally prevents catalysis of substrates at alkaline pH (Xu, 1997). The inhibition of activity by hydroxide prevents auto-oxidation at

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alkaline pH, with a resultant increase in stability at alkaline pH (Xu, 1996). The extent of inhibition by halides depends on the laccase isozyme and therefore likely related to the size of the channel of the trinuclear cluster (where oxygen binds) (Xu, 1996). Other types of inhibitors include certain metal ions (e.g., Hg2þ), fatty acids, sulphydryl reagents, hydroxyglycine, kojic acid, and cationic quaternary ammonium detergents (Gianfreda et al., 1999). The laccase activity was altered these chelators by acting on the copper (II) atoms, and may elicit a conformational change in the glycoprotein (Xu, 1996). Laccase from Coriolopsis gallica was modified with polyethylene glycol (PEG: 5000 MW) to improve catalytic efficiency (Vandertol Vanier et al., 2002). 1300-fold improvement of catalytic efficiency of laccase was reported for syringaldazine oxidation and a 1000-fold improvement in oxidation of polycyclic aromatic hydrocarbons.

2. Decolorization of Synthetic Dyes by Laccase Dyes that are manufactured from organic molecules are called synthetic dyes; they are unlike natural dyes that can be extracted from flowers, wood, minerals, insects etc. Synthetic dyes can be manufactured accurately giving exactly same color and intensity in every batch by the use of computer color matching (CCM) technique. Synthetic dyes are harmful for our environment as they get accumulated in water bodies and are mostly nonbiodegradable Exposure to large doses of these compounds is toxic and has adverse effects to the human body (Chacko et al., 2011). Synthetic dyes also consist of heavy metals like mercury, lead, chromium, copper and aromatic compounds like toluene and benzene which are toxic to environment and humans if consumed in doses above permissible limit. Unlike natural dyes synthetic dyes are used commercially worldwide as they provide wide range of hues and high color stability. Classification of dyes can be done based on their chemical composition, color, and type of fibers they are applied to also their method of application. The Society of Dyers and Colourists (SDC) and the American Association of Textile Chemists and Colorists (AATCC) classify dyes by their chemical composition and a Color Index constitution number (CI number) is given to them for identification. The conventional methods used in the textile industry for color removal from effluents include physicochemical methods like coagulation/flocculation and activated carbon adsorption. Both flocculation and adsorption generate large amounts of sludge and waste, which require separate treatment before disposal (Chacko et al., 2011) (Table 7.1). Large amount of industrial applications for laccases have been proposed, and they include food, pulp and paper, textile, organic synthesis, environmental, pharmaceuticals and nanobiotechnology. Laccase-based biocatalysts are specific, energy-saving, and biodegradable, fits well with the development of highly efficient, sustainable, and ecofriendly industries.

134 Chapter 7 Table 7.1: Type of synthetic dyes. Types of dyes Acidic

Basic

Azoic

Direct

Disperse

Reactive

Properties Anionic in nature Suitable for wool, silk, polyamide and modified acrylics Not suitable for cellulosics Combine with the fiber by hydrogen bonds, van der waals forces or through ionic linkages Cationic stain Aniline dyes • great tinctorial strength Brightness

Directly insoluble in water Insoluble azo group present in it Used in cellulosic materials Alkaline coupling is necessary Are water soluble Have affinity for cellulose Benzidine derivatives Sodium salts of aromatic compounds Water insoluble Dye polyester and acetate fibers Color dissolves in hydrophobic fibers Forms covalent bond between fibers Color cellulosics

Advantages

Limitations

Examples

Can be kept for long periods without loss of color Soluble in water Safe and easy to use Can be permanently fixed to fiber with heat

Can cause irritation if inhaled poor washing fastness

Alizarin yellow Azophloxin Bismarck brown R

Moderate substantively Relatively economical High Tinctorial strength Wide shade range Shows good brightness Good color fastness Used for lighter shades Brightness is great Wash fastness is good

High acid content Colored backwaters Poor shade stability Preferential dyeing Very poor light fastness

Methylene blue Crystal violet Basic fuchsine safranin Mauvenine

Application time required is more Good for only small amount of material

Acid orange Alcian yellow Amaranth

Color fastness to light is good Lower cost fabrics produced

Color fastness to laundry is bad

Brilliant yellow Direct black 38 Chlorazol violet N Direct yellow 12

Colorfastness is excellent Leveling is good Temperature required low Bright colors Good color fastness good color stability

Low solubility Could make polymer structure loose Volatility can lead to loss of color density Can be damaged by chlorine bleaches

Disperse violet 33 Disperse red 60 Disperse blue 26

Remazol brilliant blue R Supra Procion T Cibacron C

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135

Table 7.1: Type of synthetic dyes.dcont’d Types of dyes Vat

Mordant

Sulfur

Properties Insoluble in water Derivative of indigo dyes Anthraquinone also present Applied on cotton and cellulosics Negatively charged Have no affinity for textile fibers Requires mordant for application have hydroxyl and carboxyl groups Metallic salts are used with them Contain thiozine ring Water insoluble Treated with reducing agents to make them water soluble Usually amorphous

Advantages

Limitations

Examples

High color fastness

Poor rubbing fastness

Vat blue 1 Vat blue 30 Vat blue 20 Vat blue 4 Vat blue 21

Prevents color bleeding Good color fastness Can brighten others dyes ecofriendly

Can cause irritation and inflammation when inhaled Range of shade is limited

Mordant brown 33 Mordant red 3 Mordant yellow 1 Mordant yellow 10

Cheap Good wash fastness Easy to apply

Have limited range of hues Lacks brightness Susceptible to damage by chlorine

Sulfur black 1 Sulfur blue BRN Sulfur yellow GC

The two-thirds of the total dyestuff market comprised of textile industry (Riu et al., 1998) and wet processing of textiles require water in very large quantity and also the chemicals. The chemical reagents requirement is very diverse e.g., from inorganic compounds to polymers and organic compound and their chemical composition (Mishra and Tripathy, 1993; Banat et al., 1996; Juang et al., 1996). There are more than 100,000 commercially available dyes with over 7105 t of dyestuff produced annually (Meyer, 1981; Zollinger, 2002). Several dyes are made from known carcinogens such as benzidine and other aromatic compounds (Baughman and Perenich, 1988). Processes to treat dye wastewater in current times are ineffective and not economical (Cooper, 1995). Use of laccases found to be an ecofriendly alternative in degrading dyes of diverse chemical structure used in the industry (Abadulla et al., 2000; Blanquez et al., 2004; Hou et al., 2004). Table 7.2 highlights the laccase uses in dye decolorization. Laccases have many possible applications in bioremediation (Xu et al., 1999; D’Acunzo et al., 2002). To degrade plastic waste having olefin units laccase may be applied since, an oxidation of the olefin units by the laccase mediator system (LMS), could initiate a radical chain reaction, leading to the disintegration of the plastic. Also, this LMS can be used to

136 Chapter 7 Table 7.2: Laccase catalyzed degradation of synthetic dyes. Microorganism name Pycnoporus sanguineus Pycnoporus cinnabarinus

Pleurotus sajor-caju

Trametes versicolor

Coprinus cinereus

Pleurotus ostreatus

Marasimus scorodonius

Trametes hirsuta

Ganoderma lucidum Coriolopsis gallicia

Sclerotium rolfsii

Podocypha elegans

Dyes targeted Orange G Amaranth Reactive black 5 Reactive blue 19 Acid blue 74 Acid red 18 Acid black 1 Direct blue 71 Alizarin red 5 Acid orange 7 Acid blue 74 Reactive red 2 Reactive black 5 Orange g Crystal violet Malachite green Blue H3R Yellow FG Red 3B Malachite green Crystal violet Congo red Methyl green Reactive orange 16 Reamazol brilliant blue R Acid blue Reactive black 5 Basic red 9 Acid blue 74 Remazol brilliant blue R Remazol black 5 Remazol brilliant blue R Reactive black 5 Bismarck brown R Lanaset gray G Remazol brilliant red Indigo Lancet marine blue Diamond black Orange G Congo red Direct blue 15 Rose Bengal Direct yellow 27

References Pointing et al. (2000) Prasad et al., 2012

Murugesan et al.,2006

Ramirezmontoya et al. (2015)

Lin et al. (2013)

Abdulredha et al. (2014)

Jeon et al. (2017)

Castillo et al. (2012) Abadulla et al. (2000)

Murugesan et al., 2007 Daassi et al. (2014)

Ryan et al. (2003)

Pramanik et al. (2018)

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degrade polyurethanes (Kimura, 2006). LMS facilitated the degradation of phenolic compounds (environmental hormones) from biphenol and alkylphenol derivatives (Saito et al., 2004). Laccase could be used for the removal of foul odor from places such as livestock farms, garbage disposal sites, pulp mills (Xu et al., 2004). Laccase also finds its use in decolorizing dye house effluents which are hard to carry out by conventional sewage treatment plants (Maximo et al., 2004). Laccases can decolorize waste waters from olive oil mills (D’Annibale et al., 2000) and pulp mills (Manzanares et al., 1995) by removing colored phenolic compounds. Laccase found to have potential environmental application in the field of bioremediation of contaminated soils, as laccases and LMS are able to oxidize toxic organic pollutants, such as various xenobiotics, polycyclic aromatic hydrocarbons, and chlorophenols (Duncan, 2004). Laccase finds its role in various industrial processes, such as production of organic chemicals, coal conversion, olive oil, and petroleum refining, and others where the phenolic compounds are present (Aggelis et al., 2003). Hublik et al. (2000) reported use of immobilized laccase for the removal of phenolic and chlorinated phenolic pollutants. Laccase was used for the transformation of 2,4,6- trichlorophenol to 2,6-dichloro-1,4hydroquinol and 2,6-dichloro-1,4-benzoquinone by Leontievsky et al. (2000). LMSs found to have application in oxidizing alkenes, carbazole, N-ethylcarbazole, fluorene, and dibenzothiophene (Bressler et al., 2000). Herbicide, e.g., isoxaflutole in soils and plants gets converted to its diketonitrile derivative, the active form and it was reported that laccases can convert diketonitrile into acid (Mougin et al., 2000). Synthetic heterocyclic compound such as halogenated organic pesticides in the soil can also be reduced by laccase (Duncan, 2004). Oxidation of recalcitrant PAHs, main components of several ship spills found to be reduced by LMS and was utilized in various enzymatic bioremediation programs (Alcalde et al., 2006). Laccases considered as potential candidate for different biotechnological applications because of its broad substrate specificity. Phenolic and nonphenolic subunits of lignin compounds were reported to be oxidized by laccase (Vasdev and Kuhad, 1994). Laccases action on variety of substrate range is mainly due to its nonspecific formation of a free radical from a substrate and air oxygen as a second substrate. Another attractive feature of laccase is its oxidative action on uncharacteristic substrates by the addition of low molecular weight chemicals which are termed mediators. These mediators improve the applicability of laccases for bioremediation (Fernandez-Sanchez et al., 2002; Johannes and Majcherczyk, 2000). Several naturally occurring mediators of fungal origins have been identified as phenol, aniline, 4-hydroxybenzoic acid and 4-hydroxybenzyl alcohol (Johannes and Majcherczyk, 2000). Several artificial mediators have also been identified which include 2, 20 azino-bis-(3-ethylbenzothiazoline-6-sulfonic acid) (ABTS) and 1-hydroxybenzotriazole (HBT). Despite the fact that mediators may broaden the action of laccase but are of limited use due to their toxic nature (Bermek et al., 2002). Sometimes

138 Chapter 7 laccase may indirectly involved in the catalytic process on variety of substrate through the addition of a recognized substrate, which in turn indirectly oxidize other compound (a secondary substrates), since it cannot bind to the active site of the enzyme because of steric hindrance or may exhibit a higher redox potential than that possessed by the enzyme alone. The most frequently used mediators of laccase for industrial applications are ABTS [2-20 -azino-bis-(3-ethylbenzothiazoline-6-sulfonic acid)] and HBT [1hydroxybenzotriazole] (Johannes and Majcherczyk, 2000). Nowadays, over 200 mediators have been identified but the choice of mediator is an important parameter since the mediator may affect the final outcome by forming other byproducts, or acting a specific oxidation depending on its redox potential or structure (d’Acunzo et al., 2002; Johannes and Majcherczyk, 2000). Coprinus comatus laccase isoenzyme was induced by synthetic dyes and production studies were made. Jiang et al. (2013) made decolorization studies of synthetic dyes such as anthraquinone, azo, and triphenylmethane, by crude laccases of different isoenzymes produced under selected culture conditions showed that the LacA is the key isoenzyme contributing to dyes decolorization especially in the presence of 1-hydroxybenzotriazol.) Similar studies were also made on synthetic dyes were made by Legerska et al., (2016). Induction of laccase by synthetic dyes in Pycnoporus sanguineus and its possible use for sugar cane bagasse delignification was studied by Hernandez et al. (2017). The significant effect of addition of different synthetic dyes such as carminic acid (CA), alizarin yellow, to liquid cultures of Pycnoporus sanguineus on laccase production was also reported by Hernandez et al. (2017). Frondosa et al. (2011) studied major laccase isozyme from Grifola frondosa (Lac 1) for decolorizing of synthetic dyes and bisphenol A degradation. The oxidative capability of Lac 1 toward synthetic dyes and bisphenol A was enhanced in the presence of the redox mediator, 1-hydroxybenzotriazole. The major product from the degradation of bisphenol A by Lac one was determined to be 4-isopropenylphenol (Nitheranont et al., 2011). Yang et al. (2017) isolated Trametes versicolor CBR43 having high laccase and Mn-dependent peroxidase, but low lignin peroxidase activity. The strain was able to decolorize >90% of 200 mg L1 acid dyes (red 114, black 172 and blue 62) and reactive dyes (blue 4, orange 16, black five and red 120) in 6 days of fermentation. 200 mg L1 acid orange was 67% decolorized within 9 days. Disperse dyes (black 1, red 1, and orange 3) were decolorized almost 51%e80% within 9 days. The rate of dye decolorization rate was maximum at 150 rpm, 28
C and pH 5, Potato Dextrose Broth medium. Decolorization of six synthetic dyes by three sources of fungal laccase of Aspergillus oryzae, Trametes versicolor and Paraconiothyrium variabile were investigated by Forootanfar et al. (2012). Among them, the enzyme from P. variabile was the most efficient in decolorizing bromophenol blue (100%), commassie brilliant blue (91%), panseu-S (56%), ramazol brilliant blue R (RBBR; 47%), Congo red (18.5%), and methylene blue (21.3%) on 3 h incubation with hydroxybenzotriazole (HBT; 5 mM) as the laccase mediator (Forootanfar et al., 2012).

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Laccase of A. oryzae was efficient in decolorization of methylene blue 53% and 26% of RBBR after 30 min incubation in absence of HBT, but the enzyme could not efficiently decolorize other dyes even in presence of HBT(5 mM). In the case of laccase from T. versicolor, only RBBR was decolorized (93%) in absence of HBT after 3 h incubation. Zeng et al. (2011) reported the decolorization of synthetic dyes by crude laccase from a newly isolated Trametes trogii strain in solid state fermentation using agro-industrial residue. Crude enzyme extract of T. trogii found to decolorize 85.2% Remazol Brilliant Blue R, 69.6% Reactive Blue 4% and 45.6% Acid Blue 129 without redox mediators, 90.2% Acid Red 1% and 65.4% Reactive Black 5 with the addition of 1 mM 1hydroxybenzotriazole in 30 min (Zeng et al., 2011).Catalytic property of laccase of Coriolopsis caperataDN was studied to decolorize and detoxify RBBR dye and action of laccase significantly reduced toxicity (phyto-, cyto-, and micro-) of RBBR dye (Patel et al., 2017). Decolorization of Reactive Blue 19 (RB19) dye by laccase from Ganoderma sp. was optimized using response surface methodology (RSM) and it was found to be 1.27 times efficient than traditional single factor approach (Ohammadian-Azli et al., 2010). Crude Laccase from the white-rot fungus Trametes pubescens was optimized using RSM for decoloration of diazo dye Reactive Black 5 (RB5) by wherein three variables laccase redox mediator HBT, RB5 dye was used to optimize the decolorization efficiency. The optimum concentrations of laccase 500 U/l, HBT1.17 mM, RB5 150 mg/L for 60% decoloration of RB5 dye in 20 min (Roriz et al., 2009). Theerachat et al. (2012) conducted synthetic dye decolorization study by whole cells and a laccase enriched extract of Trametes versicolor DSM11269. They reported that the anthraquinone derivative dyes Alizarin Red S and Remazol Brilliant Blue R were decolorized in 3 h at 50
C by 55% and 70%, respectively. The azo compounds Cibacron Brilliant Red 3B-A, Amaranth, Reactive Black 5, Direct Blue 71 and the indigo molecule (Indigo Carmine), showed a higher resistance to decolorization (<10% in 6 h), but Amaranth, Reactive Black 5 and Indigo Carmine) were efficiently decolorized by T. versicolor in agar plate assays. This suggested that different oxidizing activities from laccase alone may be involved in the decolorization process (Theerachat et al., 2012). Bio-bleaching of industrial textile dyes, including anthraquinonic dyes, indigoid, az and triarylmethane by laccase has been studied by several workers (Abadulla et al., 2000; Zilly et al., 2002). Almost half of the synthetic dyes constitute azo dyes, and its different forms. Amino-substituted azo dyes are considered to be very toxic, sometimes mutagenic and carcinogenic (Selvam et al., 2003). Recent developments in processing to treat azo dye wastewater produces huge amount of sludge furthermore not much effective in degrading dye mixtures. Therefore, enzyme which has an ability to degrade these wastes has large potential market (Lorenzo et al., 2002). Enzymatic treatment especially by fungal laccases utilizing oxidative mechanisms to degrade azo dyes has an advantage over other microorganisms is that it do not form hazardous breakdown products such as anilines

140 Chapter 7 which is generally the product of reductive cleavage of azo dyes (Call and Mu¨cke, 1997; Martins et al., 2003). White-rot fungi Lentinus edodes, showed dye decolourization ability both in and dyes used were Reactive Red 195 (0.025%), Reactive Blue 19 (0.05%), Reactive Black 5 (0.05%) and Reactive Yellow 145 (0.05%) (Minussui et al., 2001). Font et al. (2003) studied white-rot fungus Trametes versicolor for decolorization, detoxification of black liquors from a soda pulping mill. Though T. versicolor known to produce Laccase, lignin peroxidase (LiP), and manganese peroxidase but only laccase activity was detected. The amount of aromatic compounds and Chemical Oxygen Demand (COD) had been determined. The fungal pellets was used in aerated reactors (air-pulsed reactors, fluidized and stirred), COD of 60%, aromatic compounds of 70%e80% and reductions in color were noticed because of the activity of laccase. Ramsay and Nugyen (2002) reported decolorization of Tropaeolin O, Reactive Blue 15, Amaranth, Congo Red and Reactive Black five by Trametes versicolor with no uptake of dye by the fungus. Cibacron Brilliant Yellow 3B-A, Cibacron Brilliant Red 3G-P and Remazol Brilliant Blue R were decolorized partly with some dye uptake by the biomass. Lentinus sp a fungal strain produces extracellular laccases (58,300U/L). 61% Acid Red 37, 88& RBBR and 97% Acid Blue 80 were delocolrized by purified laccase of Lentinus sp.(lacc3). Protein dye interaction were made by structural modeling. RBBR was making hydrogen bonds with Ser134, His132, Asp482, Acid Red 37 with Arg178 and Acid Blue 80 with arg178, Arrg182. Reversal of toxicity of Anthroquinone and azo dyes by lcc3 reported in textile effluent treatment (Hsu et al., 2012). Becker et al. (2016) studied the removal of antibiotics in wastewater by enzymatic treatment with fungal laccase. The immobilized laccase (Trametes versicolor) was investigated in combination with the mediator syringaldehyde (SYR) in removing a mixture of 38 antibiotics in an enzymatic membrane reactor (EMR) and these type of enzymatic treatment may be a valuable addition to existing water treatment technologies Becker et al. (2016). The decolorization studies were made on variety of synthetic dyes by Trametes sp. SQ01 strain, including azo, triphenylmethane and anthraquinone dyes. Best substrate was found to be RBBR (anthraquinone) for the enzyme in the study. The pH4.5 was reported to be optimum for dye decolorization, at this pH the decolorization efficiency was >85% at 25.8
C on 20 min incubation. Among all azo dyes tested, FBRR, Amino black 10B and Orange G were good substrates for the laccase and extent of degradation were completed in 12 h. Bromphenol Blue was the best substrate for the laccase, degraded completely in 4 h whereas least degradation was observed in Acid Red, as only 21% was degraded in 12 h. Congo Red and Crystal Violet were degraded by 47% and 65%, respectively, but on further incubation no changes were observed. Laccase of Trametes sp. SQ01, when incubated with different dyes CBB G250, Acid Red, CongoRed, Crystal Violet and Cresol

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Red and color changes were observed for 12e16 h, it was reported that beyond 16h of incubation no decolorization observed (Xiu et al., 2009). D’Souza-Ticlo et al. (2005) reported the effect of laccase on alcohol, pulp and textile effluents. Effluents decolorization studies were made by fungal laccases which was produced with different types of nitrogenous sources. Mishra and kumar (2011) reported laccase enzyme production in an inexpensive culture medium also studied the simultaneous dye decolorization. Setti et al. (1999) exploited laccase in the bleaching of textiles and even to synthetic dyes. An industrial application of laccase enzyme in denim finishing was launched by Novozyme (Novo Nordisk, Denmark) in 1996 as DeniLite, and was also the first bleaching enzyme acting with mediator molecule. A formulation based on LMS was developed by Zytex (Zytex Pvt. Ltd., Mumbai, India) in 2001 with the trade name as Zylite. Laccase is used in commercial textile applications to improve the whiteness in conventional bleaching of cotton and recently biostoning (Zhu et al., 2005). Cellulases are generally used to reduce the load of pumice stones partially and laccases have ability to bleach indigo-dyed denim fabrics to lighter shades (Xu, 1999). Laccase also can be used in situ to convert dye precursors for better, more efficient fabric dyeing (Kitamoto et al., 2004). Potential applications of laccases are in cleansing, such as cloth and dishwashing (Someya et al., 2003). Laccase may be included in a cleansing formulation to eliminate the odor on fabrics, including cloth, sofa surface, and curtain, or in a detergent to eliminate the odor generated during cloth washing (Wolfgang et al., 2005). The use of laccase-mediator systems (LMS) to increase the shrink resistance of wool was patented by Yoon (1998). Also, Lantto et al. (2004) found that wool fibers can be activated with LMS. Therefore, the use of laccase for anti-shrink treatment of wool seems very attractive phenomena. The potential multicopper oxidase (IOX) by Iodidimonas sp. Q-1 for decolorization of recalcitrant dyes was determined (Taguchi et al., 2018). Redox meadiators was needed for IOX activity since it did not decolorize any dyes in the absence of redox mediator. Amido Black, Indigo Carmine, Orange G, and Remazol Brilliant Blue R (RBBR) was decolorized in the presence of iodide. More than 50% decolorization was observed in wastewater discharged of dyeing factory. IOX-iodide system is advantageous because of its low price, naturally occurring and nontoxic as compared to other mediator systems for decolorization of recalcitrant dyes. Immobilized form of enzymes are stable, resistant to environmental changes with easy recovery and multiple reuse than free enzymes. Immobilization method are generally used for enhancing the stability of enzymes in unfavorable conditions. Different immobilization methods and substrates were used to study laccases. Peralta-Zamora et al. (2003) reported different matrices for immobilization of laccase from Trametes versicolor such as modified amberlite IRA-400, modified glass-ceramic (with carbodiimide/glutaraldehyde) and silica (with imidazole groups). Studies on decolorization of textile reactive dyes were made on these supports. Prasad et al. (2006) noticed the enhanced expression of laccase when

142 Chapter 7 immobilized on PUF cubes. Immobilization of laccase were also made on different vitroceramics supports, such as pyrolytic graphite and also on a carbon fiber electrode (Minussi et al., 2007). Fabrication of an optical biosensor by using stacked films of 3methyl-2-benzothiazolinone hydrazone (MBTH) immobilized in a hybrid nafion/solegel silicate film and chitosan film was conceptualized and executed by Alimin Abdul and Annuar (2009), for phenolic compounds detection. The natural support medium like clay or soil are desirable since it possess no environmental risk and can be useful for bioremediation on terrestrial system (Ahn et al., 2002). The benefits of immobilization may however be offset by the increased cost and loss of enzyme activity during immobilization (Ahn et al. 2002). Chhabra et al. (2015) studied on decolorization of azo dye AR 27 by laccase immobilized in PVA-nitrate. The dye degradation studies showed that AR 27 underwent degradation to smaller moieties and polymerization products can be avoided through continuous decolorization process by providing appropriate hydraulic retention time. Laccase from Coriolopsis gallica UAMH8260 was immobilized on activated agarose was tested for repeated decolorization of industrial dyes. Decolorization studies of Reactive Blue 198 dye by immobilized enzyme showed 85% of activity after 10 cycles, and 70% after 3 months of intermittent use. Immobilized laccase was found to have higher thermal stability at 70
C than free enzyme (Reyes et al., 1999). Laccase from Trichoderma harzianum strain HZN10 produced using wheat bran under solid state fermentation and used in decolorization of synthetic dyes. Laccase was entrapped in various matrix such as calcium alginate, copper alginate, calcium alginateechitosan beads and solegel system. Optimization studies showed that laccase immobilized in solegel was optimally active in wide pH range (4.0e7.0) and thermo-stable (50e70
C) than free enzyme which was optimum at 50
C and pH 6.0. Malachite Green, congo red and methyl blue were used for decolorization studies by free and immobilized laccase. Findings reported as 100% of malachite green, 90% of methylene blue and 60% of congo red dyes decolorized with initial concentration of 200 mg/L within 16, 18 and 20 h, respectively by laccase immobilized in solegel matrix in the presence of 1-hydroxybenzotriazole (HBT) mediator (Bagewadi et al., 2017). Laccase from Trametes modesta immobilized on g-aluminum oxide pellets and enzyme reactor was attached to different UV/Vis spectroscopic sensors allowing the continuous online monitoring of the textile dye decolorization. Working with different types of commercial textile dyes it was found that for decolorization the process was not limited to a certain structural group of dyes. Indigo Carmine, Anthrachinonic dyes (Lanaset Blue 2R, Terasil Pink 2GLA), some azo dyes, and the triphenylmethane dye Crystal Violet were efficiently decolorized. However, the laccase showed substrate specificities when a range of structurally related model azo dyes was used for biotransformation. Hydroxy groups in ortho or para position when present on azodyes azo bonds were preferentially oxidized (Kandelbauer et al., 2004). Studies on decolorization of triarylmethane, indigoid, azo, and anthraquinonic dyes by Trametes hirsuta and a purified laccase showed that initial decolorization velocities depended on the

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derivatives present on the phenolic rings of the dyes. Immobilization of the T. hirsuta laccase on alumina increases the heat stability of the enzyme and its tolerance against some enzyme inhibitors, like copper chelators, halides and dyeing additives (Abadulla et al., 2000).

3. Concluding Remarks Broad substrate specificity of laccase has made it an interesting area for its biotechnological applications. The enzyme shows high affinity toward aromatic compounds having phenolic, methoxyl, and methyl groups but no affinity toward a nitro group bearing benzene ring or toward nonphenolic ligninerelated compounds. It may form an enzyme-mediator complex when there is a redox barrier between the substrate and the enzyme. Thus, the laccases from different natural sources may be helpful in overcoming the drawbacks of currently available commercial laccases.

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