Applications of biosynthesized metallic nanoparticles – A review

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Contents lists available at ScienceDirect

Acta Biomaterialia journal homepage: www.elsevier.com/locate/actabiomat

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Review

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Applications of biosynthesized metallic nanoparticles – A review

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Adam Schröfel a,b,e,⇑, Gabriela Kratošová c, Ivo Šafarˇík a, Mirka Šafarˇíková a, Ivan Raška e, Leslie M. Shor b,d a

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Department of Nanobiotechnology, Institute of Nanobiology and Structural Biology of GCRC, Academy of Sciences, Ceske Budejovice, Czech Republic Department of Chemical and Biomolecular Engineering, University of Connecticut, Storrs, CT, USA c Nanotechnology Centre, VSB-Technical University in Ostrava, Ostrava, Czech Republic d Center for Environmental Sciences & Engineering, University of Connecticut, Storrs, CT, USA e Charles University, Institute of Cellular Biology and Pathology, Prague, Czech Republic b

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a r t i c l e

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Article history: Received 16 January 2014 Received in revised form 13 April 2014 Accepted 21 May 2014 Available online xxxx

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Keywords: Biosynthesis Metallic nanoparticles Nanomedicine Bioimaging Sensors

a b s t r a c t We present a comprehensive review of the applications of biosynthesized metallic nanoparticles (NPs). The biosynthesis of metallic NPs is the subject of a number of recent reviews, which focus on the various ‘‘bottom-up’’ biofabrication methods and characterization of the final products. Numerous applications exploit the advantages of biosynthesis over chemical or physical NP syntheses, including lower capital and operating expenses, reduced environmental impacts, and superior biocompatibility and stability of the NP products. The key applications reviewed here include biomedical applications, especially antimicrobial applications, but also imaging applications, catalytic applications such as reduction of environmental contaminants, and electrochemical applications including sensing. The discussion of each application is augmented with a critical review of the potential for continued development. Ó 2014 Acta Materialia Inc. Published by Elsevier Ltd. All rights reserved.

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1. Introduction

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The unique properties of nanoscale materials have given rise to tremendous research activity directed towards nanoparticle (NP) fabrication, characterization and applications. In order to reveal ever more favorable NP functionality, some researchers look to nature for methods to produce NPs with novel properties or enhanced function. Many organisms are known to form inorganic materials either intra- or extracellularly. For example, iron-reducing bacteria have been known to reduce labile and/or toxic metals into their zero-valent form [1]. The same or similar metal-reducing capability used as an NP production method is called biosynthesis [2]. As reviewed recently, many different prokaryotic and eukaryotic organisms have been used to produce metallic NPs [3], and biosynthesis of NPs has attracted increasing attention in the past 10 years [4]. Among the key advantages that the biological approach has over traditional chemical and physical NP synthesis methods is the biological capacity to catalyze reactions in aqueous media at standard temperature and pressure. Production in aqueous media under standard conditions leads to many cost advantages, in terms of both capital equipment and operating expenses, especially in the

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⇑ Corresponding author at: Charles University, Institute of Cellular Biology and

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purchase and disposal of solvents and other consumable reagents. Biosynthesis can be implemented in nearly any setting and at any scale [3]. In addition, extensive investment in biotechnology know-how for optimized production of food, pharmaceuticals and fuels also informs NP biosynthesis techniques. One important drawback of NP biosynthesis methods is the requirement in some applications to purify the sample or to separate the NPs from the Q3 biological material used in their synthesis (See Figs. 1–6). The properties of biosynthesized materials may differ from materials prepared by other methods. Biosynthesis can result in forms that are difficult to make using other techniques, such as alloys and wires. Biosynthesized NPs can also have enhanced stability and biocompatibility and reduced toxicity, mainly due to coating them with biogenic surfactants or capping agents. The potential range of sizes, shapes and compositions of biosynthesized NPs translates into a broad domain of existing and new nanomaterial applications. Applications of biosynthesized metal-based NPs range from various biomedical purposes (e.g. antimicrobial coatings, medical imaging and drug delivery) to catalytic water treatment and environmental sensors. We have organized this review according to the applications that use biosynthesized NPs. The chemical composition, form and organism used for the biosynthesis are also described.

Pathology, Prague, Czech Republic. Tel.: +420 777864404; fax: +420 224917418. E-mail address: [email protected] (A. Schröfel). http://dx.doi.org/10.1016/j.actbio.2014.05.022 1742-7061/Ó 2014 Acta Materialia Inc. Published by Elsevier Ltd. All rights reserved.

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Fig. 1. Light microscopy of gold nanoparticle biosynthesis inside the moss leaf. The purple color indicates the presence of gold nanoparticles inside the cells (picture taken and kindly provided by Markéta Bohunická).

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2. Biomedical applications

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Applications of metallic NPs in the biomedical fields are numerous, and there is strong potential for continued growth in this area. Metallic NPs are widely used for their antimicrobial functionality; for example, silver NPs (AgNPs) have been incorporated into wound dressings, bone cements and implants [5]. Gold NPs (AuNPs) have medically relevant optical and anticancer properties. For example, Alanazi et al. [6] describe how surface plasmon absorption and surface plasmon light scattering can be used for diagnostic and therapeutic applications, and Patra et al. [7] describe the fabrication and application of AuNPs for targeted cancer therapy. As described by Pankhurst et al. [8,9], magnetic NPs appear promising for targeted drug delivery and hyperthermia applications.

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2.1. Antimicrobial applications

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The ongoing development of antimicrobial agents is important Q4 due to the continuous selection of antibiotic resistance traits in bacteria and other pathogens. Different metallic NPs, including

titanium, copper, magnesium and particularly silver and gold, are known for their antimicrobial, antiviral and antifungal capabilities [10]. These metallic NPs are actively investigated as disinfectants, in food processing, and for use as additives in clothing and in medical devices [11]. The following sections describe the key antibacterial, antiviral and antifungal properties described in the literature for biosynthesized NPs (Tables 1 and 2). However, due to the large number of papers describing antimicrobial activity using slightly different materials, endpoints or methods, in some cases only representative examples are provided.

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2.1.1. Antibacterial activity AgNP exposure causes toxicity to bacteria, primarily from Ag ions released into aqueous solution following partial oxidation [5]. Ag ions and small NPs interact with the plasma membrane, disturbing cellular functions, including permeability and respiration, and ultimately leading to lysis. AgNP exposure can prevent DNA replication and protein synthesis by binding to DNA or by denaturizing ribosomes [5]. The detailed mechanisms of AuNP antibacterial functionality against Escherichia coli is described by Cui et al. [12]. AuNPs were shown to collapse membrane potential, strongly inhibiting ATPase activity and resulting in a decrease in cellular ATP levels. Another consequence of AuNP exposure was inhibited binding of tRNA to the ribosome subunit. Bacterial susceptibility to antimicrobial agents can depend on the cell wall structure. Bacteria are classified into two categories, based on their cell wall structure: Gram-negative (G) bacteria have a multi-layer cell wall and Gram-positive (G+) bacteria have a single-layer cell wall. Antibacterial activity of biosynthesized NPs has been studied for both types of bacteria. A variety of biological materials have been used for the biosynthesis of NPs with demonstrable antibacterial effects. These materials include fungal, bacterial and algal biomass, as well as extracts of botanical materials, including leaves, bark, roots and tubers. One of the first reports of antibacterial effects of biosynthesized NPs was published by Vigneshwaran et al. [13]. These authors used the edible mushroom Pleurotus sajor-caju for the synthesis of AgNPs and performed successful antimicrobial testing against

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Fig. 2. Antimicrobial activity of AgNPs synthesized by S. hygroscopicus. (a) Candida albicans; (b) Bacillus subtilis; (c) Escherichia coli; (d) Enterococcus faecalis; (e) Salmonella typhimurium; (f) Saccharomyces cerevisiae. Each plate shows (A) culture supernatant; (B) AgNO3 control; (C, D) synthesized AgNPs, respectively. Reprinted from Ref. [15] with permission from Elsevier.

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Fig. 3. Probable anti-proliferative mechanism of AuNP. Reprinted from Ref. [49] with kind permission from Springer Science and Business Media.

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Staphylococcus aureus (G+) and Klebsiella pneumoniae (G) bacteria. Raheman et al. [14] reported the extracellular synthesis of AgNPs by means of an endophytic fungus, Pestalotia sp., isolated from leaves of Syzygium cumini and the antimicrobial properties of AgNPs against S. aureus (ATCC-25923) and Salmonella typhi (ATCC-51812). Synergistic effects were observed for combined exposure to biosynthesized AgNPs and the commercially available antibiotics gentamycin and sulphamethizole. Antimicrobial properties of bacteria-biosynthesized NPs were illustrated in two studies by Sadhasivam et al. [15,16]. Streptomyces hygroscopicus cells were used for biosynthesis of Ag- and AuNPs with antimicrobial properties against Bacillus subtilis, Enterococcus faecalis, E. coli, Salmonella typhimurium, Staphylococcus epidermidis and S. aureus. An example of algae-based NP biosynthesis is described by Merin et al. [17], where AgNPs with antibacterial properties were synthesized by the microalgal strains Chaetocerus calcitrans, Chlorella salina, Isochrysis galbana and Tetraselmis gracilis. These NPs showed antimicrobial properties against K. pneumoniae, Proteus vulgaris, Pseudomonas aeruginosa and E. coli, as measured using a clearing zone assay. Venkatpurwar and Pokharkar [18] introduced a method for synthesis of AgNPs using sulfated polysaccharides isolated from the marine red alga Porphyra vietnamensis. The dose-dependent effect of AgNPs synthesized in this study revealed strong antibacterial activity against E. coli (G) and lesser effectiveness against S. aureus (G+). The synthesis of antibacterial AuNPs using powder or ethanolic extract from a marine alga Galaxaura elongata was demonstrated by Abdel-Raouf et al. [19]. These authors also performed spectroscopy experiments in order to identify the algal compounds which may play a role as reducing agents or nanoparticle capping agents.

By far the most abundant studies on biosynthesized antibacterial NPs are those using plant tissues and extracts as reducing agents. As previously mentioned, biosynthesized NPs may require purification to remove pathogenic or poisonous compounds, particularly for materials intended for use in vivo. One approach to avoiding toxicity concerns is to use only well-characterized and benign botanical extracts for biosynthesis [20]. For example, green tea extract (prepared from Camellia sinensis leaves) is a widely used reducing agent used in the biosynthesis of NPs. Vaseeharan et al. [21] used tea extract to prepare AgNPs with demonstrated antibacterial activity against Vibrio harveyi. Other botanical extracts have been used for biosynthesis of antimicrobial AgNPs. Stem callus extract of bitter apple (Citrullus colocynthis) was used for AgNPs synthesis and demonstrated activity against biofilm-forming E. coli, Vibrio paraheamolyticus, Pseudomonas aeruginosa, Proteus vulgaris and Listeria monocytogenes [22]. No activity was observed in the case of Proteus mirabilis, Salmonella enteritidis or Staphylococcus aureus. Kaviya et al. [23] studied biosynthesis of AgNPs using navel orange (Citrus sinensis) peel extract and demonstrated antibacterial activity against E. coli, Pseudomonas. aeruginosa and S. aureus. Finally, Nagajyothi and Lee [24] used Chinese yam (Dioscorea batatas) rhizome extract for the biosynthesis of antibacterial AgNPs. Several reports have described synergistic antimicrobial effects of phytosynthesized nanoparticles used in combination with antibiotics. Ghosh et al. [25] synthesized AgNPs prepared with tuber extract of Dioscorea bulbifera, then measured synergistic antimicrobial potential using 22 types of commercially available antibiotics and seven bacterial strains. For instance, they found an 11.8-fold inhibition efficiency increase when streptomycin and AgNPS are used in combination against E. coli compared with the inhibition efficiency using streptomycin only.

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Fig. 4. Optical images (right column) and reconstructed images from the intensity of Raman spectra with excitation at 514 nm (left column) and 633 nm (middle column), for encapsulated cells before (top line) and after (second line) gold production and for free cells before (third line) and after (bottom line) gold production. Reproduced from Ref. [61] by permission of The Royal Society of Chemistry.

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Plant extracts have also been used for the biosynthesis of AuNPs with antibacterial activity. Kumar et al. [26] used a deciduous tree (Terminalia chebula) extract for the biosynthesis of AuNPs effective against S. aureus and E. coli. MubarakAli et al. [27] used Mentha piperita leaf extract for biosynthesis of AuNPs and AgNPs, and likewise demonstrated antimicrobial effects against S. aureus and E. coli bacteria. Biosynthesized metallic NPs that are immobilized on cotton cloth have many important applications as material for wound dressings. For example, Durán et al. [28] reported the extracellular production of AgNPs mediated by the fungus Fusarium oxysporum. Here, AgNPs were incorporated into cotton fabrics for inhibition of S. aureus. However, one limitation of immobilized AgNPs in fabric is the loss of the Ag ions, and sometimes the AgNPs, with washing. El-Rafie et al. [29,30] demonstrated the use of immobilized biogenic AgNPs on cotton fabric. In these studies, the AgNPs were prepared with Fusarium solani and were applied to cotton fabrics using an acrylate based binder. The cotton fabric showed a high antimicrobial efficiency of approximately 90% against S. aureus and E. coli after 20 washing cycles. Tripathi et al. [31] examined biosynthesis of AgNPs using an aqueous extract of Azadirachta indica leaves and their subsequent immobilization on cotton cloth. These authors observed the bactericidal effect against E. coli and S. aureus with washing in distilled water. Similarly, the biosynthesis of AgNPs in Eucalyptus citriodora and Ficus bengalensis leaf extracts and their loading into cotton fibers

Fig. 5. Electron micrograph of palladized cells of Shewanella oneidensis (kindly provided by Simon de Corte).

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was reported by Ravindra et al. [32]. Cotton fibers were immersed in the leaf extract containing AgNPs, kept on a shaker for 24 h and then tested against E. coli using a modified disk diffusion method. Antibacterial effect against E. coli was also tested in AgNPs that were prepared by means of the extract and powder of Curcuma longa tubers [33], then immobilized on cotton cloth. AgNPs were resuspended in water or in polyvinylidene fluoride (PVDF), then sprayed over pre-sterilized cotton cloth. Cloth treated with NPs in PVDF exhibited lower antibacterial activity but much longer reusability. Recently, antimicrobial applications for biosynthesized AgNPs incorporated into nonwoven fabrics have been demonstrated. Yang and Li [34] prepared AgNPs using mango peel extract and demonstrated the antimicrobial effectiveness of these nanoparticles immobilized on non-woven fabrics against E. coli, S. aureus and B. subtilis. Sundaramoorthi et al. [35] described a wound-healing application for biosynthesized AgNPs, prepared extracellularly using the Q5 fungus Aspergillus niger. The efficiency of the AgNPs was demonstrated following excision in a rat model. The study supported both the antimicrobial effects of Ag and the ability of AgNPs to modulate cytokines involved in wound healing. Similarly, the medicinal plant Indigofera aspalathoides was used for biosynthesis of AgNPs tested in wound-healing applications following excision in animal models [36]. Finally, biogenic AgNPs derived from Chrysanthemum morifolium have been added to clinical ultrasound gel. In the study, the gel was used on an ultrasound probe, and the bactericidal activity and instrument sterility were evaluated [37].

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2.1.2. Antifungal activity Several studies have described the bacteria Aspergillus niger antifungal activity of biosynthesized NPs. Gajbhiye et al. [38] described the antifungal properties of biosynthesized NPs against Phoma glomerata, P. herbarum, Fusarium semitectum, Trichoderma sp. and Candida albicans in combination with fluconazol (a triazole antifungal drug). AgNPs biosynthesized by another fungus, Q6 Alternaria alternata, enhanced the antifungal activity of fluconazole against all tested strains except P. herbarum and F. semitectum. In another study, mycelia-free water extracts of the fungal strain Amylomyces rouxii were used for biosynthesis of AgNPs that were effective against the bacteria Shigella dysenteriae type I, Staphylococcus aureus, Citrobacter sp., E. coli, Pseudomonas aeruginosa and Bacillus subtilis, and also against the fungi Candida albicans and Fusarium oxysporum [39]. Antifungal activity of biosynthesized AuNPs has also been described. Das et al. [40] synthesized AuNPs on the surface of the fungus Rhizopus oryzae and demonstrated the growth inhibition of G and G+ bacterial strains, as well as the fungi Saccharomyces cerevisiae and C. albicans. AuNPs that inhibit the growth of C. albicans have also been obtained following biosynthesis using a banana peel extract [41].

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2.1.3. Antiviral activity Although viruses also represent serious problems in medicine or agriculture, there have been relatively few reports on the antiviral activity of biosynthesized NPs. Vijayakumar and Prasad [42] described the antiviral activity of Ag NPs prepared intracellularly

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Fig. 6. Electron micrographs of crystal morphologies and intracellular organization of magnetosomes found in various magnetotactic bacteria. The shapes of the magnetic crystals include cubo-octahedral (a), elongated hexagonal prismatic (b, d, e, f) and bullet-shaped morphologies (c). The particles are arranged in one (a, b, c), two (e) or multiple chains (d), or irregularly (f). The scale bar is equivalent to 100 nm. Reprinted from Schueler D, Frankel RB. Bacterial magnetosomes: microbiology, biomineralization and biotechnological applications. Appl Microbiol Biotechnol 1999;52(4):464–473, with kind permission from Springer Science and Business Media.

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Table 1 Antibacterial activity. NP

Organism used

Activity against

References

Ag Ag Ag

Pleurotus sajor-caju Pestalotia sp. Streptomyces hygroscopicus

Vigneshwaran et al. [13] Raheman et al. [14] Sadhasivam et al. [15,16]

Au Ag Ag Au Ag Ag

S. hygroscopicus Chaetocerus calcitrans, Chlorella salina, Isochrysis galbana, Tetraselmis gracilis Porphyra vietnamensis Galaxaura elongata Camellia sinensis Citrullus colocynthis

Staphylococcus aureus, Klebsiella pneumonia S. aureus, Salmonella typhi Bacillus subtilis, Enterococcus faecalis, Escherichia coli, Salmonella typhimurium B. subtilis, E. faecalis, E. coli, S. typhimurium, S. epidermidis, S. aureus K. pneumoniae, Proteus vulgaris, Pseudomonas aeruginosa, E. coli

Venkatpurwar and Pokharkar [18] Abdel-Raouf et al. [19] Vaseeharan et al. [21] Satyavani et al. [56]

Ag Ag Ag

Citrus sinensis Dioscorea batatas Dioscorea bulbifera

Au Au, Ag Ag Ag Ag Ag Ag Ag Ag Ag Ag

Terminalia chebula Mentha piperita Fusarium oxysporum Fusarium solani Azadirachta indica Eucalyptus citriodora, Ficus bengalensis Curcuma longa Mangifera indica Aspergillus niger Indigofera aspalathoides Chrysanthemum morifolium

S. aureus, E. coli E. coli, K. pneumonia, S. aureus, P. aeruginosa Vibrio harveyi E. coli, Vibrio paraheamolyticus, P. aeruginosa, P. vulgaris, Listeria monocytogens E. coli, P. aeruginosa, S. aureus B. subtilis, S. aureus, E. coli Acinetobacter baumannii, Enterobacter cloacae, E. coli, Haemophilus influenzae, K. pneumoniae, Neisseria mucosa, Proteus mirabilis S. aureus, E. coli S. aureus, E. coli S. aureus on cotton fabrics S. aureus, E. coli on cotton fabrics S. aureus, E. coli on cotton fabrics E. coli on cotton fabrics E. coli on cotton fabrics E. coli, S. aureus, B. subtilis on non-woven fabrics Wound healing activity Wound healing activity Bactericidal ultrasound gel

Sadhasivam et al. [15,16] Merin et al. [17]

Kaviya et al. [23] Nagajyothi and Lee [24] Ghosh et al. [25] Kumar et al. [20,26] MubarakAli et al. [27] Durán et al. [28] El-Rafie et al. [29,30] Tripathi et al. [31] Ravindra et al. [32] Sathishkumar et al. [33] Yang and Li [34] Sundaramoorthi et al. [35] Arunachalam et al. [36] He et al. [37]

Table 2 Antifungal, antiviral and anti-parasite activity.

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NP

Organism used

Activity against

References

Ag

Alternaria alternata

Gajbhiye et al. [38]

Ag Au Au Ag Ce Ag Ag Ag Ag Ag Ag

Amylomyces rouxii Rhizopus oryzae Musa sp. Aspergillus ochraceus Leptothrix discophora, Pseudomonas putida Lactobacillus fermentum Lactobacillus fermentum Nelumbo nucifera Rhizophora mucronata Lawsonia inermis Manilkara zapota

Phoma glomerata, Phoma herbarum, Fusarium semitectum, Trichoderma sp., C. albicans – combination w/fluconazole Candida albicans, Fusarium oxysporum Saccharomyces cerevisiae, C. albicans C. albicans M13 phage virus Bacteriophage UZ1 Bacteriophage UZ1, application to NanoCeram filter Bacteriophage UZ1, application to PVDF membrane Larvae of Anopheles subpictus, Culex quinquefasciatus Larvae of Aedes aegypti, Culex quinquefasciatus Pediculus humanus capitis, Bovicola ovis Rhipicephalus microplus

in Aspergillus ochraceus. In the study, AgNPs embedded in a carbonaceous matrix were obtained by heat treatment of the cells, and the effectiveness against M13 phage was determined using the plaque count method. In another study, De Gusseme et al. [43] described virus inhibition by zero-valent cerium produced by aqueous Ce(III) added to Leptothrix discophora and Pseudomonas putida cultures. The as-prepared cerium exhibited efficient antivirus activity against bacteriophage UZ1. In another study by the same researchers [44], Lactobacillus fermentum bacteria were used both as a reducing agent and as a scaffold for AgNPs. Their antiviral activity was determined for murine norovirus 1 and bacteriophage UZ1. In another study, the continuous antiviral capability of AgNPs embedded in Lactobacillus cells was tested in an aqueous environment by depositing the cells onto a NanoCeram electropositive filter. The study demonstrated that the filter with cell-embedded NPs had remarkably higher antiviral activity compared with the original filter. Similarly, De Gusseme et al. [45] demonstrated the inactivation of UZ1 bacteriophages using a similar approach with cell-embedded NPs on a PVDF membrane.

Musarrat et al. [39] Das et al. [40] Bankar et al. [41] Vijayakumar and Prasad [42] De Gusseme et al. [43–45] De Gusseme et al. [43–45] De Gusseme et al. [43–45] Santhoshkumar et al. [46] Gnanadesigan et al. [47] Marimuthu et al. [48] Rajakumar and Rahuman [49]

2.1.4. Anti-parasite applications Biosynthesized NPs are effective against various disease-causing insects or parasites. Santhoshkumar et al. [46] compared larvicidal activity of AgNPs biosynthesized using different lotus leaf (Nelumbo nucifera) extracts. In the study, antilarval activity was measured for the fourth instar larvae of Anopheles subpictus and Culex quinquefasciatus, both well-known vectors for malaria and lymphatic filariasis. A similar study by Gnanadesigan et al. [47] evaluated AgNPs biosynthesized with mangrove (Rhizophora mucronata) leaf extract against Aedes aegypti and C. quinquefasciatus larva. In another study, the larvicidal properties of AgNPs biosynthesized with henna (Lawsonia inermis) leaf extract was determined for the human head louse Pediculus humanus capitis and the sheep body louse Bovicola ovis [48]. The study determined lousicidal activity using both a direct contact method (P. humanus) and an impregnated filter paper method (B. ovis). Finally, the acaricidal activity of an evergreen tree (Manilkara zapota) aqueous extract and AgNPs synthesized by means of this extract were determined against the cattle tick (Rhipicephalus microplus) [49].

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2.2. Drug delivery and cancer treatment

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Biosynthesized NPs can interact with and alter the function of certain mammalian tissues. For example, metallic NPs can interfere with the antioxidant defense mechanism, leading to accumulation of reactive oxygen species, destruction of mitochondria and cell apoptosis [50]. This effect can be targeted, because the in vivo effects of metal NP exposure strongly depend on the capping agent: the same AgNPs with different capping agents have been reported to be both cytotoxic [50] and non-cytotoxic [51]. The use of stable noble metal NPs as carriers may minimize the side effect of conventional chemotherapeutic agents by the selective delivery of anticancer agents to malignant cells without affecting the normal cells. For instance, gold can be readily modified due to its ability to bind strongly to thiols (–SH) and amines (–NH2). Thus, covering the NP surface with biomolecules acting as chemotherapeutic and targeting agents is relatively straightforward [7]. With the selection of different capping agents, the cytotoxic activity of metallic NPs can be used for both drug delivery and cancer cell targeting (Table 3). Whether the targeted delivery of NPs themselves is therapeutic or the NPs act as carriers for some other agent, biosynthesized NPs are becoming increasingly important in nanomedicine.

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368 369 370 371

2.2.1. Biocompatibility Whenever NPs are used for in vivo applications, biocompatibility with normal tissue is an important consideration. Moulton et al. [51] described the biosynthesis of AgNPs using tea leaf extract as a reducing and capping agent. These authors exposed these NPs to human keratinocytes and evaluated mitochondrial function to assess cell viability and membrane integrity. The results showed that AgNPs biosynthesized with tea leaf extract were nontoxic, suggesting this method may be promising for future in vivo applications. The biocompatibility of tea-extract-biosynthesized AgNPs may be attributed to the antioxidant effect of polyphenol and flavonoid surfactants. Kumar et al. [20] described the blood compatibility of AuNPs synthesized with ginger (Zingiber officionale) extract. Upon contact with human blood, these AuNPs were shown to be non-platelet activating, and did not bring about the aggregation of other blood cells. Moreover, they were highly stable under normal physiological conditions compared to chemically synthesized NPs (citrate capped), which tended to aggregate blood cells. 2.2.2. Anticancer NPs Cytotoxicology studies against various cancer cell lines have been described for biosynthesized NPs. Amarnath et al. [52] published experiments using AuNPs synthesized using phytochemicals

present in grapes (Vitis vinifera). These AuNPs exhibited remarkable affinity towards HBL-100 (human breast cancer cells), and AuNP exposure resulted in HBL-100 apoptosis. Mishra et al. [53] described AuNP biosynthesis by the supernatant, live cell filtrate and biomass of the fungus Penicillium brevicompactum. In this work, the cytotoxic properties of biosynthesized NPs were analyzed using mouse myoblast cancer C2C12 cells. In a different study, guava and clove extracts were used to reduce Au and Ag salts [54]. Although biosynthesized AuNPs exhibited an anticancer effect on HEK-293, HeLa and HT-29 cancer cell lines, AgNPs did not show any anticancer activity in this study. In contrast, other reports have demonstrated anticancer effects from AgNPs. Biosynthesis of anti-tumor AgNPs using Piper longum leaf as a reducing and capping agent was reported by Jacob et al. [55]. These NPs showed an excellent cytotoxic effect on HEp-2 cancer cell lines. Similarly, callus extract of Citrullus colocynthis was use to form AgNPs which were effective against HEp-2 cells [56]. Similar efficiency against HeLa cells and a lymphoma mouse model was observed for AgNPs biosynthesized using Melia azedarach, a species of deciduous tree from the mahogany family [57]. A sophisticated evaluation of AgNPs effect on cancerous cell lines was given by Jeyaraj et al. [58]. The cytotoxicity effect of biogenic silver nanoparticles against human breast cancer cells in vitro was studied by means of the MTT, acridine orange/ethidium bromide and Hoechst methods and the COMET assay. Extracellular synthesis of copper NPs was performed using stem latex of Euphorbia nivulia [50]. This study concluded that copper NPs are toxic to A549 (human lung carcinoma) cells in a dose-dependent manner. Recently, the anti-metastatic activity of biologically synthesized AuNPs was reported for the human fibrosarcoma cell line HT-1080 [59]. Although the biosynthesized AuNPs had no toxic effects on HT-1080 cells in terms of cell viability, the study showed that AuNPs inhibit cell migration of HT-1080 cells by interfering with the actin polymerization pathway.

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2.2.3. NP drug carriers Magnetosomes are naturally occurring metallic nanoparticles found in some species of magnetotactic bacteria. These chains are membranous prokaryotic structures, and are composed of approximately 20 magnetite crystals surrounded by a lipid bilayer. Sun et al. [60] demonstrated the use of bacterial magnetosomes as carriers for drug delivery applications. In the study, isolated and cleaned bacterial magnetosomes from the magnetotactic bacterium Magnetospirillum gryphiswaldense were loaded with the chemotherapy drug doxorubicin (DOX), attached via amino groups. The anticancer effect of DOX-loaded bacterial magnetosomes was demonstrated using a cytotoxicity assay with HL60 and EMT-6 carcinoma cells. Inhibition of cancer cell proliferation and suppression

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Table 3 Drug delivery and cancer treatment applications. NP

Organism used

Application

References

Ag Au Au Au Au Ag Ag Ag Cu Ag Au Fe3O4 Fe3O4 Au

Camellia sinensis Zingiber officinale Vites vinefera Penicillium brevicompactum Guava Piper longum Citrullus colocynthis (L.) Schrad Melia azedarach Euphorbia nivulia Sesbania grandiflora Dysomsa pleiantha Magnetospirillum gryphiswaldense Magnetospirillum gryphiswaldense Porphyra vietnamensis

Biocompatible Blood compatibility Cytotoxic activity against HBL-100 cells Cytotoxic activity against mouse mayo blast cancer cells Cytotoxic activity against HEK-293, HeLa, and HT-29 cells Cytotoxic activity against Hep-2 cells Cytotoxic activity against HEp-2 cells Cytotoxic activity against HeLa cell lines and lymphoma mice model Anticancer efficiency against human lung carcinoma cells Anticancer efficiency against human breast cancer cells Cell migration of HT-1080 cell line blocking Carriers for drug delivery applications Biocompatibility of BM Carrier for drug delivery

Moulton et al. [51] Kumar et al. [20] Amarnath et al. [52] Mishra et al. [53] Raghunandan et al. [54] Jacob et al. [55] Satyavani et al. [56] Sukirtha et al. [57] Valodkar et al. [50] Jeyaraj et al. [58] Karuppaiya et al. [59] Sun et al. [60] Li et al. [61] Venkatpurwar et al. [62]

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of mRNA levels of the important oncogene c-myc suggest DOXloaded magnetosomes are promising for cancer therapy. Bacterial magnetosomes are able to carry a large amount of drug, are easy to prepare, and are more stable and more uniform compared with artificial magnetic NPs. They are also biocompatible. Li et al. [61] demonstrated the biocompatibility of purified and sterilized magnetosomes surrounded by a lipid/protein membrane to mouse fibroblasts in vitro. Another drug delivery study employed porphyran from the marine alga Porphyra vietnamensis as a reducing and capping agent for the biosynthesis of AuNPs [62]. These NPs were used as a carrier for DOX. The results demonstrated that AuNPbound DOX showed higher cytotoxicity to LN-229 (human glioma) cells than unbound DOX. Spectroscopy revealed that hydrogen bonds are involved in the DOX–AuNP conjugation.

433

2.3. Medical diagnostics and sensors

434

Biosynthesized NPs are also making important contributions to medicine in the sensing and diagnostics areas (Table 4). These materials have been successfully incorporated into chemical sensors that can detect medically relevant compounds, including peroxides and glucose. For example, eggshell membrane was used as a reducing agent and scaffold in the biosynthesis of AuNPs [63]. The sensor showed a linear response to different glucose concentrations, with a detection limit of 17 lM. The same material was used to measure the glucose content of human blood serum samples, and analysis showed agreement with a standard routine medical spectrophotometric test [64]. Hydrogen peroxide has been acknowledged as a diagnostic marker of oxidative stress, playing an important role in asthma or chronic obstructive pulmonary disease (COPD). Wang et al. [65] constructed a hydrogen peroxide sensor based on biosynthesized selenium NPs (SeNPs) prepared using the bacterial strain Bacillus subtilis. The resulting SeNPs were spherical and could be converted into one-dimensional trigonal wires (proteins excreted from B. subtilis cells act as a template). A clean glassy carbon electrode (GCE) was amended with a drop of a colloidal suspension of SeNPs and a drop of the enzyme horseradish peroxidase. Cyclic

419 420 421 422 423 424 425 426 427 428 429 430 431

435 436 437 438 439 440 441 442 443 444 445 446 447 448 449 450 451 452 453 454

voltammetry studies confirmed that SeNPs enhanced the detection of H2O2 resulting in an 80 nM detection limit). This material can therefore be used, for instance, for the detection of hydrogen peroxide in the exhaled breath condensate of patients affected with COPD (see Table 5). Other authors have also used a GCE modified with biosynthesized nanoparticles for electrochemical sensing. Zheng et al. [66] synthesized Au–Ag alloy NPs using yeast cells and demonstrated an enhanced electrochemical response for vanillin (from vanilla beans and vanilla tea). With a linear range of 0.2–50 lM and a detection limit of 40 nM, this sensor can be a simple and cheap alternative to analytical instruments involving gas or liquid chromatography, and can be used to check the quality of food products. Another possible medical application of biogenic AuNPs was proposed and tested by MubarakAli et al. [67], who suggested that the conjugation of DNA with biosynthesized nanoparticles can be used for diagnosis of genetic disease.

455

2.4. Medical imaging applications

472

The optical properties of metallic nanocrystals have been of interest for centuries. The incorporation of biosynthesis methods has made possible the preparation of metal NPs with a range of sizes, shapes and dielectric properties. Optical properties associated with metallic NPs include a high- or low-refractive index, high transparency, novel photoluminescence properties, photonic crystals and plasmon resonance [68]. Nanophotonics studies in the field, where the light interacts with particles smaller than its wavelength, lead to novel phenomena, such as localized surface plasmon resonance and a size-dependent semiconductor band gap [69]. The biosynthesis AuNPs by silica-encapsulated Klebsormidium flaccidum microalgae leads to the formation of a ‘‘living’’ biohybrid material [70]. Researchers have used Raman spectroscopy for in situ imaging of entrapped cells and have investigated the influence of the AuNPs on the photosynthetic system of the algae. The coupling of Raman imaging and sol–gel encapsulation might allow for the development of photosynthesis-based biosensors.

473

Table 4 Medical diagnostics and sensors. NP

Organism used

Application

References

Au Au Se Au–Ag Au

Eggshell membrane Eggshell membrane Bacillus subtilis Saccharomyces cerevisiae Different microalgae

Glucose sensor Glucose sensor in human blood serum H2O2 sensor Vanillin sensor DNA conjugation

Zheng et al. [63] Zheng et al. [64] Wang et al. [65] Zheng et al. [66] MubarakAli et al. [67]

Table 5 Imaging and other medical applications. NP

Organism used

Application

References

Au Ag Ag Ag Te Au Au CdTe CdTe CdS Au Au, Ag Au Ag

Klebsormidium flaccidum Trichoderma viride Parthenium hysterophorus Coriandrum sativum leaf Bacillus selenitireducens Maduca longifolia Cymbopogon citratus Saccharomyces cerevisiae Escherichia coli Brevibacterium casei Psidium guajava Brevibacterium casei Solanum nigrum Trichoderma reesei

Photosynthesis-based environmental biosensor NP photoluminescence NP photoluminescence Optical limiting Optical limiting Efficiency in absorbing infrared radiation Infrared absorbing optical coatings Biolabeling and bioimaging Biolabeling and bioimaging Fluorescence emission Diabetes treatment –tyrosine phosphatase type PTP 1B inhibition Anticoagulation activity Free radical scavenging effect HIV treatment

Sicard et al. [70] Fayaz et al. [71] Sarkar et al. [72] Sathyavathi et al. [74] Liao et al. [75] Fayaz et al. [76] Shankar et al. [77] Bao et al. [78] Bao et al. [79] Pandian et al. [80] Basha et al. [81] Kalishwaralal et al. [82] Muthuvel et al. [83] Vahabi et al. [84]

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Blue orange light emission from biosynthesized AgNPs was reported by Fayaz et al. [71]. Fungal-mediated AgNPs were prepared using a Trichoderma viride filtrate. Photoluminescence measurements after laser excitation showed an emission in the range of 320–520 nm, making such AgNPs promising for future labeling and imaging applications. A similar study was introduced by Sarkar et al. [72] using Parthenium hysterophorus leaf extract for AgNP biosynthesis. An important problem of modern laser medicine is the extensive exposure of vulnerable tissues outside of the operational field. This problem can be solved by placing dyes that are capable of reversible darkening of the radiation onto the surface of irradiated tissues. This phenomenon is called optical radiation limiting [73]. AgNPs biosynthesized using Coriandrum sativum leaf extract were found to exhibit strong reverse saturable absorption of laser irradiation [74]. The authors measured nonlinear refraction and absorption coefficients using a Z-scan technique with laser pulses. These results suggest AgNPs are capable of nonlinear optics. Similarly, microbiologically formed nanorods prepared using Bacilus selenitireducens and composed of elemental tellurium Te(0) have been described elsewhere [75]. These TeNPs form unusual nanocomposites when combined with an organic chemical host and exhibit excellent broadband optical limiting at 532 and 1064 nm. In this regard, they significantly exceeded the best commercial optical limiters currently available. Their relative ease of biomanufacturing combined with their unique properties makes these Te-based nanocomposites particularly attractive for their immediate employment as coatings in medicine or industry (e.g. to protect eyes from damage caused by exposure to focused beams and lasers). Fayaz et al. [76] biosynthesized AuNPs using Maduca longifolia extract and showed strong near-infrared absorption. Although some applications are not directly medical in nature, such as energy-saving window coatings, a similar technology can also be applied for cancer hyperthermia coatings [77]. The same research team published two additional studies describing cadmium telluride quantum dots (CdTeQDs) fabricated via extracellular synthesis using Saccharomyces cerevisiae [78] and Escherichia coli [79]. The authors evaluated the NP’s size-dependent optical properties. CdTeQD were relatively small, capped with protein and highly soluble in water. The optical properties were studied in both cases using UV–visible spectroscopy and spectrofluorimetry with photoluminescence emission from 488 to 551 nm. CdTeQDs functionalized with folic acid were used for in vitro imaging of cancer cells, and were also found to be biocompatible in a cytotoxicity assay [79]. This study clearly shows the capacity of biosynthesized QDs to be used in bioimaging and biolabeling applications. Finally, a study using Brevibacterium casei for the biosynthesis of CdSNPs [80] showed that the NPs exhibited fluorescence emission even after immobilization within a polyhydroxybutyrate matrix.

542

2.5. Other medical applications

543

Several studies have shown biosynthesized NPs to have potential applications for the treatment of other diseases, including diabetes and bleeding disorders. Biosynthesized AuNPs have been shown to inhibit the enzyme tyrosine phosphatase type PTP 1B in vitro [81]. Since PTP 1B has been found to dephosphorylate insulin receptors, reducing its activity can enhance the activity of insulin. AuNPs prepared by means of guavanoic acid from a leaf extract of Psidium guajava showed a significant inhibitory effect, with an IC50 of 1.14 lg ml1. Another study showed that biosynthesized Au- and AgNPs produced and stabilized using Brevibacterium casei exhibited anticoagulation activity [82]. Exposure of the particles to

544 545 546 547 548 549 550 551 552 553

9

blood plasma for 24 h did not show any significant reduction in the anticoagulation activity. Free radical scavenging activity was demonstrated by Muthuvel et al. [83]. Au-NPs biosynthesized by means of Solanum nigrum were tested for the scavenging effect on 10 1-diphenyl-2-picrylhydrazyl radical and hydroxyl radicals according to the method of Blois and the deoxyribose method, respectively. The synthetic Q7 antioxidant butyl hydroxyl toluene was used as a positive control, and biogenic nanoparticles showed up to 60% inhibition efficiency for both radical types. Interestingly, Trichoderma reesei-produced AgNPs prevent HIV-1 particles from binding to host cells [84]. Finally, Gopinath et al. [85] described enhanced mitotic cell division and pollen germination activity caused by AuNPs synthesized using Terminalia arjuna leaf extract. These studies demonstrate the wide range of biomedically relevent effects possible by exposure to biosynthesized NPs. Additional research will offer new discoveries and insights into the use of biosynthesized NPs as promising treatments for human diseases.

554

3. Environmental remediation applications

572

3.1. Metal biosorption, bioremediation and biorecovery

573

Oxidation–reduction processes are universally used for cellular metabolism; therefore biomolecules with the ability to reduce or oxidize other chemical compounds are abundant in any living cell. Many microorganisms are able to bind and concentrate dissolved metals as an active mechanism to detoxify their environment. Other biological processes, and even dead biomass, simply couple metal reduction with oxidation of an electron donor. Since the product of cellular metal reduction is usually nanostructured, bioremediation of metals in solution and biosynthesis of metallic NPs are in fact closely related processes [86]. In this section, we review studies that describe biological metal removal and NP formation via biologically mediated processes (see Table 6). The biomass of algae, fungi, bacteria and yeasts, along with some biopolymers and biowaste materials, are known to bind and concentrate precious metals [87]. This so-called biosorption process can represent a cost-effective alternative to the common chemical methods for recovery of various dissolved metals from aqueous solution. The mechanisms involved in binding and concentrating metals by microbes have been extensively studied in natural environments [87]. Chakraborty et al. [88] demonstrated the ability of cyanobacteria and algae to bind and concentrate Au and form AuNPs. The NP formation process is specific to a particular genus, and they described NP formation using the cyanobacterial strains Lyngbya majuscula and Spirulina subsalsa, and the freshwater green alga Rhizoclonium hieroglyphicum. AuNPs formation during biosorption by the seaweed Fucus vesiculosus was reported by Mata et al. [89]. These authors described the pH dependence on NP formation and discussed the stages of the bioreduction process. Dead biomass of the macrofungus Pleurotus platypus was used for biosorption of Ag in a study by Das et al. [90]. The fungal biomass exhibited the highest Ag uptake of 46.7 mg g1 at pH 6.0 in the presence of 200 mg l1 Ag(I) at 20 °C. These authors also offered detailed kinetic and thermodynamic analysis of the biosorption process. Zhang et al. [91] demonstrated the use of the G facultative anaerobic bacteria Aeromonas SH10 to treat Ag in waste water. In this study, biomass was shown to accumulate Ag+ and [Ag(NH3)2]+ ions as AgNPs. The maximum uptake of [Ag(NH3)2]+ was 0.23 g of Ag per g of cell dry weight. An example of platinum recovery by polyethyleneimine (PEI)modified biomass was described by Won et al. [92]. In this study, PEI was attached to the surface of E. coli biomass and the resulting

574

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555 556 557 558 559 560 561 562 563 564 565 566 567 568 569 570 571

575 576 577 578 579 580 581 582 583 584 585 586 587 588 589 590 591 592 593 594 595 596 597 598 599 600 601 602 603 604 605 606 607 608 609 610 611 612 613 614 615

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Table 6 Metal biosorption, bioremediation and biorecovery. NP

Organism used

Application

References

Au Au Ag Ag Pt Au Ag MnO2

Lyngbya majuscula, Spirulina subsalsa, Rhizoclonium hieroglyphicum Fucus vesiculosus Pleurotus platypus Aeromonas sp. SH10 Escherichia coli Sargassum sp. Saccharomyces cerevisiae Bacillus sp. (MTCC10650)

Bioaccumulation Bioaccumulation, biorecovery Biosorption Silver-containing waste water treatment Biosorption, biorecovery by incineration Biosorption, biorecovery by incineration As(V) bioaccumulation and removal Mn bioremediation

Chakraborty et al. [88] Mata et al. [8] Das et al. [90] Zhang et al. [91] Won et al. [92] Sathishkumar et al. [93] Selvakumar et al. [94] Sinha et al. [95]

635

material was used to accumulate platinum from waste water. Subsequent incineration of the modified biomass resulted in 98.7% recovery of platinum from the ash. A similar study employed the brown macroalga Sargassum sp. [93] for Au recovery and reported an efficiency of greater than 90%. Toxic concentrations of naturally occurring arsenic in drinking water are a major public health problem in Southeast Asia. Selvakumar et al. [94] described a promising solution to this problem through their development of an AgNP sorbent for As(V) removal. In the study, the reducing capabilities of a novel yeast strain of Saccharomyces cerevisiae was used to sequester the metal. Finally, Sinha et al. [95] showed that a heavy-metal-resistant strain of Bacillus sp. formed MnO2 NPs simultaneously with the remediation of manganese. Hexavalent chromium compounds are dangerous toxins, while Cr(III) ions and compounds are relatively non-toxic. Bare living cells of Shewanella algae, Pseudomonas putida and Desulfovibrio vulgaris have been shown to reduce Cr(VI) to Cr(III) [96]. Many other studies rely on biosynthesized PdNPs to catalytically reduce chromium. (See Section 3.4 on catalytic Cr(VI) reduction.)

636

3.2. Coupling biosorption with catalytic contaminant degradation

637

Due to their large surface area per weight, metallic NPs are widely used for catalysis, and in particular for heterogeneous catalysis. Metallic NPs offer selectivity, high activity and stability. The major drawback of metallic NP catalysis is cost: the constituent metals, including gold, platinum and palladium, are very expensive, and their fabrication into nanoparticles is energy intensive. Coupled biosynthetic approaches can generate catalytically active NPs through biosorption of waste streams containing precious metals. The coupling of biological metal removal with catalyst formation has been described in recent reviews by De Corte et al. [97] and Hennebel et al. [98]. These biosynthesized metallic NPs can then be used for catalytic dehalogenation, organic oxidation or metal reduction. Most environmental remediation applications of biosynthesized catalyst employ palladium (Pd) NPs (see Table 7).

616 617 618 619 620 621 622 623 624 625 626 627 628 629 630 631 632 633 634

638 639 640 641 642 643 644 645 646 647 648 649 650

The following sections describe catalytic treatment of organic compounds and metals using biosynthesized metallic NPs.

651

3.3. Catalytic degradation of organic pollutants

653

3.3.1. Catalytic dehalogenation Palladium-based catalysts are able to dehalogenate aromatic compounds. This reaction is very important for organic synthesis in research and industry, and also for contaminant remediation. Halogenated organic compounds dominate the priority list of persistent, bioaccumulative and toxic (PBT) pollutants as designated by the US Environmental Protection Agency. By definition, PBT compounds do not break down naturally in the environment, so enhanced processes to dehalogenate these compounds are of great interest. Halogenated organic PBTs include several banned pesticides, including chlordane, dichlorodiphenyltrichloroethane (DDT), dieldrin and hexachlorobenzene, as well as polychlorinated biphenyls (PCBs), compounds formerly used in electronic devices and as coolants, lubricants and plasticizers. Baxter-Plant et al. [99,100] described the dehalogenation of chlorophenol (CP) and selected PCB congeners, including 4-chlorobiphenyl, 2,4,6-trichlorobiphenyl, 2,3,4,5-tetrachlorobiphenyl and 2,20 ,4,40 ,6,60 -hexachlorobiphenyl, via palladized cells of G Desulfovibrio bacteria. Biosynthesized PdNPs were obtained by the reduction of the palladium precursor in the presence of Desulfovibrio desulfuricans, Desulfovibrio vulgaris and Desulfovibrio sp. Oz-7. As described by Bunge et al. [101], reduction in the absence of cells does not lead to the formation of PdNPs; rather, this process requires an electron donor, such as formate (see Tables 8 and 9). Shewanella oneidensis is another strain of bacteria that has been used to biosynthesize PdNPs for dehalogenation of PCB and other chlorinated organic compounds. De Windt et al. [102] described PdNPs precipitated on the cell wall and inside the periplasmic space of S. oneidensis and demonstrated the effective dehalogenation of PCBs in water and sediment. Their study described in detail bioreduction with different electron donors and varying fractions of PdNPs associated with the biomass. They showed that

654

Table 7 Catalytic dehalogenation. NP

Organism used

Application

References

Pd Pd Pd Pd

Desulfovibrio vulgaris, D. desulfuricans D. desulfuricans Shewanella oneidensis S. oneidensis

Dechlorination Dechlorination Dechlorination Dechlorination

Pd Pd Pd Pd Fe/Pd Pd Pd Pd Pd

D. desulfuricans, Rhodobacter sphaeroides S. oneidensis S. oneidensis S. oneidensis Camellia sinensis D. desulfuricans D. desulfuricans S. oneidensis S. oneidensis

Dechlorination of (PCBs) and penta-CP Dechlorination of lindane Dechlorination of TCE, membrane reactor Dechlorination of TCE, fixed bed reactor Dechlorination of TCE Dehalogenation PCBs and polybrominated diphenyl ether Dehalogenation of flame retardant materials Deiodination of diatrizoate Dehalogenation of diatrizoate in microbial electrolysis cells

of of of of

CP and PCBs CP and PCBs chlorophenol and PCBs perchlorate and PCBs

Baxter-Plant et al. [99] Baxter-Plant et al. [100] De Windt et al. [102] De Windt et al. [103] Macaskie et al. [104] Redwood et al. [105] Mertens et al. [106] Hennebel et al. [107] Hennebel et al. [108] Smuleac et al. [109] Harrad et al. [110] Deplanche et al. [111] Hennebel et al. [112] De Gusseme et al. [113]

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the catalytic activity of biosynthesized PdNPs was 100 higher than commercial palladium catalyst powder. In a follow-on report, De Windt et al. [103] performed a detailed assessment of the bioreduction process and its conditions. In particular, they investigated the factors influencing the particle size and catalytic properties of PdNPs formed from a soluble palladium precursor by S. oneidensis. Interestingly, the relatively large palladium crystals formed on non-viable biomass exhibited high catalytic efficiency towards hydrophobic molecules such as PCBs, while the smaller PdNPs created on living bacterial cells showed high catalytic activity towards perchlorate. Macaskie et al. [104] extensively studied the catalytic dechlorination of 2-chlorophenol, pentachlorophenol and various PCB congeners by palladized cells of Desulfovibrio and Escherichia coli. Redwood et al. [105] compared the efficiency of palladized D. desulfuricans with Rhodobacter sphaeroides for catalytic dechlorination of PCBs and pentachlorophenol. Mertens et al. [106] demostrated the efficiency of palladized S. oneidensis for the catalytic decomposition of the pesticide lindane. These authors also incorporated the catalytic material into a membrane bioreactor for the continuous treatment of lindane-contaminated water. Other studies have demonstrated the use of palladized cells for dechlorination of the common groundwater contaminant trichlorethylene (TCE). Hennebel et al. described two reactor geometries for catalytic dechlorination of TCE by biosynthesized PdNPs: a pilot-scale membrane reactor [107] and a fixed bed reactor with PdNPs embedded in a polyurethane foam [108]. These authors described the cumulative removal of 98% of TCE after 22 h, with ethane as the predominant product, and a maximum removal rate of 1.059 mg of TCE per g of biosynthesized PdNPs per day. Other authors used Fe and Fe/Pd NPs biosynthesized with tea extract (Camellia sinensis) then immobilized in polymer membranes for the catalytic degradation of TCE [109]. These authors found that the reaction rate constant was higher for the bimetallic

Fe/PdNPs. The biosynthesized NPs exhibited a lower reaction rate than chemically synthesized FeNPs, though the reactivity of chemically synthesized FeNPs diminished to less than 20% within four cycles. By contrast, the reactivity of the green tea extract-synthesized NPs was preserved throughout 3 months of repeated use under conditions simulating a real water treatment system, possibly due to a number of polyphenols that can act as capping agents. Biosynthesized PdNPs can also catalytically dehalogenate brominated organic compounds. Harrad et al. [110] demonstrated that palladized D. desulfuricans is able to catalytically dehalogenate polybrominated diphenyl ether (PBDE). Hydrophobic brominated compounds such as PBDE are used as flame retardants in building materials, textiles and plastics. Deplanche et al. [111] also used palladized cells of D. desulfuricans for the catalytic dehalogenation of flame retardants, including PBDE and tris-(chloroisopropyl)phosphate (TCPP), and compared their performance with chemically reduced palladium powder. The chemically reduced Pd was more effective in debrominating PBDE, but the biosynthesized PdNPs were five times more effective in TCPP dechlorination. Two studies have demonstrated that biosynthesized NPs can remediate diatrizoic acid (or diatrizoate), a radiocontrast agent. Hennebel et al. [112] demonstrated that PdNPs encapsulated on PVDF membranes effectively deiodinate diatrizoate in water. Similarly, De Gusseme et al. [113] showed that biosynthesized PdNPs contributed to higher dehalogenation rates of TCE and higher deiodination rates of diatrizoate when applied on the surface of a graphite cathode. The presence of PdNPs on the cathode enhanced the rate of diatrizoate removal by both direct electrochemical reduction and catalytic reduction using the hydrogen produced at the cathode of the microbial electrolysis cell.

720

3.3.2. Catalytic 4-nitrophenol degradation The rapid development and use of synthetic pesticides, dyes, explosives and pharmaceuticals in the middle of the last century

750

Table 8 Catalytic 4-nitrophenol degradation and catalytic treatment of other aqueous organic compounds. NP

Organism used

Application

References

Au Au Ag Ag Au Pd/Au Ag Fe Au ZnS

Sesbania drummondii Cacumen platycladi Sepia esculenta Breynia rhamnoides B. rhamnoides Cupriavidus necator Rhizopus oryzae C. sinensis C. sinensis Streptococcus thermophiles, Lactobacillus bulgaricus, Lactobacillus acidophilus Coccinia grandis Pseudomonas putida

Reduction of 4-nitrophenol Reduction of 4-nitrophenol Reduction of 4-nitrophenol Reduction of 4-nitrophenol Reduction of 4-nitrophenol Reduction of 4-nitrophenol Reduction of 4-nitrophenol Degradation of aqueous cationic and anionic dyes Reduction of methylene blue Photocatalytic degradation of fuchsine

Sharma et al. [114] Huang et al. [115] Jia et al. [118] Gangula et al. [116] Gangula et al. [116] Hosseinkhani et al. [117] Das et al. [119] Shahwan et al. [120] Gupta et al. [121] Zhou et al. [122]

Photocatalytic degradation of Coomassie Brilliant Blue G-250 Removal of micropollutants (e.g. ibuprofen, diclofenac, mecoprop)

Arunachalam et al. [123] Forrez et al. [124]

Ag Pd

Table 9 Catalytic Cr(VI) reduction.

*

NP

Organism used

Application

Pd Pd Pd Pd Pd/MM* Pd Pd Pd

E. coli mutant strains D. desulfuricans Desulfovibrio vulgaris, Desulfovibrio desulfuricans D. desulfuricans D. desulfuricans, Escherichia coli Serratia sp. (NCIMB) Clostridium pasteurianum E. coli, Desulfovibrio spp.

Reduction Reduction Reduction Reduction Reduction Reduction Reduction Reduction

of of of of of of of of

References Cr(VI) Cr(VI) Cr(VI) Cr(VI) Cr(VI) Cr(VI) Cr(VI) Cr(VI)

to to to to to to to to

Cr(III) Cr(III) Cr(III) Cr(III) Cr(III) Cr(III) Cr(III) in aquifer environment Cr(III)

Deplanche et al. [125] Mabbett and Macaskie [126] Humphries et al. [127] Mabbett et al. [128] Mabbett et al. [129] Beauregard et al. [130] Chidambaram et al. [131] Macaskie et al. [146]

Mixed precious metals.

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751 752

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has resulted in a legacy of toxic nitro-aromatic contamination in soil and water. Technologies for catalytic removal of compounds such a 4-nitrophenol (also known as p-nitrophenol or PNP) can help restore impacted environments. Furthermore, the degradation of PNP can be measured easily using widely available and inexpensive optical methods such as UV–visible spectrophotometry. The catalytic degradation of PNP has thus become a common test system to evaluate the catalytic reduction capabilities of biosynthesized NPs. The first report of PNP reduction employing biosynthesized NPs was published by Sharma et al. [114]. Seedlings of the plant Sesbania drummondii were grown in a hydrogen tetrachloroaurate solution and stable AuNPs were subsequently formed in plant tissues. This AuNP-rich plant tissue was used as an efficient catalyst for PNP reduction in the presence of sodium borohydride. Subsequently, others have used plant materials to biosynthesize noble metal NPs for catalytic PNP reduction. Huang et al. [115] carried out an extensive study using 21 species of traditional Chinese herbs and medicinal plants. These plants were divided into four Q8 groups, and their leaves, flowers, fruits or grasses were used for NP biosynthesis by 30 min incubation in aqueous HAuCl4. Due to their monodispersity and small size, AuNPs prepared using Cacumen platycladi leaves were used to demonstrate catalytic PNP reduction. Gangula et al. [116] used the stem extract of a medicinal plant Breynia rhamnoides for fast (7 min) biosynthesis of AgNPs and AuNPs. These authors found the conversion efficiency to be dependent on the NP size, which is possibly controlled by the stem extract concentration used for biosynthesis. Bacteria have also been used for biosynthesis of bimetallic Pd/ AuNPs for PNP reduction. Hosseinkhani et al. [117] formed biosupported Pd(0) and Au(0) NPs on the surface of Cupriavidus necator cells. Bimetallic particles were subsequently formed following the addition of either Au(III) or Pd(II) salt to the biosupported NPs. Although the bimetallic NPs did not have a core–shell structure, they exhibited superior catalytic efficiency in PNP conversion compared with monometallic NPs. Catalytic PNP reduction has also been done using animal-derived materials for the biosynthesis of NPs. Jia et al. [118] described AgNP biosynthesis and immobilization using a cuttlebone-derived organic matrix from the cuttlefish Sepia esculenta. The calcareous matrix of the cuttlebone functioned as both a reducer and a scaffold for AgNP formation. These researchers also described the reusability of the composite material and the potential for separation of NPs from the matrix. Das et al. [119] showed that the immobilization of the biogenic AgNPs on the nanostructured silica leads to their excellent hydrogenation catalytic efficiency. Protein extract from Rhizopus oryzae was applied on the nanosilica and used for AgNP biosynthesis. The resulting material was subsequently used for catalytic hydrogenation of 4-nitrophenol. 3.3.3. Catalytic treatment of other aqueous organic compounds Other organic compounds have been effectively reduced using biosynthesized NPs. Iron and gold NPs have been used to catalytically remove dyes from aqueous solutions. In one study, FeNPs biosynthesized by means of green tea extract were used as a Fenton-like catalyst for the decolorization of aqueous solutions of methylene blue and methyl orange dyes [120]. Compared with iron NPs produced by the reduction of sodium borohydride, the biosynthesized iron NPs exhibited faster dye removal and a greater extent of dye removal. Gupta et al. [121] used green tea extract to biosynthesize AuNPs for catalytic reduction of the dye methylene blue in the presence of Sn(II) in both aqueous solution and micelles. The authors showed that a small quantity of AuNPs decreases the activation energy for reduction of methylene blue, and complete removal of dye could be achieved even at low temperature. Zhou et al. [122] described the photocatalytic degradation of the

magenta dye fuchsine using PbS and ZnS hollow nanostructures formed on two species of bacteria. Photocatalytic degradation of the dye Coomassie Brilliant Blue G-250 in the presence of UV light has also been shown by AgNPs prepared from the aqueous extract of Coccinia grandis leaves [123]. Finally, Forrez et al. [124] used biosynthesized PdNPs in a membrane reactor to remove micropollutants such as ibuprofen (>95%), diclofenac (86%), mecoprop (81%) and triclosan (>78%) from the secondary effluent of a sewage treatment plant. The authors suggested that the removal mechanisms could include chemical oxidation by PdNPs and/or biological removal by Pseudomonas putida bacteria.

818

3.4. Catalytic Cr(VI) reduction

830

Another important environmental application for biosynthesized NPs is the catalytic reduction of the powerful oxidant Cr(VI) to the relatively non-toxic valence state Cr(III). Several recent studies have shown that PdNPs biosynthesized by various species of bacteria, including E. coli, Desulfovibrio, Serratia and Clostridium, can effectively catalyze the reduction of Cr(VI) to Cr(III) under both batch and continuous flow conditions. For example, Deplanche et al. [125] evaluated how three types of hydrogenases encoded by E. coli influence the activity of biosynthesized catalyst for Cr(VI)/Cr(III) reduction. This study also described the hydrogenase involvement in Pd(II) reduction. Macaskie et al. [104] compared E. coli and Desulfovibrio spp. for the biosynthesis of PdNPs for catalytic Cr(VI)/Cr(III) reduction. Mabbett and Macaskie [126] used Desulfovibrio desulfuricans for the biosynthesis of PdNPs for Cr(VI)/Cr(III) reduction in waste water. These authors found that the biosynthesized PdNPs were more efficient reduction catalysts than either bare living D. desulfuricans biomass or chemically reduced palladium. They proposed that the palladium catalyzes the hemolytic cleavage of H2 and that the H⁄ radicals then donate their electrons to reduce the Cr(VI). Unlike the previous experiments, all of which were carried out under batch conditions, Humphries et al. [127] reported a continuous flow system for Cr(VI)/Cr(III) reduction. In this study, biosupported PdNPs formed by Desulfovibrio vulgaris were immobilized in agar and the effects of Pd concentration, Cr(VI) concentration and process flow rate were investigated. This work built on a study by Mabbett et al. [128], who had previously demonstrated a continuous flow system for Cr(VI)/Cr(III) reduction by PdNPs biosynthesized by D. desulfuricans. Mabett et al. [129] subsequently described the formation of a mixed metal catalyst biosynthesized with D. desulfuricans and E. coli from a metal waste stream for Cr(VI)/Cr(III) reduction. Beauregard et al. [130] used a biofilm-forming bacterial species Serratia sp. to mediate the adherence of bio-PdNPs to porous polyurethane foam. The foam was used as a scaffold for the catalyst and supported the growth of the bacterium. Magnetic resonance imaging was used to directly monitor Cr(VI)/Cr(III) reduction since Cr(VI)aq is non-paramagnetic and Cr(III)aq is paramagnetic. Finally, Chidambaram et al. [131] demonstrated successful Cr(VI) reduction experiments using PdNs biosynthesized by the bacterium Clostridium pasteurianum. This study is unique because, unlike the previous studies, the C. pasteurianum communities were grown on aquifer material and catalytic reduction experiments were performed in a natural aquifer environment. This study opens up the potential for in situ Cr(VI) remediation via Pd(II) injection into the aquifer.

831

3.5. Biosynthesized NPs to enhance membrane treatment processes

877

Technologies to reduce biofouling can greatly enhance the performance of membrane-based water treatment processes.

878

Please cite this article in press as: Schröfel A et al. Applications of biosynthesized metallic nanoparticles – A review. Acta Biomater (2014), http:// dx.doi.org/10.1016/j.actbio.2014.05.022

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Zhang et al. [132] showed that different amounts of biogenic AgNPs formed by Lactobacillus fermentum prevented biofouling on polyethersulfone membranes. The membranes were used to remove organophosphate pesticides and E. coli cells from a waste water model. The authors measured the structure and performance of the membrane and assessed biofouling using E. coli and P. aeruginosa bacteria both individually and in mixed culture. The nanofunctionalized membrane coating exhibited good antibacterial activity and prevented biofilm formation on the membrane surface during the 9 week test.

890

4. Industrially important applications

891

4.1. Catalytic organic synthesis

892

Cheap specific catalysts for commercially important organic synthesis reactions, including hydrogenation, cross-coupling reactions and epoxidation, are extremely important in industry. Biosynthesized palladium, gold and platinum catalysts have been used successfully in several different organic synthesis pathways (see Table 10). Creamer et al. [133] used palladized cells of bacterial strains Desulfovibrio desulfuricans (G) and Bacillus sphaericus (G+) for catalytic hydrogenation of itaconic (or methylenesuccinic) acid. Comparisons performed in a stirred autoclave between biosynthesized PdNPs and commercial graphite-supported catalysts displayed similar activity. Bennett et al. [134] investigated the hydrogenation and isomerization of 2-pentane using palladized D. desulfuricans in a stainless steel Büchi reactor. They found that, although the rate of 2-pentane hydrogenation was lower for the biosynthesized Pd catalyst than for the commercial Pd/Al2O3 catalyst, the selectivity was similar. Wood et al. [135] used palladized Rhodobacter capsulatas and Arthrobacter oxidans for the hydrogenation of 2-butyne-1, 4-diol. The biosynthesized PdNPs exhibited high selectivity during partial hydrogenation to 2-butene-1,4-diol. Creamer et al. [136] demonstrated the use of biosynthesized PdNPs to catalyze non-aqueous hydrogenation. Desulfovibrio desulfuricans and B. sphaericus produced palladium catalyst, which catalyzed the hydrogenation of 4-azidoaniline hydrochloride to 1,4-phenylenediamine and 3-nitrostyrene to 1-ethyl-3-nitrobenzene in methanol. Unlike the aforementioned studies, Jia et al. [137] published a method for PdNPs biosynthesis that does not require the H2 donor. Biosynthetic PdNPs were formed by the reduction of palladium chloride in a crude extract of Gardenia jasminoides. The authors measured catalytic hydrogenation of p-nitrotoluene and demonstrated a conversion of 100% at 5 MPa and 150 °C for 2 h, with a selectivity of 26.3% for the product p-methyl-cyclohexylamine.

893 894 895 896 897 898 899 900 901 902 903 904 905 906 907 908 909 910 911 912 913 914 915 916 917 918 919 920 921 922 923 924

Reusability studies demonstrated that the catalyst retained its activity over five cycles. Biosynthesized NPs have been used to catalyze cross-coupling reactions (i.e. C–C bond formation). Søbjerg et al. [138] showed that palladized bacteria Cupriavidus necator, Pseudomonas putida and Staphylococcus sciuri were effective catalysts for both the Suzuki–Miyaura and Mizoroki–Heck reactions. In a follow-on report, these authors described how biomass/Pd ratio and NPs sizes influenced the hydrogenation of (E)-3-(4-methoxyphenyl)N-methylacrylamide and the reduction of 4-chloro-nitrobenzene [139]. Finally, Gauthier et al. [140] demonstrated the formation of catalyst for C–C bond formation was coupled to the recovery of Pd from a waste stream using Cupriavidus necator cells. In addition to palladium, biosynthesized gold and platinum NPs have been used to catalyze other organic synthesis reactions. Du et al. [141] used biosynthesized AuNPs to catalyze propylene epoxidation. Negatively charged AuNPs were immobilized on a titanium silicalite support using electrostatic attractive interactions in an extract of Cacumen platycladi. These authors achieved a propylene epoxide formation rate higher than previously described in other reports. The authors proposed that the efficiency and selectivity of biosynthesized catalysts could be influenced by residual biomolecules. A more detailed investigation of the same catalyst by Zhan et al. [142] described the optimum reaction parameters, including the Si/Ti molar ratio, Au loading, immobilization pH and reaction temperature, together with possible reaction mechanisms. Similarly, AuNPs immobilized on a titanium silicalite support were calcined and used for industrially important epoxidation of styrene to styrene oxide [143]. This experimental setup enables a styrene conversion of 92.7% and a styrene oxide selectivity of 90.4% under optimal conditions. Finally, biosynthesized PtNPs have been used to catalyze the synthesis of the organic dye antipyrilquinoneimine from aniline and 4-aminoantipyrine in acidic aqueous solution [144]. In this report, honey-mediated platinum nanostructures were found to be stable in water for more than 4 months.

925

4.2. Energy-related applications

961

The ability of different organisms to reduce and absorb precious metal salts and form NPs has been used to enhance several aspects of fuel cell performance. Biogenic NPs have been used to produce H2 fuel, to catalyze chemical oxidation of the fuel and to improve power recovery (Table 11). Several investigators have used biosynthesized PdNPs for H2 production. Bunge et al. [101] used three species of bacteria (Cupriavidus necator, Pseudomonas putida and Paracoccus denitrificans) to biosynthesize PdNPs for catalytic H2 production from hypophosphite. Wu et al. [145] biosynthesized PdNPs with gardenia extract on

962

Table 10 Catalytic organic synthesis. NP

Organism used

Application

References

Pd Pd Pd Pd Pd Pd Pd Pd Pd Au Au Au Pt

D. desulfuricans, Bacillus sphaericus D. desulfuricans Rhodobacter capsulatus, Arthrobacter oxidans D. desulfuricans, B. sphaericus Gardenia jasminoides Cupriavidus necator, Pseudomonas putida C. necator, Staphylococcus sciuri C. necator, Staphylococcus sciuri C. necator Cacumen platycladi C. platycladi C. platycladi Honey

Hydrogenation of itaconic acid Hydrogenation of 2-pentane Hydrogenation of 2-butyne-1,4-diol Hydrogenation, reduction and selective dehalogenation in non-aqueous solvents Hydrogenation of p-nitrotoluene Suzuki–Miyaura and Mizoroki–Heck reactions Suzuki–Miyaura, hydrogenation of (E)-3-(4-methoxyphenyl)-N-methylacrylamide 4-chloronitrobenzene reduction Catalysis of C–C bond formation Propylene epoxidation Propylene epoxidation Styrene epoxidation Preparation of organic dye

Creamer et al. [133] Bennett et al. [134] Wood et al. [135] Creamer et al. [136] Jia et al. [137] Søbjerg et al. [138] Søbjerg et al. [139] Søbjerg et al. [139] Gauthier et al. [140] Du et al. [141] Zhan et al. [142] Huang et al. [143] Venu et al. [144]

Please cite this article in press as: Schröfel A et al. Applications of biosynthesized metallic nanoparticles – A review. Acta Biomater (2014), http:// dx.doi.org/10.1016/j.actbio.2014.05.022

926 927 928 929 930 931 932 933 934 935 936 937 938 939 940 941 942 943 944 945 946 947 948 949 950 951 952 953 954 955 956 957 958 959 960

963 964 965 966 967 968 969 970 971

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TiO2 supports to enhance photocatalytic H2 evolution from pure water. Macaskie et al. [146] provided a brief overview of bacterial hydrogenase activity for several applications, including waste decontamination, production of precious metal nanocatalyst and biohydrogen production. These authors also described how E. coli with modified hydrogenase and dehydrogenase regulation could be used to further enhance performance. Biosynthesized NPs have been incorporated into fuel cells to catalyze chemical reactions and have been used in electrode construction. Yong et al. [147] bioaccumulated Pt and Pd as NPs using Desulfovibrio desulfuricans and mixed the dried biomaterial with activated carbon powder to create carbon paper used in a commercial fuel cell system. Dimitriadis et al. [148] used yeast biomass immobilized in polyvinyl alcohol (PVA) cryogels for the biorecovery of platinum from aqueous solution, then directly incorporated this PtNP–biomass–PVA material into a fuel cell. Another study described four different concentrations of biomass-supported palladium NPs using Shewanella oneidensis as an electrode catalyst in a polymer exchange membrane fuel cell [149]. Orozco et al. [150] studied the ability of PdNPs biosynthesized by two different strains of E. coli to both produce hydrogen via fermentation and convert the H2 into energy in a fuel cell. Both the parent strain MC4100 and the mutant strain IC007 were coated with PdNPs after the bioreduction of palladium precursor, then modified and tested as anodes in a fuel cell. The mutant strain IC007 showed a threefold greater power conversion compared with the parent strain, but produced about half of the power of commercial Pd powder or biosynthesized PdNPs made with D. desulfuricans. Yong et al. [151] described the coupling of waste biorefining with fuel cell power generation using biosynthesis to recover precious metals and form nanocatalysts. Palladium was biorecovered from industrial processing waste and transformed into biosupported PdNPs using D. desulfuricans, E. coli and Cupriavidus metallidurans. The study also described the biosynthesis and performance of a mixed metal catalyst produced from the waste stream.

1008

4.3. Electrodes and sensors

972 973 974 975 976 977 978 979 980 981 982 983 984 985 986 987 988 989 990 991 992 993 994 995 996 997 998 999 1000 1001 1002 1003 1004 1005 1006

1009 1010 1011 1012 1013 1014 1015 1016 1017 1018 1019 1020 1021 1022 1023

Fundamental electrochemical phenomena can be better understood through nanoscale science and nanotechnology, and performance of electrodes and sensors can be altered or enhanced using biosynthesized nanoparticles. Several aspects of biosynthesized metallic nanoparticles have been studied in detail, including their surface chemistry, biological compatibility and electrical conductivity. For nanoelectrochemical applications, special attention has been paid to AuNPs because they provide a suitable substrate for the immobilization of biomolecules without altering their biological activity, and they provide excellent electron transfer between the biomolecule and the electrode surface [152]. The presence of capping agents and surfactants in biosynthesized AuNPs can modulate electrode functionality and may enhance the operating range or selectivity compared with conventional materials (see Table 12).

Several studies have examined the electrical transmission properties of biosynthesized NPs incorporated into electrodes. In one study, dried whole plant extract from Scutellaria barbata was used for the biosynthesis of AuNPs [153]. These AuNPs were applied to a glassy carbon electrode (GCE), and the authors found enhanced electrical transmission between the modified electrode and PNP. Another study also demonstrated enhanced electrical transmission using a GCE modified with AuNPs prepared from the flower extract of Rosa damascene [154]. This study employed cyclic voltammetry in a solution of 0.1 M KCl and 5.0 mM [Fe(CN)6]3-/4- to demonstrate an increase in the electronic transmission rate for the modified electrode. Sadhasivam et al. [16] performed cyclic voltammetry studies using a three-electrode configuration employing AuNPs biosynthesized by Streptomyces hygroscopicus. Platinum and Ag/ AgCl were used as counter and reference electrodes, respectively, and electrochemically coated Cu2O on a Pt substrate (Cu2O–Pt) with an AuNPs–methylene blue monolayer was employed as the working electrode. Various electrochemical sensing applications can make use of the unique properties of biosynthesized NPs. Jha and Prasad [155] introduced a biosynthetic method to prepare ferroelectric BaTiO3 NPs using the bacterium Lactobacillus sp. The resulting NPs were mixed with a PVDF solution then agitated and warmed until the mixture became viscous. The process resulted in thin nanocomposite sheets that exhibited significantly enhanced dielectric properties. Torres-Chavolla et al. [156] biosynthesized AuNPs using three species of actinomycetes, Thermomonospora curvata, T. fusca and T. chromogena, and stabilized the NPs using the cross-linker glutaraldehyde for enhanced biosensing applications. Shilov et al. [157] investigated different electrophysical characteristics, such as cell zeta potential, surface conductivity, electrophoretic mobility and the dispersion of cell conductivity, of Candida albicans yeast cells with Ag precipitate prepared using the reducer hydrazine. Du et al. [158] introduced the bioreduction of Au by E. coli cells and their application for direct electrochemical sensing of hemoglobin. Biosynthesized AuNPs bound to the surface of the bacterial cells were incorporated on a GCE. The authors performed cyclic voltammetry measurements for different electrode configurations on small samples of hemoglobin placed directly on the electrode surface. The results showed a pair of redox peaks with a formal potential of 0.325 V vs. an Ag/AgCl reference electrode. This study demonstrated that biosynthesized nanocomposites can assist electron transfer between hemoglobin and the surface of a GCE. Biosynthesized CdSNPs have also been used to fabricate a heterojunction with asymmetric electronic transfer properties [159]. Semiconducting wurtzite-type structured NPs were prepared using Schizosaccharomyces pombe. Tin-doped indium oxide-coated glass was covered by a thin film of spin-coated polyphenylene vinylene and washed with S. pombe. While polyphenylene vinylene is a p-type material, CdSNPs represent an n-type material. With added Ag contacts, the resulting diode had a forward current of 75 mA cm2 at 10 V and experienced breakdown at approximately 15 V in reverse mode.

Table 11 Energy-related applications. NP

Organism used

Application

References

Pd Pd/TiO2 Pd Pd Pt Pd Pd Pd

Cupriavidus necator, Pseudomonas putida, Paracoccus denitrificans Gardenia jasminoides Escherichia coli Desulfovibrio desulfuricans Saccharomyces cerevisiae S. oneidensis E. coli D. desulfuricans, E. coli, Cupriavidus metallidurans

Hydrogen production from hypophosphite Photocatalytic H2 evolution from pure water Biohydrogen production fuel cell electrode Pt biorecovery, fuel cell electrode Fuel cell electrode Fuel cell electrode Waste biorefining, fuel cell electrode

Bunge et al. [101] Wu et al. [145] Macaskie et al.[146] Yong et al. [147] Dimitriadis et al.[148] Ogi et al. [149] Orozco et al. [150] Yong et al. [151]

Please cite this article in press as: Schröfel A et al. Applications of biosynthesized metallic nanoparticles – A review. Acta Biomater (2014), http:// dx.doi.org/10.1016/j.actbio.2014.05.022

1024 1025 1026 1027 1028 1029 1030 1031 1032 1033 1034 1035 1036 1037 1038 1039 1040 1041 1042 1043 1044 1045 1046 1047 1048 1049 1050 1051 1052 1053 1054 1055 1056 1057 1058 1059 1060 1061 1062 1063 1064 1065 1066 1067 1068 1069 1070 1071 1072 1073 1074 1075 1076 1077

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Organism used

Application

References

Au Ag, Au BaTiO3 Au Au CdS Au Au, Ag

Scutellaria barbata Rosa damascena Lactobacillus sp. Thermomonospora curvata, T. fusca, T. chromogena Escherichia coli Schizosaccharomyces pombe Black tea Solanum lycopersicum

Direct electrochemistry of 4-NP Modified glassy carbon electrode Nanocomposite with significantly enhanced dielectric properties Applications in enhanced biosensors Direct electrochemistry of hemoglobin Construction of ideal diode Capacitors construction Metallic ion detection

Wang et al. [153] Ghoreishi et al. [154] Jha and Prasad [155] Torres-Chavolla et al. [156] Du et al. [158] Kowshik et al. [159] Uddin et al. [160] Bindhu and Umadevi [161]

1087

Biogenic AuNPs in polyvinyl alcohol–KH2PO4 films were used by Uddin et al. [160] to ameliorate the percolative behavior of these nanocomposite films and to generate high dielectric permittivity at room temperature. The performance of the material is promising for use in capacitors. The unique optical properties of metallic nanoparticles can be also used for chemical sensing. AuNPs and AgNPs reduced using extract from the tomato Solanum lycopersicum were used for detection of metallic ions, including Fe3+ and Cu4+, in water based on subtle changes in their surface plasmon resonance spectra [161].

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5. Applications for magnetically responsive NPs

1078 1079 1080 1081 1082 1083 1084 1085 1086

1089 1090 1091 1092 1093 1094 1095 1096 1097 1098 1099 1100 1101 1102 1103 1104 1105 1106 1107 1108 1109 1110 1111 1112 1113 1114

Magnetotactic bacteria have a natural ability to synthesize magnetite NPs (MNPs), which are useful for various applications (Table 13). Only certain NP forms are synthesized spontaneously by magnetotactic bacteria [162,163]. The biological synthesis of magnetically responsive NPs is well established, and their use in various medical, environmental and industrial applications has been reviewed [164–166]. The yield and properties of MNPs can be manipulated and optimized to suit a particular purpose. Kundu et al. [167] described changes in magnetosome size, number, and alignment with biosynthesis performed in the presence of Zn and Ni salts. Other investigators have described the formation of zinc–ferrite NPs by Q9 Thermoanaerobacter strain TOR-39 [168]. Coker et al. [160] described improvement of magnetic properties of biosynthesized magnetic NPs. In the study, FeCo-oxyhydroxides were created by adding CoCl2.6H2O to FeCl3 precursor and then treating them with Geobacter sulfurreducens culture. The resulting cobalt ferrite (CoFe2O4) NPs exhibited dramatically enhanced magnetic properties compared with simultaneously produced magnetite MNPs. Staniland et al. [169] described controlled cobalt doping of magnetosomes in vivo, where an estimated cobalt content of between 0.2 and 1.4% resulted in a 36–45% increase in the coercive field. Roh et al. [170] also reported Co, Cr, Mn and Ni doping of magnetite biosynthesized extracellularly by Thermoanaerobacter ethanolicus and a psychrotolerant Shewanella sp. In a follow-up report, these authors described how the process is amenable to large-scale

production and can produce magnetic particles at a fraction of the cost of traditional chemical synthesis [171]. Telling et al. [172] employed MNPs to catalyze Cr(VI) reduction (see also Section 3.4). MNPs were biosynthesized by Geobacter sulfurreducens and the reduction of Cr(VI) to Cr(III) at sites within the magnetic spinel surface were studied using X-ray absorption and X-ray magnetic circular dichroism. The same group also investigated the use of biosynthesized magnetites produced by G. sulfurreducens for recovery of metal contaminants from water [173]. MNPs produced by the bacterial reduction of powdered schwertmannite (an iron-oxyhydroxysulfate mineral) were found to be more efficient at reducing Cr(VI) than ferrihydrite (an oxyhydroxide mineral), ‘‘gel’’-derived biomagnetite and commercial nanoscale Fe3O4. One key advantage of MNPs is the ease of collection and recovery. Magnetic properties can also ensure that particles remain dispersed and distributed throughout a reaction vessel. Coker et al. [174] employed MNPs synthesized by G. sulfurreducens as a biomagnetic support for palladium nanocatalyst. The Pd-MNPs were used to catalyze the C–C bond-forming Mizoroki–Heck reaction, coupling iodobenzene to ethyl acrylate or styrene. Crean et al. [175] used a similar approach for the continuous removal of Cr(VI).

1115

6. Biosynthesis of unique formulations and geometries

1137

The properties and potential applications of nanoscale materials are determined by their chemical composition, crystal structure, particle size and particle shape. Several studies have described the biosynthesis of NPs with unique compositions and/or physical forms that will modulate performance in a range of applications (Table 14). NPs with certain chemical compositions have been difficult to synthesize using conventional chemical methods. Ahmad et al. [176] described fungal biosynthesis of transparent p-type conducting oxide CuAlO2 NPs with Humicola sp. In this case, traditional chemical synthesis is challenging because high temperatures are necessary for overcoming reaction barriers, but low temperatures are necessary for maintaining the Cu(1+) valence. Ankamwar et al. [177] introduced a biosynthetic approach

1138

Table 13 Application enhancements using magnetically responsive NPs. NP

Organism used

Application

References

Fe3O4 CoFe2O4 Fe3O4

Magnetite substituted with Zn Enhanced magnetic properties of biosynthesized composite Cobalt doping of magnetosomes

Fe3O4 Fe3O4

Thermoanaerobacter sp. TOR-39 Geobacter sulfurreducens Magnetospirillum gryphiswaldense, Magnetospirillum magnetotacticum Thermoanaerobacter ethanolicus, Shewanella sp. Thermoanaerobacter sp. TOR-39

Yeary et al. [168] Coker et al. [174] Staniland et al. [169] Roh et al. [170] Moon et al. [171]

Fe3O4 Fe3O4 Fe3O4 Fe3O4

G. G. G. G.

sulfurreducens sulfurreducens sulfurreducens sulfurreducens

Magnetite substituted with Co, Ni, Cr, Mn Magnetite substituted with Co, Ni, Cr, Mn, Zn and rare earth metals Cr(VI) remediation Cr(VI) and Tc(VII) remediation Magnetically recoverable Pd nanocatalyst Cr(VI) remediation

Telling et al. [172] Cutting et al. [173] Coker et al. [174] Crean et al. [175]

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1116 1117 1118 1119 1120 1121 1122 1123 1124 1125 1126 1127 1128 1129 1130 1131 1132 1133 1134 1135 1136

1139 1140 1141 1142 1143 1144 1145 1146 1147 1148 1149 1150 1151

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Table 14 Unique formulations and geometries. NP

Organism used

Application

References

CuAlO2 Au, Ag Au–Ag–Cu Au–Ag Au–Ag Au–Pd Au PbS, ZnS

Humicola sp. Emblica officinalis Brassica juncea Fusarium oxysporum Fusarium semitectum Escherichia coli Tamarindus indica Streptococcus thermophilus, Lactobacillus bulgaricus, Lactobacillus acidophilus Hansenula anomala

Difficult-to-synthesize NPs Phase transfer, transmetallation Alloy Alloy Alloy Core/shell Au/Pd NPs Nanotriangles, vapor sensing Hollow nanostructures; light harvesting and photocatalytic properties Bio-ink

Ahmad et al. [176] Ankamwar et al. [177] Haverkamp et al. [178] Senapati et al. [179] Sawle et al. [180] Deplanche et al. [181] Ankamwar et al. [182] Zhou et al. [122]

Au

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using transmetallation reactions. AgNPs and AuNPs phytosynthesized using Emblica officinalis fruit extract were transferred into methanol solution using a cationic surfactant, and transmetallation was carried out between AgNPs and chloroaurate ions in chloroform. The creation of metal alloys by casting requires heavy equipment and high temperatures. Bottom-up biosynthesis of Au–Ag–Cu alloys by Brassica juncea seed was introduced by Haverkamp et al. [178]. Similar studies reported bimetallic Au–Ag alloy biosynthesis employing the fungus Fusarium [179,180]. Deplanche et al. [181] likewise introduced a hybrid two-step method for the production of core–shell Pd–Au NPs by means of E. coli cells. NP biosynthesis can also result in NPs with various useful shapes. Ankamwar et al. [182] described the phytosynthesis of Au nanotriangles using tamarind (Tamarindus indica) leaf extract. The authors measured the electrical conductivity of these triangular NPs in different organic solvents, and suggested a possible chemical vapor sensor application. The biosynthesis of Ag nanoplates was described by Xie et al. [183], who employed the green alga Chlorella vulgaris. Hollow structures created for various photocatalytic applications were described in a paper by Zhou et al. [122], who coated empty bacterial cells with PbS and ZnS NPs. The authors chose bacteria with spherical (Streptococcus thermophilus) and rod-like shapes (Lactobacillus bulgaricus, L. acidophilus). Although the photocatalytic activity of the resulting hollow nanostructures had been described previously, the authors described additional uses, including as electromagnetic wave absorbers, ultraviolet shielding materials and photocatalysts for solar cells. Sathish Kumar et al. [184] biosynthesized Au NPs by means of the yeast Hansenula anomala and its extract. These AuNPs were further stabilized by the addition of two different types of poly(amido amine) dendrimers. The authors demonstrated the use of these AuNPs as bioink for rubber stamps.

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7. Future outlook of biosynthesized NPs

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This review highlights the key medical, environmental and industrial applications of biosynthesized NPs. The natural machinery used by all biological systems to execute redox reactions with specificity, in aqueous solution, and under conditions of standard temperature and pressure provides a powerful strategy for producing a wide range of nanosized materials, often at a fraction of the cost of traditional chemical synthesis. Biosynthesized NPs are frequently attached to a biological carrier or scaffold, and many feature biogenic capping materials that enhance the compatibility and stability of the NPs under environmental conditions. Capping agents are specific to the particular organisms used for biosynthesis, so a wide range of interesting properties can be achieved. Biosynthesized NPs have been used in nearly every field where traditional NPs have been employed. One of the challenges of biogenic NPs is the separation of the NPs from the biological material. In addition, contamination from biological cells can be a problem

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1202 especially in medical applications, due to the potential introduc1203 tion of allergens or pathogens. 1204 Considering the volume and growth in NP biosynthesis research 1205 in recent years, the field appears to be on the threshold of much more widespread and intensive research into applications. Q101206 1207 Meanwhile, further research and development of the underlying 1208 biosynthesis methods themselves and the creation of novel biosyn1209 thetic NP forms is anticipated.

Appendix A. Figures with essential colour discrimination

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Certain figures in this article, particularly Figs. 1–4 are difficult to interpret in black and white. The full colour images can be found in the on-line version, at doi:http://dx.doi.org/10.1016/j.actbio. 2014.05.022).

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