review article bacteria in nanoparticle synthesis:...

Review ArticleBacteria in Nanoparticle Synthesis Current Statusand Future Prospects

Siavash Iravani

Biotechnology Department Faculty of Pharmacy and Pharmaceutical Sciences Isfahan University of Medical SciencesIsfahan 81744-176 Iran

Correspondence should be addressed to Siavash Iravani siavashiragmailcom

Received 26 March 2014 Revised 9 July 2014 Accepted 4 August 2014 Published 29 October 2014

Academic Editor Matthias Labrenz

Copyright copy 2014 Siavash Iravani This is an open access article distributed under the Creative Commons Attribution Licensewhich permits unrestricted use distribution and reproduction in any medium provided the original work is properly cited

Microbial metal reduction can be a strategy for remediation of metal contaminations and wastes Bacteria are capable ofmobilization and immobilization of metals and in some cases the bacteria which can reduce metal ions show the ability toprecipitatemetals at nanometer scale Biosynthesis of nanoparticles (NPs) using bacteria has emerged as rapidly developing researcharea in green nanotechnology across the globe with various biological entities being employed in synthesis of NPs constantlyforming an impute alternative for conventional chemical and physicalmethodsOptimization of the processes can result in synthesisof NPs with desired morphologies and controlled sizes fast and clean The aim of this review is therefore to make a reflection onthe current state and future prospects and especially the possibilities and limitations of the above mentioned bio-based techniquefor industries

1 Introduction

Nanoscience and nanotechnology has attracted a great inter-est over the last few years due to its potential impact onmanyscientific areas such as energy medicine pharmaceuticalindustries electronics and space industries This technologydeals with small structures and small-sized materials ofdimensions in the range of few nanometers to less than 100nanometers Nanoparticles (NPs) show unique and consid-erably changed chemical physical and biological proper-ties compared to bulk of the same chemical compositiondue to their high surface-to-volume ratio NPs exhibit sizeand shape-dependent properties which are of interest forapplications ranging from biosensing and catalysts to opticsantimicrobial activity computer transistors electrometerschemical sensors and wireless electronic logic and memoryschemes These particles also have many applications indifferent fields such as medical imaging nanocompositesfilters drug delivery and hyperthermia of tumors [1ndash4]

An important area of research in nanoscience dealswith the synthesis of nanometer-size particles of differentmorphologies sizes and monodispersity [5] In this regardthere is a growing need to develop reliable nontoxic clean

ecofriendly and green experimental protocols for the syn-thesis of NPs [6ndash12] One of the options to achieve thisobjective is to use natural processes such as use of enzymesmicrobial enzymes vitamins polysaccharides biodegradablepolymers microorganisms and biological systems for syn-thesis of NPs One approach that shows immense potentialis based on the biosynthesis of NPs using bacteria (a kindof bottom up approach) [6 7 11] The objects of recentstudies tend to provide a controlled and up-scalable processfor biosynthesis of monodispersed and highly stableNPsThus a wide number of bacterial species have been used ingreen nanotechnology to research alternativemethods for thesynthesis of NPs Researchers have started to use biomassor cell extracts of bacteria for synthesizing NPs Bacteriaare considered as a potential biofactory for the synthesis ofNPs like gold silver platinum palladium titanium titaniumdioxide magnetite cadmium sulphide and so forth Somewell-known examples of bacteria synthesizing inorganicmaterials includemagnetotactic bacteria and S layer bacteriaMost metal ions are toxic for bacteria and therefore thebioreduction of ions or the formation of water insolublecomplexes is a defense mechanism developed by the bacteriato overcome such toxicity [13ndash16] In this review most of the

Hindawi Publishing CorporationInternational Scholarly Research NoticesVolume 2014 Article ID 359316 18 pageshttpdxdoiorg1011552014359316

2 International Scholarly Research Notices

bacteria used in nanoparticle biosynthesis are shownThe aimof this paper is therefore to make a reflection on the currentstate and future prospects and especially the possibilities andlimitations of the above mentioned bio-based technique forindustries

2 Bacteria in Nanoparticle Synthesis

Bacteriapossess remarkable ability to reduce heavy metalions and are one of the best candidates for nanoparticlesynthesis For instance somebacterial species have developedthe ability to resort to specific defense mechanisms to quellstresses like toxicity of heavy metal ions or metals It wasobserved that some of them could survive and grow evenat high metal ion concentrations (eg Pseudomonas stutzeriand Pseudomonas aeruginosa) [47 55] Moreover Brock andGustafson [56] reported that Thiobacillus ferrooxidans Tthiooxidans and Sulfolobus acidocaldariuswere able to reduceferric ion to the ferrous state when growing on elementalsulfur as an energy source T thiooxidans was able to reduceferric iron at low pH medium aerobically The ferrous ironformed was stable to autoxidation and T thiooxidans wasunable to oxidize ferrous iron but the bioreduction of ferriciron using T ferrooxidans was not aerobic because of therapid bacterial reoxidation of the ferrous iron in the presenceof oxygen [56] Other biomineralization phenomena suchas the formation of tellurium (Te) in Escherichia coli K12[57] the direct enzymatic reduction of Tc (VII) by restingcells of Shewanella (previouslyAlteromonas) putrefaciens andGeobactermetallireducens (previously known as strainGS-15)[58] and the reduction of selenite to selenium by Enterobac-ter cloacae Desulfovibrio desulfuricans and Rhodospirillumrubrum [26] have been reported as well Mullen et al [14]examined the ability of Bacillus cereus B subtilis E coliand P aeruginosa for removing Ag+ Cd2+ Cu2+ and La3+from solutionThey found that bacterial cells were capable ofbinding large quantities of metallic cations Moreover someof these bacteria are able to synthesize inorganicmaterials likethe magnetotactic bacteria which synthesize intracellularmagnetite NPs [53] In this section most of the bacterialspecies used in nanoparticle biosynthesis are shown (Table 1)

21 Silver NPs Saifuddin et al [22] have described a novelcombinational synthesis approach for green biosynthesis ofsilver NPs using a combination of culture supernatant ofBacillus subtilis and microwave irradiation in water Theyreported the extracellular biosynthesis of monodispersedsilver NPs (sim5ndash50 nm) using supernatants of B subtilisbut in order to increase the rate of reaction and reducethe aggregation of the produced NPs they used microwaveradiation which might provide uniform heating around theNPs and could assist the digestive ripening of particles withno aggregation [22] Kalishwaralal et al [59] reported extra-cellular synthesis of silver NPs (sim40 nm) by bioreduction ofaqueous Ag+ ions with the culture supernatant of Bacilluslicheniformis Moreover well-dispersed silver nanocrystals(sim50 nm)were synthesized usingB licheniformis [60] In caseof Bacillus flexus spherical and triangular shaped silver NPs

(sim12ndash65 nm) were successfully biosynthesized The NPs werestable in aqueous solution in five-month period of storageat room temperature in the dark These NPs showed efficacyon antibacterial property against clinically isolatedmultidrugresistant (MDR)microorganisms [61]Wei et al [62] reportedthe synthesis of circular and triangular crystalline silver NPs(sim146 nm) by solar irradiation of cell-free extracts of Bacillusamyloliquefaciens and silver nitrate (AgNO

3) Light intensity

extract concentration and NaCl addition influenced thesynthesis of silver NPs Under optimized conditions (solarintensity 70000 lx extract concentration 3mgmL andNaClcontent 2mM) 9823 plusmn 006 of the Ag+ (1mM) wasreduced to silver NPs within 80min Since heat-inactivatedextracts also mediated the formation of silver NPs enzymaticreactions are likely not involved in silver NPs formationThe produced NPs showed antimicrobial activity againstB subtilis and Escherichia coli in liquid and solid medium[62] Furthermore Bacillus cereus isolated from the Garciniaxanthochymus was used for green biosynthesis of silver NPs(sim20ndash40 nm) [18] The produced NPs showed antibacterialactivity against pathogenic bacteria like E coli Pseudomonasaeruginosa Salmonella typhi and Klebsiella pneumoniae

Pseudomonas stutzeriAG259 the silver-resistant bacterialstrain isolated from a silver mine intracellularly accumu-lated silver NPs along with some silver sulfide ranging in sizefrom 35 to 46 nm [63] Larger particles were formed whenP stutzeri AG259 challenged high concentrations of silverions during culturing resulting in intracellular formationof silver NPs ranging in size from a few nm to 200 nm[13 64] P stutzeri AG259 detoxificated silver through itsprecipitation in the periplasmic space and its bioreduction toelemental silver with a variety of crystal typologies such ashexagons and equilateral triangles as well as three differenttypes of particles elemental crystalline silver monoclinicsilver sulfide acanthite (Ag

2S) and a further undetermined

structure [64]The periplasmic space limited the thickness ofthe crystals but not their width which could be rather large(sim100ndash200 nm) [13]

Cell-free culture supernatants of five psychrophilicbacteria Phaeocystis antarctica Pseudomonas proteolyticaPseudomonas meridiana Arthrobacter kerguelensis andArthrobacter gangotriensis and two mesophilic bacteriaBacillus indicus and Bacillus cecembensis have been used tobiosynthesize silver NPs (sim6ndash13 nm) These NPs were stablefor 8 months in the dark The synthesis and stability of silverNPs appeared to depend on the temperature pH or thespecies of bacteria from which the supernatant was used Itwas observed that the A kerguelensis supernatant could notproduce silver NPs at the temperature where P antarcticacould synthesize silver NPs Therefore this study providedimportant evidence that the factors in the cell-free culturesupernatants which facilitated the synthesis of silver NPsvaried from bacterial species to species [65]

Our research group demonstrated the green biosynthesisof silver NPs using Lactobacillus casei subsp casei at roomtemperature [12] (Figure 1) Previous researchers reportedqualitative synthesis of silver NPs by Lactobacillus sp butthey did not optimize the reaction mixture The biosynthe-sized NPs were almost spherical single (sim25ndash50 nm) or in

International Scholarly Research Notices 3

Table 1 Green biosynthesis of NPs using bacteria

Bacteria Nanoparticle Size (nm) Morphology ReferencesAeromonas sp SH10 Silver 64 mdash [17]Bacillus cereus Silver 20ndash40 Spherical [18]Bacillus megatherium D01 Gold 19 plusmn 08 Spherical [19]Bacillus subtilis 168 Gold 5ndash25 Octahedral [20 21]Bacillus subtilis Silver 5ndash50 Spherical and triangular [22]Clostridium thermoaceticum Cadmium sulfide mdash Amorphous [23]Corynebacterium sp SH09 Silver 10ndash15 mdash [24]Desulfobacteraceae Zinc sulfide 2ndash5 Spherical [25]Desulfovibrio desulfuricans Palladium and selenium mdash mdash [26 27]

Desulfovibrio vulgaris Gold uranium andchromium mdash mdash [28]

Desulfovibrio magneticusstrain RS-1 Magnetite Up to 30 Crystalline [29]

Enterobacter cloacae Silver and selenium mdash mdash [26]Escherichia coli Cadmium sulfide 2ndash5 Wurtzite crystal [30]Escherichia coli Silver 8-9 Spherical [31]Escherichia coli DH5120572 Silver 10ndash100 Spherical [32]

Escherichia coli DH5120572 Gold 25 plusmn 8 Spherical triangular andquasi-hexagonal [33]

Escherichia coliMC4100 Gold Less than 10 to 50 Spherical triangular hexagonal androd shape [34]

Geobacillus sp Gold 5ndash50 Quasi-hexagonal [35]Geovibrio ferrireducens Gold mdash mdash [28]Klebsiella aerogenes Cadmium sulfide 20ndash200 Crystalline [36]

Klebsiella pneumonia Silver282ndash122(average size of522)

Spherical [37]

Lactobacillus strains Gold 20ndash50 and above100

Crystalline hexagonal triangular andcluster [38]

Lactobacillus strains Silver 15ndash500 Crystalline hexagonal triangular andcluster [38]

Lactobacillus strains Silver-gold alloys 100ndash300 Crystalline and cluster [38]Lactobacillus strains Titanium 40ndash60 Spherical [39]Lactobacillus casei subsp casei Silver 25ndash50 Spherical [12]Magnetospirillummagnetotacticum Magnetite mdash Cluster (folded-chain and flux-closure

ring) [40]

Nocardiopsis sp MBRC-1 Silver sim45 Spherical [41]

Plectonema boryanum UTEX 485 Gold10ndash25 andsim1ndash10 and10 to 6000

Cubic and octahedral Platelet [42 43]

Pseudomonas aeruginosa Gold 15ndash30 mdash [44]Pseudomonas aeruginosa Lanthanum mdash Crystalline and needle-like [12 14]Pseudomonas fluorescens Gold 50ndash70 Spherical [45]Pseudomonas putidaNCIM 2650 Silver sim70 Spherical [46]

Pseudomonasstutzeri AG259 Silver 35ndash46 and

up to 200

Hexagonal equilateral trianglecrystalline silver and monoclinic silversulfide acanthite

[47]

Rhodobacter sphaeroides Zinc sulfide Average diameterof 8 Spherical [48]

Rhodopseudomonas capsulata Gold 10ndash20 Nanoplate and spherical [15 49]


Table 1 Continued

Bacteria Nanoparticle Size (nm) Morphology ReferencesRhodopseudomonaspalustris Cadmium sulfide 801 plusmn 025 Crystalline face-centered cubic [50]

Serratia nematodiphila Silver 10ndash31 spherical and crystalline [51]Shewanella algae Platinum 5 elemental [52]

Shewanella algae strain BRY Gold Various sizeschanged with pH mdash [28]

Shewanella putrefaciens(Gs-15) Magnetite 10ndash50 Fine-grained crystal [53]

Thermoanaerobacter ethanolicusTOR-39

Magnetitecobalt nickel andchromium

mdash Octahedral [13 54]

Figure 1 Our research group demonstratedthe bioreductive syn-thesis of silver NPs using Lactobacillus casei subsp casei (anunpublished TEM image recorded from silver NPs synthesized byreaction of silver nitrate solution (1mM) with L casei subsp casei)

aggregates (sim100 nm) attached to the surface of biomass orwere inside and outside of the cellsThe bioreduction ofmetalions and stabilization of the silver NPs were confirmed tooccur by an enzymatic process Electron microscopy analysisindicated that the silverNPswere formed on the surface of thecytoplasmic cell membrane inside the cytoplasm and outsideof the cells possibly due to the bioreduction of the metal ionsby enzymes present on the cytoplasmicmembrane andwithinthe cytoplasm [12]

A number of metal-reducing bacteria have been iso-lated and characterized from a variety of habitats andmuch work has focused on Shewanella oneidensis andGeobacter spp [66] The biosynthesis of extracellular silver-based single nanocrystallites ofwell-defined composition andhomogeneous morphology utilizing the 120574-proteobacteriumS oneidensis MR-1 upon incubation with aqueous silvernitrate solution was reported Further characterization ofthese particles revealed that the crystals consist of small

reasonably monodispersed spheres in the 2ndash11 nm size range(sim 4 plusmn 15 nm) [67]

The rapid biosynthesis of silver NPs using the biore-duction of aqueous Ag+ ion by the culture supernatantsof Klebsiella pneumonia E coli and Enterobacter cloacae(Enterobacteriaceae) was reported [37]The synthetic processwas quite fast and the produced NPs were formed within5min of silver ions coming in contact with the cell filtratePiperitone (a natural product which show an inhibitoryeffect on nitro reduction activity of Enterobacteriaceae) couldpartially inhibit the bioreduction of silver ions to silverNPs by different strains of Enterobacteriaceae including Kpneumoniae As a result of this control experiment nitrore-ductase enzymes might be responsible for bioreduction ofsilver ions Recently it was shown that visible-light emissioncould significantly prompt synthesis of silver NPs by culturesupernatants of K pneumoniae [68] Silver NPs with uniformsize and shape (sim1ndash6 nm) were biosynthesized using silverchloride (as the substrate)

When some quantities of NaOH were added to thebioreduction system silver NPs were successfully preparedwith reduction of [Ag(NH

3)2]+ by Aeromonas sp SH10

and Corynebacterium sp SH09 [69] It was speculated that[Ag(NH

3)2]+ first reacted with OHminus to form Ag

2O which

was then metabolized independently and reduced to silverNPs by the biomass The color of the bioreduction systemchanged from pale yellow to dark yellow The silver NPswere monodispersed and uniform in size without distinctaggregation and it was observed that the solution containingthe NPs remained stable for more than six monthsThe colorchange indicated the formation of silver NPs in the reactionmixture as it is well-known that silver NPs exhibit strikingcolors (light yellow to brown) due to excitation of surfaceplasmon vibrations (SPV) in the particles [70]

22 Gold NPs It was reported that Bacillus subtilis 168 wasable to reduce Au3+ ions to octahedral gold NPs (sim5ndash25 nm)within bacterial cells by incubation of the cells with goldchloride under ambient temperature and pressure conditions[20 21] The reduction processes of chloroaurate and silverions by B subtilis were found to be different [71] Gold NPswere biosynthesized both intracellularly and extracellularlywhile silver NPs were exclusively formed extracellularly


The gold NPs were formed after one day of addition ofchloroaurate ions while the silver NPs were formed afterseven days Transmission electronmicroscopy (TEM)micro-graphs depicted the formation of gold NPs intracellularly andextracellularly which had an average size of 76plusmn18 and 73plusmn23 nm respectively while silver NPs were exclusively formedextracellularly with an average size of 61 plusmn 16 nm The bac-terial proteins were analyzed by sodium dodecyl sulfonate-polyacrylamide electrophoresis (SDS-PAGE) before and afterthe addition of metal ion solutions Satyanarayana et alreported that proteins of a molecular weight between 25 and66 kDa could be responsible for chloroaurate ions reductionwhile the formation of silver NPs could be attributed toproteins of a molecular weight between 66 and 116 kDaTheyreported that the NPs were stabilized by the surface-activemolecules that is surfactin or other biomolecules releasedinto the solution by B subtilis

Bacillus megateriumD01 have shown the strong potentialof Au3+ adsorption [19] When B megaterium D01 biomasswas exposed to the aqueous solution of HAuCl

4 monodis-

persed spherical gold NPs capped with self-assembledmono-layer (SAM) of thiol of 19 plusmn 08 nm sizes have been syn-thesized extracellularly The gold NPs were stable withoutany aggregation over a period of several weeks Thereforeby addition of dodecanethiol (as the capping ligand) intothe reactionmixture monodispersed spherical gold NPs wereproduced Moreover Lactobacillus strains when exposed togold ions resulted in formation of gold NPs within thebacterial cells [38] It was reported that exposure of lactic acidbacteria present in the whey of buttermilk tomixtures of goldions could be used to grow gold NPs The nucleation of goldNPs occurred on the cell surface through sugars and enzymesin the cell wall and then the metal nuclei were transportedinto the cell where they aggregated to larger-sized particles

All members of the genus Shewanella reported so farare facultatively anaerobic gram-negative motile by polarflagella rod-like and generally associated with aquatic ormarine habitats [72ndash79] Most of Shewanella species aremesophilic psychrotolerant and psychrophilic bacteria [7280] Shewanella alga is a gram-negative bacillus which iswidely distributed in the environment and its natural habitatsare water and soil [81] Konishi et al [82] reported microbialdeposition of gold NPs using S algae This bacteriumcangrow anaerobically in medium with lactate or H

2as the

electron donor and Fe (III) citrate as the electron acceptorThey demonstrated that resting cells of S algae were capableof reducing AuCl

4

minus ions (1mM) into elemental gold within30min at 25∘C over the pH range from 20 to 70 whenH

2gas

was provided as the electron donor [83] At pH 70 biogenicgold NPs (sim10ndash20 nm) were deposited in the periplasmicspace of S algae cells When the solution pH decreased tobelow 28 some gold NPs were deposited extracellularly Atthis pH the biogenic gold NPs (sim15ndash200 nm) on the bacterialcells exhibited various morphologies At a solution of pH 20biogenic gold NPs (sim20 nm) were deposited on the bacterialcells and larger gold particles (sim350 nm) were depositedextracellularly Thus it could be concluded that the solutionpH is an important factor in controlling the morphology of

biogenic gold NPs and in the location of gold deposition[82] They observed that the decrease in the soluble Au (III)concentration was presumably caused by its rapid reductioninto insoluble gold In the absence of H

2gas however S

algae cells were not able to reduce Au (III) with lactate asan alternative electron donor Moreover in a sterile controlmedium without S algae cells Au (III) was not chemicallyreduced by H

2gas Thus resting cells of S algae were able to

reduce the soluble Au (III) into insoluble gold in the presenceof molecular H

2as the electron donor [28 84]

Escherichia coli DH5120572 can be used in synthesizing goldNPs (sim 25 plusmn 8 nm) [33] Shapes and sizes of the NPs were nothomogenous They were mostly spherical and a few amountsof triangles and quasi-hexagons were observed as well TEMmicrographs showed that goldNPswere bound on the surfaceof the bacteria Using E coli-gold NPs composite Liangweiet al made an Hb-coli-nAu-Glassy Carbon electrode whichcould be used to achieve the direct electrochemistry ofhemoglobin In another study biorecovery of gold fromjewellery wastes was obtained using E coli MC4100 (non-pathogenic strain) and Desulfovibrio desulfuricans ATCC29577 [34] When these bacteria were exposed to HAuCl

4

solution (2mM) gold NPs was formed In order to controlsize and shape of the NPs Deplanche et al investigatedthe influence of pH on Au (III) bioreduction using E coliand D desulfuricans At acidic pH spherical gold NPs (lessthan 10 nm diameter) were produced but at pH 70 and 90a mixture of smaller (sim10 nm) and bigger (sim50 nm) well-defined triangles hexagons and rods were formed

Rhodopseudomonas capsulata showed the ability to pro-duce gold NPs in different sizes and the shape of goldNPs was controlled by pH [15] R capsulate was capable ofproducing gold NPs extracellularly and the gold NPs werequite stable in the solution The aqueous chloroaurate ionswere reduced during exposure to the biomass and the colorof the reaction solution turned from pale yellow to purpleWhen the pHwas adjusted to 4 a number of nanoplates wereobserved in addition to the spherical gold NPs in the reactionsolution Size and morphology of gold NPs might be affectedby AuCl

4

minus ions concentration At lower concentration ofAuCl4

minus ions as the substrate spherical gold NPs (sim10ndash20 nm)were synthesized exclusively while at higher concentrationsnetworked gold nanowires were produced in the aqueoussolution [49] The AuCl

4

minus ions could bind to the biomassthrough themain groups of secreted enzymesThese enzymesshowed an important role in reduction of AuCl

4

minus ionsBioreduction of Au (3+) to Au (0) and formation of goldNPs might be due to NADH dependent enzymes which weresecreted by R capsulateThemechanism of reduction seemedto be initiated by electron transfer from NADH by NADHdependent reductase as the electron carrier

Lengke et al [42] controlled morphology of goldNPs using filamentous cyanobacteria such as Plectonemaboryanum UTEX 485 They produced cubic gold NPs (lt10ndash25 nm) and octahedral gold platelets (sim1ndash10120583m) interactingP boryanum UTEX 485 with aqueous Au (S

2O3)

2

3minus andAuCl4

minus solutions at 25ndash100∘C for up to 1 month and at 200∘Cfor one day The interaction of cyanobacteria with aqueous


Au (S2O3)

2

3minus promoted the precipitation of cubic gold NPs atmembrane vesicles and admixed with gold sulfide within thecells and encrusted on the cyanobacteria whereas reactionwith AuCl

4

minus resulted in the precipitation of octahedral goldplatelets in solutions and NPs of gold (lt10 nm) within bacte-rial cellsMoreover themechanisms of gold bioaccumulationby cyanobacteria from gold (III)-chloride solutions haveshown that the interaction of cyanobacteria with aqueousgold (III)-chloride initially promoted the precipitation ofNPs of amorphous gold (I)-sulfide at the cell walls andfinally deposited metallic gold in the form of octahedral (III)platelets (sim10 nmndash6120583m) near cell surfaces and in solutions[43]

Plant-growth-promoting bacteria isolated from Philip-pine soils were screened for their ability to extracellularlysynthesize gold NPs Extracellular synthesis of gold NPs(sim10ndash100 nm) was determined by incubation of the plant-growth-promoting culture supernatant with gold (III) chlo-ride trihydrate (HAuCl

4∙3H2O) for 7 days at 28∘C It was

suggested that nitrate reductase was one of the enzymesresponsible in the bioreduction of ionic gold [85]

23 Magnetite NPs Desulfovibrio magneticus strain RS-1 isan anaerobic sulfate-reducing bacterium which also respiresand grows with fumarate as the terminal electron acceptor[86] D magneticus strain RS-1 accumulated magnetite NPsintracellularly Most magnetite crystals in the cells were onlyslightly larger than 30 nm (super paramagnetic NPs) [29]Klaus-Joerger reported that metals including Co Cr and Nimight be substituted into magnetite crystals biosynthesizedin the thermophilic iron-reducing bacterium Thermoanaer-obacter ethanolicus (TOR-39) [13 54 87] This procedure ledto formation of octahedral-shaped magnetite (Fe

3O4) NPs

(lt12 nm) in large quantities that coexisted with a poorlycrystalline magnetite phase near the surface of the cells[87] A more fundamental investigation in the assemblyof single-domain magnetite particles into folded-chain andflux-closure ring morphologies by harvested magnetotacticbacterium Magnetospirillum magnetotacticum was carriedout by Philipse and Maas [40] Magnetic NPs were alsoassembled into ordered structures when the motion of Mmagnetotacticum (MS-1) was controlled by applying a mag-netic field [88]

Fe (III) is an important oxidant of natural and contam-inant organic compound in surface and subsurface aquaticsediments [89 90] Fe (III) and Mn (IV) could influencethe inorganic geochemistry of sedimentary environmentby greatly increasing the dissolved concentration of irontrace metal manganese and phosphate [91 92] Sulfate-reducing bacteria were capable of producing magnetic ironsulfide (FeS) NPs Adsorption of radioactive metals by thesemagnetic iron sulfide NPs occurred due to high surfacearea (400ndash500m2g) which could provide a suitable matrixfor the long-term safe storage of hazardous radioactivepertechnetate ion [93 94] GS-15 (an obligately anaerobicgram-negative rod) oxidized simple organic compoundssuch as acetate butyrate and ethanol to carbon dioxidewith Fe (III) or Mn (IV) as the sole electron acceptor [5395] Iron-reducing microorganism GS-15 produced copious

quantities of ultrafine-grainedmagnetite with size range of 10to 50 nm under anaerobic conditions by coupling the organicmatter to the reduction of ferric iron [53] In this process thenonmagnetic brown amorphic ferric oxidewas converted to ablack solidmaterial which was strongly attracted to amagnetBut GS-15 was not magnetotactic because the crystals wereclearly external to the cells and were not aligned in chainsLovely et al [96] investigated the ability of Alteromonasputrefaciens to couple the oxidation of potential electrondonors (such as lactate pyruvate hydrogen and formate) tothe reduction of Fe (III) and Mn (IV) Also they reportedthat Pelobacter acetylenicus and P venetianus were able toreduce Fe (III) They demonstrated that P carbinolicus wascapable of conversing energy to support growth from Fe (III)respiration as it also grew with H

2or formate as the electron

donor and Fe (III) as the electron acceptor P carbinolicusgrewwith ethanol (ethanol wasmetabolized to acetate) as thesole electron donor and Fe (III) as the sole electron acceptorGrowth was also possible on Fe (III) with the oxidation ofpropanol to propionate or butanol to butyrate if acetate wasprovided as a carbon source [97]

Jahn et al [98] discovered a novelmechanism for electrontransfer from iron-reducing microorganisms to insolubleiron phases They monitored iron reduction kinetics withsoluble electron acceptors such as ferric citrate ferrihydritecolloids and solid ferrihydrite Roden and Lovley [99] havedemonstrated that the marine strain of Desulfuromonasacetoxidans was capable of dissimilatory Fe (III) and Mn(IV) reduction They reported that washed cell suspensionsof the type strain of D acetoxidans reduced soluble Fe (III)-citrate and Fe (III) complexedwith nitriloacetic acid Ethanolpropanol pyruvate and butanol served as electron donorsfor Fe (III) reduction as well In addition Kashefi andLovley [100] reported that P islandicum owns the ability toreduce Fe (III) at 100∘C in a medium with hydrogen as theelectron donor and Fe (III)-citrate as the electron acceptorCell suspensions of P islandicum reduced the followingmetals with hydrogen as the electron donor U (VI) Tc(VII) Cr (VI) Co (III) and Mn (IV) The reduction ofthese metals was dependent upon the presence of cells andhydrogen In contrast P islandicum could not reduce As (V)or Se (VII) Reducing varieties of metals by P islandicumplays an important role in geological phenomena and haveapplication for remediation of metal contaminated waterThermus specieswere able to reduce U (VI) Cr (VI) and Co(III) at 60∘C [101]Thermophilic (45 to 75∘C) bacteria showedthe ability to reduce amorphous Fe (III)-oxyhydroxide tomagnetic iron oxides [102] They could reduce Cr (VI)and Co (III) at temperatures of up to 65∘C as well [103]Hyperthermophilic metal reducing microorganisms couldhelp preventing migration of these contaminants by reduc-ing them to less mobile forms Hot radioactive or metal-containing industrial wastes could potentially be treated inbioreactors containing microorganisms with a metabolismlike that of P islandicum or their enzymes [100]

Many mesophilic microorganisms which own the abilityto use Fe (III) as a terminal electron acceptor could alsoreduce a variety of metals and metalloids other than Fe(III) [104 105] Fe (III)-reducing bacteria and archaea were


capable of precipitating gold by reducing Au (III) to Au(0) [28] The reaction seemed to be enzymatically catalyzedwhich were dependent on temperature and the presenceof hydrogen (as a specific electron donor) Many Fe (III)-reducing microorganisms could reduce forms of oxidizedmetals including radio nuclides such as uranium (VI) [8995ndash101] and technetium (VII) [28 89 98ndash103] and tracemetals including arsenic (V) [30 106] chromium (VI) [8992 94 98 104 105] cobalt (III) [1 15 30 89 92 106] man-ganese (IV) [100 107] and selenium (VI) [82 108] Many ofthesemetals andmetalloids are environmental contaminantsTherefore Fe (III)-reducing microorganisms could be usedfor removal of contaminant metals from waters and wastestreams and immobilization of metals in subsurface environ-ments Microbial reduction of some of these metals may alsoplay an important role in the formation of metal depositswhich may be especially important in hot environmentscontaining metal-rich waters [33 107ndash111] Common productof bacterial iron reduction nanosized magnetic particlesenabled early disease detection and accurate prognosis andpersonalized treatment monitoring efficacy of a prescribedtherapy or study of cellular interaction in a certain biologicalenvironment [109 110] These particles might have differentapplications in radionuclide therapy drug delivery mag-netic resonance imaging (MRI) diagnostics immunoassaysmolecular biology DNA and RNA purification cell separa-tion and purification cell adhesion research hyperthermia[111 112] andmagnetic ferrofluids for magnetocaloric pumps[113 114]

24 Palladium and Platinum NPs The sulfate-reducing bac-terium Desulfovibrio desulfuricans [27 115] and metal ion-reducing bacterium Shewanella oneidensis were capable ofreducing soluble palladium (II) into insoluble palladium (0)with formate lactate pyruvate or H

2as the electron donor

[116] Konishi et al [52] demonstrated that resting cells of Salgae were able to deposit platinum NPs by reducing PtCl

6

2minus

ions within 60min at pH 7 and 25∘C Biogenic platinumNPs of about 5 nm were located in the periplasmic space Inthis case the cell suspension changed the color from paleyellow to black in 10min The black appearance provided aconvenient visible signature for the microbial formation ofmetallic platinum NPs The observed decrease in aqueousplatinum concentration was presumably caused by the rapidreduction of PtCl

6

2minus ions into insoluble platinum In theabsence of lactate however S algae cells were not able toreduce the PtCl

6

2minus ions They reported that the PtCl6

2minus ionswere not chemically reduced by lactate Yong et al [117] alsoreported that the sulfate-reducing bacteriumD desulfuricanswas able to adsorb only 12 of platinum (IV) ions on thebacterial cells from 2mM platinum chloride solution Inanother study Gram-negative cyanobacterium P boryanumUTEX 485 extracellularly produced Pt (II)-organics andmetallic platinum NPs at 25ndash100∘C for up to 28 days and180∘C for 1 day with different morphologies of sphericalbead-like chains and dendritic in the size range of 30 nmndash03 120583m [118]

25 Selenium and Tellurium NPs Selenium has photo-optical and semiconducting properties that have applica-tions in photocopiers and microelectronic circuit devicesStenotrophomonas maltophilia SELTE02 showed promisingtransformation of selenite (SeO

3

minus2) to elemental selenium

(Se0) accumulating selenium granules either in the cell cyto-plasm or in the extracellular space In addition Enterobactercloacae SLD1a-1 Rhodospirillum rubrum and Desulfovibriodesulfuricans have also been found to bioreduce seleniteto selenium both inside and outside the cell with variousmorphologies like spherical fibrillar and granular structureor with small atomic aggregates E coli also depositedelemental selenium both in periplasmic space and cytoplasmand P stutzeri also aerobically reduced selenite to elementalselenium [119] Under aerobic conditions Hunter andManter[120] reported that Tetrathiobacter kashmirensis bioreducedselenite to elemental red selenium A 90-kDa protein presentin the cell-free extract was believed to be responsible forthis bioreduction Moreover Yadav et al [121] showed that Paeruginosa SNT1 biosynthesized nanostructured selenium bybiotransforming selenium oxyanions to spherical amorphousallotropic elemental red selenium both intracellularly andextracellularly In addition Sulfurospirillum barnesii Bacillusselenitireducens and Selenihalanaerobacter shriftii synthe-sized extracellularly stable uniform nanospheres (sim300 nm)of elemental selenium Se0 with monoclinic crystalline struc-tures [122] Microbial synthesis of elemental selenium (Se0)nanospheres resulted in unique complex compacted nanos-tructured arrangements of Se atoms These arrangementsresulted due to the dissimilatory reductions that were subtlydifferent in different microbes In another study stablepredominantly monodispersed and spherical selenium NPs(with an average size of 21 nm) were synthesized using thebacterial isolate Pseudomonas aeruginosa strain JS-11 Thebacteria exhibited significant tolerance to selenite (SeO

3

2minus)

up to 100mM concentration with an EC50

value of 140mMThe culture supernatant contained the potential of reducingsoluble and colorless SeO

3

2minus to insoluble red elementalselenium (Se0) at 37∘C It was suggested that the metabo-lite phenazine-1-carboxylic acid released by strain JS-11 inculture supernatant along with the known redox agents likeNADH and NADH dependent reductases was responsiblefor biomimetic reduction of SeO

3

2minus to Se0 nanospheres Theauthors elucidated that the red colored Se0 nanospheres mayserve as a biosensor for nanotoxicity assessment contem-plating the inhibition of SeO

3

2minus bioreduction process in NPstreated bacterial cell culture supernatant as a toxicity endpoint In other words the formation of red Se0 from SeO

3

2minus

could serve as a molecular marker whereas the inhibitionof critical bioreduction step was considered as a toxicity endpoint for the qualitative and quantitative toxicity assessment[123]

Tellurium (Te) has been reduced from tellurite to ele-mental tellurium by two anaerobic bacteria Bacillus selen-itireducens and Sulfurospirillum barnesii B selenitireducensinitially formed nanorods of 10 nm in diameter and 200 nmin length were clustered together to form larger rosettesof sim1000 nm but with S barnesii small irregularly shaped


extracellular nanospheres of diameter lt50 nm were formed[124] In another study tellurium-transforming Bacillus spBZ isolated from the Caspian Sea in northern Iran wasused for the intracellular biosynthesis of elemental telluriumNPs The biogenic NPs were released by liquid nitrogen andpurified by an n-octyl alcohol water extraction system TEManalysis showed rod-shaped NPs with dimensions of about20 nm times 180 nm The produced NPs had a hexagonal crystalstructure [125]

26 Zinc Oxide NPs Zinc oxide (ZnO) NPs have uniqueoptical and electrical properties and as a wide band gapsemiconductor they have found more uses in biosensorsnanoelectronics and solar cells These NPs are being usedin the cosmetic and sunscreen industry due to their trans-parency and ability to reflect scatter and absorbUVradiationand as food additives Furthermore zinc oxide NPs arealso being considered for use in next-generation biologicalapplications including antimicrobial agents drug deliveryand bioimaging probes [126] A low-cost and simple proce-dure for synthesis of zinc oxide NPs using reproducible bac-terium Aeromonas hydrophila was reported X-ray diffrac-tion (XRD) confirmed the crystalline nature of the NPs andatomic force microscopy (AFM) showed the morphologyof the nanoparticle to be spherical oval with an averagesize of 5772 nm The antibacterial and antifungal activitywas ended with corresponding well diffusion and minimuminhibitory concentration The maximum zone of inhibitionwas observed in the ZnO NPs (25120583gmL) against Pseu-domonas aeruginosa (sim22 plusmn18mm) and Aspergillus flavus(sim19 plusmn10mm) [126]

27 Titanium and Titanium Dioxide NPs Spherical titanium(Ti) NPs (sim40ndash60 nm) were produced extracellularly usingthe culture filtrate of Lactobacillus sp at room temperature[39] These NPs were lighter in weight and have highresistance to corrosion and have enormous applications inautomobiles missiles airplanes submarines cathode raytubes and desalting plants and have promising future rolein cancer chemotherapy and gene delivery TiO

2(titanium

dioxide) NPs has been explored in various biomedical appli-cations such as wound dressing biosensing contrast agentstargeted drug delivery agents antiwrinkle and antimicro-bial and antiparasitic agents owing to their nontoxic andbiocompatible properties [127] These NPs were biologicallysynthesized by using Bacillus subtilis The morphologicalcharacteristics were found to be spherical oval in shapeindividual NPs as well as a few aggregates having the sizeof 66ndash77 nm The XRD shows the crystallographic plane ofanatase of titanium dioxide NPs indicating that NPs struc-ture dominantly corresponds to anatase crystalline titaniumdioxide [128] In another study biosynthesis of titaniumdioxide NPs by a metal resistant bacterium isolated fromthe coal fly ash effluent was reported The bacterial strainon the basis of 16S rDNA technique and the biochemicalparameters was identified to be Propionibacterium jensenii[KC545833] a probiotic high G + C rich pleomorphicrod shaped gram-positive bacteria The produced NPs were

smooth and spherical in shape and ranged in size from 15 to80 nm [127]

28 Cadmium Sulphide NPs Several investigations haveshown that cadmium sulphide particles could be microbiallyproduced in Klebsiella aerogenes [36] and the yeasts such asCandida glabrata and Schizosaccharomyces pombe [129 130]Holmes et al [36] have demonstrated that the exposure ofthe bacterium K aerogenes to Cd2+ ions resulted in theintracellular formation of CdS NPs in the size range of 20ndash200 nm They also showed that the buffer composition ofthe growth medium plays an important role in formation ofcadmium sulfide crystallites Cadmium sulphide uptake byK aerogenes cells grown in the presence of 2mM Cd (NO

3)2

could be up to approximately 20 of the total biomass [36]Synthesis of semiconductor NPs such as CdS ZnS and

PbS for application as quantum-dot fluorescent biomarkersand cell labeling agents was reported [131]These luminescentquantum dots are emerging as a new class of materials forbiological detection and cell imaging based on the conju-gation of semiconducting quantum dots and biorecognitionmolecules Bacteria have been used with considerable successin the synthesis of CdS NPs [33 85 94] Clostridium ther-moaceticum (an acetogenic bacterium) showed the ability togrow autotrophically on CO

2and H

2 utilizing the so-called

Wood-Ljungdahl pathway to synthesize acetyl coenzyme A(acetyl-CoA) a starting material for the anabolic processesof these cells [132] Cunningham et al [23] reported thatC thermoaceticum was able to precipitate cadmium extra-cellularly at an initial concentration of 1mM This processwas energy dependent and required cysteine The yellowprecipitate of CdS appeared approximately 12 h after theaddition of CdCl

2and complete removal of the metal from

the growth medium was accomplished within 72 h CdSwas precipitated from CdCl

2in the presence of cysteine

hydrochloride by C thermoaceticum at the cell surface and inthemedium [23]Rhodopseudomonas palustriswas capable ofproducing cadmium sulfide NPs when it was incubated with1mM CdSO

4at 30∘C for 72 h [50] The researchers of this

study found that C-S-lyase (an intracellular enzyme locatedin the cytoplasm) was responsible for the synthesis of NPsOne of the interesting results of this studywas thatR palustristransported CdS NPs out of the cell

In another case E coli when incubated with cadmiumchloride (1mM) and sodium sulfide (1mM) showed thecapacity to synthesize intracellular semiconductor cadmiumsulfide (CdS) nanocrystals [30] The nanocrystals were com-posed of a wurtzite crystal phase with a size distribution of 2ndash5 nm Nanocrystals formation varied dramatically dependingon the growth phase of the cells Scanning transmission elec-tron microscopy (STEM) and high resolution transmissionelectron microscopy (HRTEM) revealed that nanocrystalsformation increased about 20-fold in E coli grown in thestationary phase cells compared to late logarithmic phasecultures

29 Zinc Sulfide NPs Labrenz et al [25] reported that spher-ical aggregates of 2 to 5 nm diameter sphalerite zinc sulfide


(ZnS) particles were formed within natural biofilms dom-inated by sulfate-reducing bacteria of the family of Desul-fobacteraceae A combination of geochemical and microbialprocesses led to ZnS biomineralization in a complex naturalsystem It is appropriate to mention that the concentrationof Zn was significantly reduced to below-acceptable levelsfor drinking water with the use of this method Rhodobactersphaeroides has been developed for the synthesis of ZnS NPswith an average diameter of 8 nm [48] In another study ZnSNPs (sim105plusmn 015 nm) were produced by using R sphaeroides[133]

3 Mechanistic Aspects

The ability of bacteria to survive and grow in stressfulsituations might be due to specific mechanisms of resistancewhich include efflux pumps metal efflux systems inactiva-tion and complexation of metals impermeability to metalsand the lack of specific metal transport systems alterationof solubility and toxicity by changes in the redox state ofthe metal ions extracellular precipitation of metals andvolatilization of toxic metals by enzymatic reactions [134135] For examplePseudomonas stutzeriAG259 isolated fromsilver mines has been shown to produce silver NPs [136]There are several examples of microorganisms-metal interac-tions which are important in biotechnological applicationsincluding the fields of biomineralization bioremediationbioleaching and microbial-influenced corrosion (MIC) pro-cesses Understanding of MIC processes in terms of micro-bially mediated localized changes in the surface chemistryof carbon steel stainless steel copper alloys or other onesis gaining growing attention [137] Bacteria also intervenein mineral precipitation reactions directly as catalysts ofaqueous chemical reactions and indirectly as geochemicallyreactive solids [138] and showed the ability to oxidate miner-als [139] These processes are commercially used in bacterialleaching operations such as the pretreatment of gold oreswhich contain arsenopyrite (FeAsS) [139]

Microbial metal reduction can be a strategy for in situand ex situ remediation of metal contaminations and wastesIn order to find out the relevance of nanoparticle synthesisand metal reduction biorecovery of heavy metals and biore-mediation of toxic ones researchers have investigated themechanisms of nanoparticle synthesis and bioreduction andfocused their attention on reducing agents in bacteria (egproteins and enzymes) and biochemical pathways leadingto metal ion reduction Because of the critical role of theseagents there were more investigations in understanding therole and application of natural and genetically engineeredbacterial strains andothermicroorganisms in bioremediationof toxic metals and radionuclide-contaminated terrestrialenvironments Moreover these microorganisms were capa-ble of mobilization and immobilization of metals [140]and in some cases the bacteria which could reduce metalions showed the ability to precipitate metals at nanometerscale These studies would then lead to check the possi-bility of genetically engineered microorganisms to overex-press specific reducing molecules and to develop microbialnanoparticle synthesis procedures which might potentially

control size shape stability and yield of NPs Actuallygenetically engineered microorganisms have started beingdeveloped in order to increase protein secretion and thuselucidate the most probable reducing agent For instanceKang et al [141] explored for the first time the systematicapproach toward the tunable synthesis of semiconductor CdSnanocrystals by genetically engineered E coli To explore thefeasibility of using E coli as a biofactory for the controlledsynthesis of CdS nanocrystals a strain was endowed withthe ability to produce phytochelatins (PCs) by expressingthe PC synthetase of S pombe (SpPCS) PCs serve as abinding templatenucleation site for the metal ions andstabilize the nanocrystal core against continued aggregationA feedback-desensitized gamma-glutamylcysteine synthase(GSHIlowast) which catalyzes the synthesis of the PC precursorglutathione (GSH) was cotransformed to enhance the levelof PC synthesis 10-fold After promoted PC synthesis CdSnanocrystals were produced with a size distribution of 2ndash6 nm Moreover it was proven that glutathione synthetaseoverexpression in ABLEC E coli strains in conjunction withmetal stress simultaneously enhanced the biosynthesis ofintracellular glutathione andCdSNPs [142] In another studystable NPs were recently achieved using the engineeringof the Desulfovibrio desulfuricans flagellar FliC protein Theintroduction of additional cysteine-derived thiol residuesin the E coli FliC protein increased Au (III) sorption andreduction on the surface of the flagellar filament and resultedin the synthesis of stabilized gold NPs (20ndash50 nm) Exhibitedbiosorption values were about 3 times higher than in the wildtype Wild type flagellar filaments showed fewer gold NPs(sim15ndash50 nm) [34] Moreover a strain of Bacillus licheniformiswas optimized for 120572-amylase production for the synthesisof gold NPs (10ndash50 nm) [143] Recombinant strains havebeen explored for developing more efficient organisms in thein vivo synthesis of NPs For instance recombinant E colistrains expressing Arabidopsis thaliana phytochelatin syn-thase (AtPCS) andor Pseudomonas putida metal-lothionein(PpMT) were used for the synthesis of Cd Se Zn Te CsSr Fe Co Ni Mn Au Ag Pr and Gd NPs Adjusting theconcentrations of supplied metal ions resulted in controllingthe size of the metal NPs

It was reported that the engineered E coli system canbe applicable to the biological synthesis of metal NPs [144]Mutant strains of some bacteria used for synthesis of NPscould help to elucidate the molecules involved in the biore-duction process For instance three E coli mutants lackingone or more of the [NiFe] hydrogenases appeared to exhibitaltered patterns of Pd (0) deposition as compared to theparental strain Mutant strains produced highly catalytic PdNPs by bioreduction of Pd (II)These studies of hydrogenase-deficient mutants suggest that the location of the Pd(0)deposits is in accordance with the subcellular localization ofthe remaining active hydrogenase and that all three hydro-genases could contribute to Pd (II) reduction in vivo [145]Besides wild type and three hydrogenase-deficient strains ofDesulfovibrio fructosivoranswere used for the reduction of Pd(II) to Pd(0) The localization of palladium was coincidentwith the localization of the hydrogenase suggesting thatthis enzyme serves as a nucleation site and assists initial Pd


nanoparticle growth probably by supplying the electrons forPd (II) reduction [146]

In case of Acidithiobacillus thiooxidans gold (I)-thiosul-fate was entered into the cell of A thiooxidans as part ofa metabolic process [147] This gold complex was initiallydecomplexed to Au(I) and thiosulfate (S

2O3

2minus) ions Thio-sulfate was used as energy source and Au(I) was presumablyreduced to elemental gold within the bacterial cells Duringthe late stationary growth phase the gold NPs which wereinitially precipitated inside the cells were released from thecells resulting in the formation of gold particles at the cellsurface Finally the gold particles in the bulk solution weregrown into micrometer-scale wire and octahedral gold [147]

According to Lengke and Southam [148 149] the pre-cipitation of gold (I)-thiosulfate complex by sulfate-reducingbacteria was caused by three possible mechanisms (a) ironsulfide formation (b) localized reducing conditions and (c)a metabolic process In the iron system the formation ofiron sulfide generated by sulfate-reducing bacteria could haveadsorbed a gold (I)-thiosulfate complex onto freshly formingsurfaces leading to the precipitation of elemental gold Thelocalized reducing conditions generated by sulfate-reducingbacteria were associated with metabolism Thiosulfate ionfrom a gold (I)-thiosulfate complex was initially reduced tohydrogen sulfide (HSminus) as the end product of metabolismThe release of hydrogen sulfide through the outer membranepores decreased redox conditions around the cells and causedthe precipitation of elemental gold The precipitation of ele-mental gold by sulfate-reducing bacteria through metabolicprocess was initiated when a gold (I)-thiosulfate entered thebacterial cells and was decomplexed to Au(I) and thiosulfateions Thiosulfate was used as energy source and Au(I) waspresumably reduced to elemental gold within the bacterialcells During the late stationary growth phase or death phasethe gold NPs which were initially precipitated inside the cellswere released into the bulk solution and formed subocta-hedral to octahedral subspherical to spherical aggregatesresembling framboids and ultimately millimeter-thick goldfoil at longer experimental duration [148 149]

Several studies widely reported the act of cytoplasmicand periplasmic hydrogenases produced by microorganismsin metal reduction [38 72] In order to show the criticalrole of these enzymes researchers used Cu (II) as a selectiveinhibitor of periplasmic hydrogenases For example In case ofD desulfuricans and E coli partial inhibition of periplasmichydrogenases with Cu (II) showed that these metal reductaseenzymes play a role in Au (III) reduction [34] Lioyd et al[115] concluded that periplasmic hydrogenases were possiblyresponsible for Pd (II) reduction and inhibited by Cu (II)Furthermore Au (III) reduction was done in the presenceof H2(as the electron donor) using microorganisms such

as T maritima S alga D vulgaris G ferrireducens Ddesulfuricans and E coli Possibly hydrogenases play animportant role in Au (III) reduction [28 34 84] but moreinvestigations were needed to know exact mechanisms ofthese reductions Moreover it was reported that hydrogenaseis involved in U+6 reduction byMicrococcus lactyliticus [150]in addition to Se+6 reduction by Clostridium pasteurianum

[151] Hydrogenases from the sulfate-reducing bacteria havebeen shown to be capable of reducing Tc+7 and Cr+6 [152]In another study it was reported that the hydrogenasesisolated from phototrophic bacteria were able to reduce Ni+2to Ni0 under an H

2atmosphere [153] In case of S algae

the microbial reduction of gold ions was dependent on thepresence of a specific electron donor the molecular H

2 It

was concluded that the S algae hydrogenase catalyzes theactivation of molecular H

2using the molecule as the electron

donor according to the following reaction

H2997888rarr 2H+ + 2eminus (1)

Therefore the S algae cells are likely to transfer electrons toAuCl4

minus ions reducing them to gold metals Consider

AuCl4

minus

+ 3eminus 997888rarr Au + 4Clminus (2)

In some cases researchers purified proteins which werebelieved to be responsible for nanoparticle synthesis Mat-sunaga et al [154] have shown thatMagA gene and its protein(isolated from Magnetospirillum sp AMB-1) were requiredfor biomagnetic nanoparticle formation Magnetotactic bac-teria (eg M magnetotacticum and M gryphiswaldense)contain magnetosome membrane (MM) proteins which playan important role in magnetite biomineralization Thusresearchers have focused on identification of these proteinsand their genes [155 156] Recentmolecular studies includinggenome sequence mutagenesis gene expression and pro-teome analyses indicated a number of genes and proteinswhich play critical roles for bacterial magnetic particlesbiomineralization [157]Moisescu et al [158] have studied thechemical composition and microstructural characteristics ofbacterial magnetosomes extracted from the magnetotacticbacterial strain M gryphiswaldense They reported the pro-duced cuboctahedral magnetite particles with an averagediameter of 46 plusmn 68 nm The particles exhibited a highchemical purity (exclusively Fe

3O4) and the majorities fall

within the single-magnetic-domain rangeIn cases of Rhodopseudomonas capsulata and Stenotroph-

omonas maltophilia the authors believed that the specificNADPH-dependent enzyme present in the isolated strainsreduced Au+3 to Au0 through an electron shuttling mecha-nism leading to the synthesis of monodispersed NPs A two-step process is needed to reduce gold ions During the firststep the AuCl

4

minus ions are reduced to the Au+ species Thenthe latter product is reduced by NADHP to a metallic gold[77 78]

Mechanisms of gold accumulation by the cyanobacteriastudied from gold chloride initially promoted the precipita-tion of amorphous gold sulfide at the cell walls and finallydeposited metallic gold in octahedral form near the cellsurfaces and in solutions [43] Moreover it was reportedthat the formation of gold NPs by Plectonema boryanumUTEX 485 occurred by three possible mechanisms involvingiron sulfide localized reducing conditions and metabolism[148] Lengke et al [118] biosynthesized spherical platinumNPs using cyanobacterium P boryanum UTEX 485 Theaddition of PtCl40 to the bacterial culture initially promoted


the precipitation of Pt+2-organic metal as spherical NPs inthe solution which then dispersed within the bacterial cellsThe cyanobacteria were immediately killed either by thePtCl40 by the acidic pH or by the elevated temperatures(sim60ndash180∘C) the resulting release of organics caused furtherprecipitation of platinum With an increase in temperaturethe Pt2-organic NPs were recrystallized and formed NPsconsisting of a platinum metal Riddin et al [159] reportedthe bioreduction of Pt+4 into the Pt0 NPs A mixed anduncharacterized consortium of sulphate-reducing bacteriawas used to investigate the mechanism in the platinumnanoparticle formation It was shown that two differenthydrogenase enzymes were involved First the Pt+4 ionswere reduced to Pt+2 by an oxygen-sensitive cytoplasmichydrogenase Then the formed ions were reduced to Pt0 NPsby a periplasmic hydrogenase that was oxygen tolerant andwas inhibited by Cu+2

To control the morphologies and sizes of NPs there wereseveral investigations focused on using proteins Interest-ingly association of proteins with spheroidal aggregates ofbiogenic zinc sulfide nanocrystals documented that extracel-lular proteins originated from microorganisms could limitthe biogenic NPs [160] Controlled formation of magnetitecrystals with uniformed size was achieved in the presence ofMms6 (a small acidic protein isolated fromMagnetospirillummagneticum AMB-1) [161] The average size of magnetitecrystals synthesized in the presence of Mms6 was about202 + 40 nm But in the absence of Mms6 the synthesizedmagnetite crystals were about 324 + 91 nm Therefore thecrystals synthesized with Mms6 were smaller than crys-tals produced without Mms6 and were distributed over anarrower range than crystals synthesized in the absence ofthe protein Mms6 also promoted formation of uniformisomorphic superparamagnetic nanocrystals [162] With abioinspired method Prozorov et al [163] have reportedthe use of the recombinant Mms6 protein for synthesisof uniform well-defined CoFe

2O4nanocrystals in vitro In

order to template hierarchical CoFe2O4nanostructures a

recombinant polyhistidine-tagged full-length Mms6 proteinand a synthetic C-terminal domain of this protein werecovalently attached to triblock copolymers (poloxamers)

In case of Klebsiella pneumoniae it was reported that noformation of silver NPs by the supernatant was observedwhen the procedure took place in the dark The visible-light emission can significantly cause the synthesis of NPsIt seems that in this case the silver ions reduction wasmainly due to conjugation shuttles with the participationof the reductase Thus it appears that the cell-associatednitroreductase enzymes may be involved in the photore-duction of silver ions [164] In addition mechanisms ofcadmium sulfide nanocrystals synthesis by E coli cells wereexplained through the control experiments (incubation ofCdCl2and Na

2S without bacterial cells) which indicated

that nanocrystals were not synthesized outside the cells andthen transported into the cells [30] These experiments haveshown that CdS nanocrystals could be synthesized followingCd2+ and S2minus ions transported into the cells In case ofzinc sulfide (ZnS) the NPs could be formed intracellularly

through the biological synthetic method suggested by Baiet al [48] They explained that soluble sulfate diffused intoimmobilized beads and then was carried to the interiormembrane of R sphaeroides cell facilitated by sulfate per-mease After that ATP sulfurylase and phosphoadenosinephosphosulfate reductase reduced sulfate to sulfite and sulfitereductase reduced sulfite to sulfide which reacted with O-acetylserine to synthesize cysteine via O-acetylserine thiollyaseThen cysteine produced S2minus by a cysteine desulfhydrasein presence of zinc After this process spherical ZnSNPsweresynthesized following the reaction of S2minus with the solublezinc salt These NPs were discharged from immobilized Rsphaeroides cells to the solution

4 Future Prospects

Major drawbacks associated with the biosynthesis of NPsusing bacteria are tedious purification steps and poorunderstanding of the mechanisms The important challengesfrequently encountered in the biosynthesis of NPs are tocontrol the shape and size of the particles and to achievethe monodispersity in solution phase It seems that severalimportant technical challenges must be overcome before thisgreen bio-based method will be a successful and competitivealternative for industrial synthesis of NPs An importantchallenge is scaling up for production level processingFurthermore little is known about the mechanistic aspectsand information in this regard is necessary for economicand rational development of nanoparticle biosynthesis Theimportant aspects which might be considered in the processof producing well-characterized NPs are as follows

(1) Selection of the best bacteria In order to choose thebest candidates researchers have focused on someimportant intrinsic properties of the bacteria includ-ing growth rate enzyme activities and biochemicalpathways Choosing a good candidate for nanoparti-cle production depends on the application we expectfrom the resulting NPs For instance one may needto synthesis NPs with smaller sizes or specific shapesor it might be important to synthesize NPs within lesstime [6 11]

(2) Selection of the biocatalyst state It seems that thebacterial enzymes (the biocatalysts) are the majoragents in nanoparticle synthesis The biocatalysts canbe used as either of whole cells crude enzymesand purified enzymes It seems that using culturesupernatant or cell extract of the cell could increasethe rate of reaction However these NPs did not showthe long term stability Moreover release of NPs fromthe cells was an important aspect which might beconsidered in case of intracellularly produced NPsMost of the reactions responsible for nanoparticlesynthesis seem to be bioreductions In bioreductionprocesses we need the coenzymes (eg NADHNADPH FAD etc) to be supplied in stoichiometricamounts As they are expensive the use of whole cellsis preferred because the coenzymes will be recycledduring the pathways in live whole cells [11]


(3) Optimal conditions for cell growth and enzyme activityWe need to produce greater amounts of the enzymeswhich can be accomplished by synthesis of morebiomassThus optimization of the growth conditionsis very important The nutrients inoculum size pHlight temperature buffer strength and mixing speedshould be optimized Induction of the responsibleenzymes seems to be crucial as well The presence ofthe substrates or related compounds in subtoxic levelsfrom the beginning of the growth would increase theactivity Harvesting time is important in case of usingwhole cells and crude enzymesTherefore it might benecessary to monitor the enzyme activity during thetime course of growth [11]

(4) Optimal reaction conditions It is better to harvest thecells (the biocatalysts) to remove unwanted residualnutrients and metabolites in order to avoid adversereactions and provide cleaner medium for better andeasier analysis In order to use bacteria for synthesisof nanoparticle in industrial scale the yield and theproduction rate are important issues to be consideredTherefore we need to optimize the bioreductionconditions in the reaction mixture The substrateconcentration (to be in subtoxic level for the bio-catalyst) the biocatalyst concentration the electrondonor (and its concentration) exposure time pHtemperature buffer strength mixing speed and lightneed to be optimized The researchers have usedsome complementary factors such as visible light ormicrowave irradiation and boiling which could affectthe morphology size and rate of reaction It seemsthat by optimization of these critical parametershighly stableNPswith desired sizes andmorphologiescan be achieved In addition purification isolationand stabilization of the produced NPs are veryimportant and challenges in this regard must beovercome Researchers have focused their attentionon finding optimal reaction conditions and cellularmechanisms involved in the bioreduction of metalions and synthesis of NPs [6ndash12 165]

(5) Extraction and purification processes The extractionand purification of the produced metal NPs frombacteria (intercellular or extracellular synthesis) forfurther applications are not well investigated butstudies are moving toward solving these problemsand finding the best ways In order to release theintracellularly produced NPs additional processingsteps such as ultrasound treatment or reaction withsuitable detergents are requiredThis can be exploitedin the recovery of precious metals from mine wastesand metal leachates Biomatrixed metal NPs couldalso be used as catalysts in various chemical reactionsThis will help to retain the NPs for continuous usagein bioreactors Physicochemical methods includingfreeze-thawing heating processes and osmotic shockcan be used to extract the produced NPs from thecells But it seems that these methods may interfere

with the structure of NPs and aggregation precipi-tation and sedimentation could happen These maychange the shape and size of NPs and interfere withthe suitable properties of them Moreover enzymaticlysis of the microbial cells containing intracellularNPs can be used but this method is expensiveand it cannot be used in up-scalable and industrialproduction of NPs It seems that surfactants andorganic solvents can be used for both extraction andstabilization of NPs but these chemical materials aretoxic expensive and hazardous It should be notedthat in case of extracellular production of nanopar-ticle centrifuge could be used for extraction andpurification of NPs but aggregation might happen

(6) Stabilization of the produced NPs Researchers haveillustrated that the NPs produced by these ecofriendlybio-based approaches showed an interesting stabilitywithout any aggregations even for many weeks inroom temperature [19 166]The stability of these NPsmight be due to the proteins and enzymes secreted bythe microorganisms Thus it seems that these greenapproaches can be used for synthesis of highly stableNPs

(7) Scaling up the laboratory process to the industrial scaleOptimization of the reaction conditions may lead tothe enhanced biosynthesis of NPs Biological proto-cols could be used for synthesis of highly stable andwell-characterized NPs when critical aspects such astypes of organisms inheritable and genetical proper-ties of organisms optimal conditions for cell growthand enzyme activity optimal reaction conditions andselection of the biocatalyst state have been consideredSize and morphology of the NPs can be controlledby altering the aforementioned reaction conditions(optimal reaction conditions section) Industrial scalesynthesis of metal NPs using biomass needs someprocesses including seed culture inoculation of theseed into the biomass harvesting the cells synthesisof NPs by adding metal ions to the cells separationof cells by filtration homogenization of the cells toisolate the produced NPs stabilization of the NPsproduct formulation and quality control [6ndash12 165]

5 Conclusion

Bio-based approaches are still in the development stages andstability and aggregation of the biosynthesizedNPs control ofcrystal growth shape size and size distribution are the mostimportant experienced problems Furthermore biologicallysynthesized NPs in comparison with chemically synthesizedones are more polydisperse The properties of NPs can becontrolled by optimization of important parameters whichcontrol the growth condition of organisms cellular activitiesand enzymatic processes (optimization of growth and reac-tion conditions)

Mechanistic aspects have not been clearly and deeplydescribed and discussed Thus more elaborated studies areneeded to know the exact mechanisms of reaction and


identify the enzymes and proteins which involve nanoparticlebiosynthesisThe large-scale synthesis ofNPs using bacteria isinteresting because it does not need any hazardous toxic andexpensive chemical materials for synthesis and stabilizationprocesses It seems that by optimizing the reaction conditionsand selecting the best bacteria these natural nanofactoriescan be used in the synthesis of stable NPs with well-definedsizes morphologies and compositions

Conflict of Interests

The author declares that there is no conflict of interestsregarding the publication of this paper

Acknowledgment

This review was supported by Faculty of Pharmacy and Phar-maceutical Sciences Isfahan University of Medical Sciences

References

[1] D Bhattacharya and R K Gupta ldquoNanotechnology and poten-tial of microorganismsrdquo Critical Reviews in Biotechnology vol25 no 4 pp 199ndash204 2005

[2] D Goodsell Bionanotechnology Lessons from Nature Willey-Less New Jersey NJ USA 2004

[3] R Paull J Wolfe P Hebert and M Sinkula ldquoInvesting innanotechnologyrdquoNature Biotechnology vol 21 no 10 pp 1144ndash1147 2003

[4] O V Salata ldquoApplications of nanoparticles in biology andmedicinerdquo Journal of Nanobiotechnology vol 2 no 1 article 32004

[5] M Sastry A Ahmad M Islam Khan and R Kumar ldquoBiosyn-thesis of metal nanoparticles using fungi and actinomyceterdquoCurrent Science vol 85 no 2 pp 162ndash170 2003

[6] S Iravani ldquoGreen synthesis ofmetal nanoparticles using plantsrdquoGreen Chemistry vol 13 no 10 pp 2638ndash2650 2011

[7] S Iravani H Korbekandi S V Mirmohammadi and HMekanik ldquoPlants in nanoparticle synthesisrdquo Reviews inAdvanced Sciences and Engineering vol 3 no 3 pp 261ndash2742014

[8] S Iravani and B Zolfaghari ldquoGreen synthesis of silver nanopar-ticles using Pinus eldarica bark extractrdquo Biomed ResearchInternational vol 2013 Article ID 639725 5 pages 2013

[9] H Korbekandi Z Ashari S Iravani and S Abbasi ldquoOptimiza-tion of biological synthesis of silver nanoparticles using Fusar-ium oxysporumrdquo Iranian Journal of Pharmaceutical Researchvol 12 no 3 pp 289ndash298 2013

[10] H Korbekandi and S Iravani ldquoBiological synthesis of nanopar-ticles using algaerdquo in Green Biosynthesis of NanoparticlesMechanisms and Applications M Rai and C Posten Eds pp53ndash60 CABI Wallingford UK 2013

[11] H Korbekandi S Iravani and S Abbasi ldquoProduction ofnanoparticles using organismsrdquo Critical Reviews in Biotechnol-ogy vol 29 no 4 pp 279ndash306 2009

[12] H Korbekandi S Iravani and S Abbasi ldquoOptimization of bio-logical synthesis of silver nanoparticles using Lactobacillus caseisubsp caseirdquo Journal of Chemical Technology amp Biotechnologyvol 87 no 7 pp 932ndash937 2012

[13] T Klaus-Joerger R Joerger E Olsson and C GranqvistldquoBacteria as workers in the living factory metal-accumulatingbacteria and their potential for materials sciencerdquo Trends inBiotechnology vol 19 no 1 pp 15ndash20 2001

[14] M D Mullen D C Wolf F G Ferris T J Beveridge CA Flemming and G W Bailey ldquoBacterial sorption of heavymetalsrdquoApplied and EnvironmentalMicrobiology vol 55 no 12pp 3143ndash3149 1989

[15] S He Z Guo Y Zhang S Zhang J Wang and N Gu ldquoBiosyn-thesis of gold nanoparticles using the bacteria Rhodopseu-domonas capsulatardquoMaterials Letters vol 61 no 18 pp 3984ndash3987 2007

[16] M F Lengke M E Fleet and G Southam ldquoBiosynthesisof silver nanoparticles by filamentous cyanobacteria from asilver(I) nitrate complexrdquo Langmuir vol 23 no 5 pp 2694ndash2699 2007

[17] A Rai A Singh A Ahmad and M Sastry ldquoRole of halide ionsand temperature on themorphology of biologically synthesizedgold nanotrianglesrdquo Langmuir vol 22 no 2 pp 736ndash741 2006

[18] S Sunkar and C V Nachiyar ldquoBiogenesis of antibacterial silvernanoparticles using the endophytic bacterium Bacillus cereusisolated from Garcinia xanthochymusrdquo Asian Pacific Journal ofTropical Biomedicine vol 2 no 12 pp 953ndash959 2012

[19] L Wen Z Lin P Gu et al ldquoExtracellular biosynthesis ofmonodispersed gold nanoparticles by a SAM capping routerdquoJournal of Nanoparticle Research vol 11 no 2 pp 279ndash2882009

[20] T J Beveridge and R G E Murray ldquoSites of metal depositionin the cell wall of Bacillus subtilisrdquo Journal of Bacteriology vol141 no 2 pp 876ndash887 1980

[21] G Southam and T J Beveridge ldquoThe in vitro formation ofplacer gold by bacteriardquo Geochimica et Cosmochimica Acta vol58 no 20 pp 4527ndash4530 1994

[22] N Saifuddin C W Wong and A A N Yasumira ldquoRapidbiosynthesis of silver nanoparticles using culture supernatantof bacteria withmicrowave irradiationrdquo E-Journal of Chemistryvol 6 no 1 pp 61ndash70 2009

[23] D P Cunningham and L L Lundie Jr ldquoPrecipitation ofcadmium by Clostridium thermoaceticumrdquo Applied and Envi-ronmental Microbiology vol 59 no 1 pp 7ndash14 1993

[24] H R Zhang Q B Li Y H Lu et al ldquoBiosorption andbioreduction of diamine silver complex by CorynebacteriumrdquoJournal of Chemical Technology and Biotechnology vol 80 no3 pp 285ndash290 2005

[25] M Labrenz G K Druschel T Thomsen-Ebert et al ldquoForma-tion of sphalerite (ZnS) deposits in natural biofilms of sulfate-reducing bacteriardquo Science vol 290 no 5497 pp 1744ndash17472000

[26] J Kessi M Ramuz E Wehrli M Spycher and R BachofenldquoReduction of selenite and detoxification of elemental sele-nium by the phototrophic bacterium Rhodospirillum rubrumrdquoApplied and Environmental Microbiology vol 65 no 11 pp4734ndash4740 1999

[27] P Yong N A Rowson J P G Farr I R Harris and L EMacaskie ldquoBioreduction and biocrystallization of palladiumbyDesulfovibrio desulfuricansNCIMB 8307rdquo Biotechnology andBioengineering vol 80 no 4 pp 369ndash379 2002

[28] K Kashefi J M Tor K P Nevin and D R Lovley ldquoReductiveprecipitation of gold by dissimilatory Fe(III)-reducing bacteriaand archaeardquo Applied and Environmental Microbiology vol 67no 7 pp 3275ndash3279 2001


[29] M Posfai B M Moskowitz B Arato et al ldquoPropertiesof intracellular magnetite crystals produced by Desulfovibriomagneticus strain RS-1rdquo Earth and Planetary Science Letters vol249 no 3-4 pp 444ndash455 2006

[30] R Y Sweeney C Mao X Gao et al ldquoBacterial biosynthesis ofcadmium sulfide nanocrystalsrdquo Chemistry and Biology vol 11no 11 pp 1553ndash1559 2004

[31] A Mahanty R Bosu P Panda S P Netam and B SarkarldquoMicrowave assisted rapid combinatorial synthesis of silvernanoparticles using E coli culture supernatantrdquo InternationalJournal of Pharma and Bio Sciences vol 4 no 2 pp 1030ndash10352013

[32] H R Ghorbani ldquoBiosynthesis of silver nanoparticles byEscherichia colirdquo Asian Journal of Chemistry vol 25 no 3 pp1247ndash1249 2013

[33] L Du H Jiang X Liu and E Wang ldquoBiosynthesis of goldnanoparticles assisted by Escherichia coli DH5120572 and its appli-cation on direct electrochemistry of hemoglobinrdquo Electrochem-istry Communications vol 9 no 5 pp 1165ndash1170 2007

[34] K Deplanche and L E Macaskie ldquoBiorecovery of gold byEscherichia coli and Desulfovibrio desulfuricansrdquo Biotechnologyand Bioengineering vol 99 no 5 pp 1055ndash1064 2008

[35] D N Correa-Llanten S A Munoz-Ibacache M E Castro PA Munoz and J M Blamey ldquoGold nanoparticles synthesizedbyGeobacillus sp strain ID17 a thermophilic bacterium isolatedfromDeception IslandAntarcticardquoMicrobial Cell Factories vol12 no 1 article 75 2013

[36] J D Holmes P R Smith R Evans-Gowing D J Richardson DA Russell and J R Sodeau ldquoEnergy-dispersive X-ray analysisof the extracellular cadmium sulfide crystallites of Klebsiellaaerogenesrdquo Archives of Microbiology vol 163 no 2 pp 143ndash1471995

[37] A R Shahverdi S Minaeian H R Shahverdi H Jamalifar andA Nohi ldquoRapid synthesis of silver nanoparticles using culturesupernatants of Enterobacteria a novel biological approachrdquoProcess Biochemistry vol 42 no 5 pp 919ndash923 2007

[38] B Nair and T Pradeep ldquoCoalescence of nanoclusters andformation of submicron crystallites assisted by Lactobacillusstrainsrdquo Crystal Growth and Design vol 2 no 4 pp 293ndash2982002

[39] K Prasad A K Jha and A R Kulkarni ldquoLactobacillus assistedsynthesis of titaniumnanoparticlesrdquoNanoscale Research Lettersvol 2 no 5 pp 248ndash250 2007

[40] A P Philipse and D Maas ldquoMagnetic colloids from mag-netotactic bacteria chain formation and colloidal stabilityrdquoLangmuir vol 18 no 25 pp 9977ndash9984 2002

[41] P Manivasagan J Venkatesan K Senthilkumar K Sivakumarand S Kim ldquoBiosynthesis antimicrobial and cytotoxic effectof silver nanoparticles using a novel Nocardiopsis sp MBRC-1rdquoBioMed Research International vol 2013 Article ID 287638 9pages 2013

[42] M F Lengke M E Fleet and G Southam ldquoMorphology ofgold nanoparticles synthesized by filamentous cyanobacteriafrom gold(I)-Thiosulfate and gold(III)-chloride complexesrdquoLangmuir vol 22 no 6 pp 2780ndash2787 2006

[43] M F Lengke B Ravel M E Fleet G Wanger R A Gordonand G Southam ldquoMechanisms of gold bioaccumulation byfilamentous cyanobacteria from gold(III)-chloride complexrdquoEnvironmental Science andTechnology vol 40 no 20 pp 6304ndash6309 2006

[44] M I Husseiny M A El-Aziz Y Badr and M A Mah-moud ldquoBiosynthesis of gold nanoparticles using Pseudomonas

aeruginosardquo Spectrochimica Acta AMolecular and BiomolecularSpectroscopy vol 67 no 3-4 pp 1003ndash1006 2007

[45] S R Rajasree and T Y Suman ldquoExtracellular biosynthesisof gold nanoparticles using a gram negative bacterium Pseu-domonas fluorescensrdquo Asian Pacific Journal of Tropical Diseasevol 2 no 2 pp S796ndashS799 2012

[46] V Thamilselvi and K V Radha ldquoSynthesis of silver nanoparti-cles from Pseudomonas putidaNCIM 2650 in silver nitrate sup-plemented growth medium and optimization using responsesurface methodologyrdquo Digest Journal of Nanomaterials andBiostructures vol 8 no 3 pp 1101ndash1111 2013

[47] C Haefeli C Franklin and K Hardy ldquoPlasmid-determinedsilver resistance in Pseudomonas stutzeri isolated from a silverminerdquo Journal of Bacteriology vol 158 no 1 pp 389ndash392 1984

[48] H Bai Z Zhang and J Gong ldquoBiological synthesis of semicon-ductor zinc sulfide nanoparticles by immobilized Rhodobactersphaeroidesrdquo Biotechnology Letters vol 28 no 14 pp 1135ndash11392006

[49] S He Y Zhang Z Guo and N Gu ldquoBiological synthesis ofgold nanowires using extract of Rhodopseudomonas capsulatardquoBiotechnology Progress vol 24 no 2 pp 476ndash480 2008

[50] H J Bai Z M Zhang Y Guo and G E Yang ldquoBiosynthesisof cadmium sulfide nanoparticles by photosynthetic bacteriaRhodopseudomonas palustrisrdquo Colloids and Surfaces B Bioint-erfaces vol 70 no 1 pp 142ndash146 2009

[51] C Malarkodi S Rajeshkumar K Paulkumar M Vanaja G DG Jobitha andGAnnadurai ldquoBactericidal activity of biomedi-ated silver nanoparticles synthesized by Serratia nematodiphilardquoDrug Invention Today vol 5 no 2 pp 119ndash125 2013

[52] Y Konishi K Ohno N Saitoh et al ldquoBioreductive depositionof platinum nanoparticles on the bacterium Shewanella algaerdquoJournal of Biotechnology vol 128 no 3 pp 648ndash653 2007

[53] D R Lovley J F Stolz G L Nord Jr and E J P PhillipsldquoAnaerobic production of magnetite by a dissimilatory iron-reducing microorganismrdquo Nature vol 330 no 6145 pp 252ndash254 1987

[54] L W Yeary J Moon L J Love J RThompson C J Rawn andT J Phelps ldquoMagnetic properties of biosynthesized magnetitenanoparticlesrdquo IEEE Transactions on Magnetics vol 41 no 12pp 4384ndash4389 2005

[55] K Bridges A Kidson E J L Lowbury and M D WilkinsldquoGentamicin- and silver-resistant Pseudomonas in a burnsunitrdquo British Medical Journal vol 1 no 6161 pp 446ndash449 1979

[56] T D Brock and J Gustafson ldquoFerric iron reduction bysulfur- and iron-oxidizing bacteriardquo Applied and Environmen-tal Microbiology vol 32 no 4 pp 567ndash571 1976

[57] D E Taylor ldquoBacterial tellurite resistancerdquo Trends in Microbiol-ogy vol 7 no 3 pp 111ndash115 1999

[58] J R Lloyd J Ridley T Khizniak N N Lyalikova and L EMacaskie ldquoReduction of technetium by Desulfovibrio desulfu-ricans biocatalyst characterization and use in a flowthroughbioreactorrdquo Applied and Environmental Microbiology vol 65no 6 pp 2691ndash2696 1999

[59] K Kalishwaralal V Deepak S Ramkumarpandian H Nella-iah and G Sangiliyandi ldquoExtracellular biosynthesis of silvernanoparticles by the culture supernatant of Bacillus licheni-formisrdquoMaterials Letters vol 62 no 29 pp 4411ndash4413 2008

[60] K Kalimuthu R Suresh Babu D Venkataraman M Bilal andS Gurunathan ldquoBiosynthesis of silver nanocrystals by Bacilluslicheniformisrdquo Colloids and Surfaces B Biointerfaces vol 65 no1 pp 150ndash153 2008


[61] S Priyadarshini V Gopinath N Meera Priyadharsshini DMubarakAli and P Velusamy ldquoSynthesis of anisotropic silvernanoparticles using novel strain Bacillus flexus and its biomed-ical applicationrdquo Colloids and Surfaces B Biointerfaces vol 102pp 232ndash237 2013

[62] XWei M LuoW Li et al ldquoSynthesis of silver nanoparticles bysolar irradiation of cell-free Bacillus amyloliquefaciens extractsandAgNO

3rdquoBioresource Technology vol 103 no 1 pp 273ndash278

2012[63] R M Slawson M I Van Dyke H Lee and J T Trevors

ldquoGermanium and silver resistance accumulation and toxicityin microorganismsrdquo Plasmid vol 27 no 1 pp 73ndash79 1992

[64] T Klaus R Joerger E Olsson and C Granqvist ldquoSilver-basedcrystalline nanoparticles microbially fabricatedrdquo Proceedings ofthe National Academy of Sciences of the United States of Americavol 96 no 24 pp 13611ndash13614 1999

[65] S Shivaji S Madhu and S Singh ldquoExtracellular synthesis ofantibacterial silver nanoparticles using psychrophilic bacteriardquoProcess Biochemistry vol 46 no 9 pp 1800ndash1807 2011

[66] D R Lovley ldquoDissimilatory Fe(III) and Mn(IV) reductionrdquoMicrobiological Reviews vol 55 no 2 pp 259ndash287 1991

[67] A K Suresh D A Pelletier W Wang et al ldquoSilver nanocrys-tallites biofabrication using shewanella oneidensis and anevaluation of their comparative toxicity on gram-negative andgram-positive bacteriardquo Environmental Science and Technologyvol 44 no 13 pp 5210ndash5215 2010

[68] N Mokhtari S Daneshpajouh S Seyedbagheri et al ldquoBio-logical synthesis of very small silver nanoparticles by culturesupernatant of Klebsiella pneumonia the effects of visible-lightirradiation and the liquid mixing processrdquo Materials ResearchBulletin vol 44 no 6 pp 1415ndash1421 2009

[69] M Fu Q Li D Sun et al ldquoRapid preparation process of silvernanoparticles by bioreduction and their characterizationsrdquoChinese Journal of Chemical Engineering vol 14 no 1 pp 114ndash117 2006

[70] S Kapoor ldquoPreparation characterization and surface modifi-cation of silver particlesrdquo Langmuir vol 14 no 5 pp 1021ndash10251998

[71] R A Satyanarayana C Chen J Jean et al ldquoBiological synthesisof gold and silver nanoparticles mediated by the bacteriaBacillus subtilisrdquo Journal of Nanoscience and Nanotechnologyvol 10 no 10 pp 6567ndash6574 2010

[72] J P Bowman S AMcCammonD SNichols et al ldquoShewanellagelidimarina sp nov and Shewanella frigidimarina sp novnovel antarctic species with the ability to produce eicosapen-taenoic acid (2051205963) and grow anaerobically by dissimilatoryfe(III) reductionrdquo International Journal of Systematic Bacteriol-ogy vol 47 no 4 pp 1040ndash1047 1997

[73] N Bozal M J Montes E Tudela F Jimenez and J GuinealdquoShewanella frigidimarina and Shewanella livingstonensis spnov isolated fromAntarctic coastal areasrdquo International Journalof Systematic and Evolutionary Microbiology vol 52 no 1 pp195ndash205 2002

[74] E P Ivanova T Sawabe N M Gorshkova et al ldquoShewanellajaponica sp novrdquo International Journal of Systematic andEvolutionary Microbiology vol 51 no 3 pp 1027ndash1033 2001

[75] E P Ivanova O I Nedashkovskaya N V Zhukova D V Nico-lau R Christen and V V Mikhailov ldquoShewanella waksmaniisp nov isolated from a sipunculla (Phascolosoma japonicum)rdquoInternational Journal of Systematic and Evolutionary Microbiol-ogy vol 53 no 5 pp 1471ndash1477 2003

[76] E P Ivanova T Sawabe K Hayashi et al ldquoShewanella fidelissp nov isolated from sediments and sea waterrdquo InternationalJournal of Systematic and Evolutionary Microbiology vol 53 no2 pp 577ndash582 2003

[77] Y Nogi C Kato andKHorikoshi ldquoTaxonomic studies of deep-sea barophilic Shewanella strains and description of Shewanellaviolacea sp novrdquo Archives of Microbiology vol 170 no 5 pp331ndash338 1998

[78] M Satomi H Oikawa and Y Yano ldquoShewanella marinintestinasp nov Shewanella schlegeliana sp nov and Shewanella sairaesp nov novel eicosapentaenic-acid-producing marine bacteriaisolated from sea-animal intestinesrdquo International Journal ofSystematic and EvolutionaryMicrobiology vol 53 no 2 pp 491ndash499 2003

[79] K Venkateswaran D P Moser M E Dollhopf et al ldquoPolypha-sic taxonomy of the genus Shewanella and description of She-wanella oneidensis sp novrdquo International Journal of SystematicBacteriology vol 49 no 2 pp 705ndash724 1999

[80] J S Zhao D Manno C Beaulieu L Paquet and JHawari ldquoShewanella sediminis sp nov a novel Na+- requir-ing and hexahydro-135-trinitro-135-triazine-degrading bac-terium frommarine sedimentrdquo International Journal of System-atic and Evolutionary Microbiology vol 55 no 4 pp 1511ndash15202005

[81] D Kim C Kang C S Lee et al ldquoTreatment failure due toemergence of resistance to carbapenem during therapy forShewanella algae bacteremiardquo Journal of Clinical Microbiologyvol 44 no 3 pp 1172ndash1174 2006

[82] Y Konishi T Tsukiyama T Tachimi N Saitoh T Nomura andS Nagamine ldquoMicrobial deposition of gold nanoparticles bythemetal-reducing bacteriumShewanella algaerdquoElectrochimicaActa vol 53 no 1 pp 186ndash192 2007

[83] F Caccavo Jr R P Blakemore and D R Lovley ldquoA hydrogen-oxidizing Fe(III)-reducing microorganism from the Great Bayestuary New Hampshirerdquo Applied and Environmental Microbi-ology vol 58 no 10 pp 3211ndash3216 1992

[84] Y Konishi T Tsukiyama K Ohno N Saitoh T Nomura and SNagamine ldquoIntracellular recovery of gold by microbial reduc-tion of AuClminus

4ions using the anaerobic bacterium Shewanella

algaerdquo Hydrometallurgy vol 81 no 1 pp 24ndash29 2006[85] L M Fernando F E Merca and E S Paterno ldquoBiogenic

synthesis of gold nanoparticles by plant-growth-promotingbacteria isolated from philippine soilsrdquo Philippine AgriculturalScientist vol 96 no 2 pp 129ndash136 2013

[86] B Arato D Schuler C Flies D Bazylinski R Frankel andP Buseck ldquoIntracellular magnetite and extracellular hematiteproduced byDesulfovibriomagneticus strainRS-1rdquoGeophysicalResearch Abstracts vol 6 2004

[87] Y Roh R J Lauf A D McMillan et al ldquoMicrobial synthesisand the characterization of metal-substituted magnetitesrdquo SolidState Communications vol 118 no 10 pp 529ndash534 2001

[88] H Lee AM PurdonV Chu andRMWestervelt ldquoControlledassembly of magnetic nanoparticles from magnetotactic bacte-ria using microelectromagnets arraysrdquo Nano Letters vol 4 no5 pp 995ndash998 2004

[89] M J Baedecker and W Back ldquoModern marine sediments asa natural analog to the chemically stressed environment of alandfillrdquo Journal of Hydrology vol 43 no 1-4 pp 393ndash414 1979

[90] D Lovley ldquoOrganicmatter mineralization with the reduction offerric ironrdquo Geomicrobiology Journal vol 5 pp 375ndash399 1987

[91] A L Graybeal and G R Heath ldquoRemobilization of transitionmetals in surficial pelagic sediments from the eastern Pacificrdquo


Geochimica et Cosmochimica Acta vol 48 no 5 pp 965ndash9751984

[92] B Bostrom M Jansson and C Forsberg ldquoPhosphorus releasefrom lake sedimentsrdquo Archiv fur HydrobiologiemdashBeiheft Ergeb-nisse der Limnologie vol 18 pp 5ndash59 1982

[93] J H P Watson D C Ellwood A K Soper and J CharnockldquoNanosized strongly-magnetic bacterially-produced iron sul-fide materialsrdquo Journal of Magnetism and Magnetic Materialsvol 203 no 1ndash3 pp 69ndash72 1999

[94] J H P Watson I W Croudace P E Warwick P A B JamesJ M Charnock and D C Ellwoods ldquoAdsorption of radioac-tive metals by strongly magnetic iron sulfide nanoparticlesproduced by sulfate-reducing bacteriardquo Separation Science andTechnology vol 36 no 12 pp 2571ndash2607 2001

[95] D R Lovley and E J P Phillips ldquoNovel mode of micro-bial energy metabolism organic carbon oxidation coupledto dissimilatory reduction of iron or manganeserdquo Applied ampEnvironmental Microbiology vol 54 no 6 pp 1472ndash1480 1988

[96] D R Lovley E J P Phillips and D J Lonergan ldquoHydrogenand formate oxidation coupled to dissimilatory reduction ofiron or manganese by Alteromonas putrefaciensrdquo Applied andEnvironmental Microbiology vol 55 no 3 pp 700ndash706 1989

[97] D R Lovley E J P Phillips D J Lonergan and P K WidmanldquoFe(III) and S0 reduction by Pelobacter carbinolicusrdquo Appliedand Environmental Microbiology vol 61 no 6 pp 2132ndash21381995

[98] M Jahn S Haderlein and R Meckenstock ldquoA novel mecha-nism of electron transfer from iron-reducing microorganismsto solid iron phasesrdquo Geophysical Research Abstracts vol 7article 01998 2005

[99] E E Roden and D R Lovley ldquoDissimilatory Fe(III) reductionby the marine microorganism Desulfuromonas acetoxidansrdquoApplied and Environmental Microbiology vol 59 no 3 pp 734ndash742 1993

[100] K Kashefi and D R Lovley ldquoReduction of Fe(III) Mn(IV) andtoxic metals at 100∘C by Pyrobaculum islandicumrdquo Applied andEnvironmental Microbiology vol 66 no 3 pp 1050ndash1056 2000

[101] T L Kieft J K Fredrickson T C Onstott et al ldquoDissimilatoryreduction of Fe(III) and other electron acceptors by a thermusisolaterdquo Applied and Environmental Microbiology vol 65 no 3pp 1214ndash1221 1999

[102] S V Liu J Zhou C Zhang D R Cole M Gajdarziska-Josifovska and T J Phelps ldquoThermophilic Fe(III)-reducingbacteria from the deep subsurface the evolutionary implica-tionsrdquo Science vol 277 no 5329 pp 1106ndash1109 1997

[103] C Zhang S Liu J Logan R Mazumder and T J PhelpsldquoEnhancement of Fe(III) Co(III) and Cr(VI) reduction at ele-vated temperatures and by a thermophilic bacteriumrdquo AppliedBiochemistry and Biotechnology A vol 57-58 pp 923ndash932 1996

[104] A Ahmad S Senapati M I Khan R Kumar and M SastryldquoExtracellular biosynthesis of monodisperse gold nanoparticlesby a novel extremophilic actinomyceteThermomonospora sprdquoLangmuir vol 19 no 8 pp 3550ndash3553 2003

[105] C Zhang H Vali C S Romaner T J Phelps and S VLiu ldquoFormation of single-domain magnetite by a thermophilicbacteriumrdquo The American Mineralogist vol 83 no 11-12 pp1409ndash1418 1998

[106] A M Laverman J S Blum J K Schaefer E J P PhillipsD R Lovley and R S Oremland ldquoGrowth of strain SES-3with arsenate and other diverse electron acceptorsrdquoApplied andEnvironmental Microbiology vol 61 no 10 pp 3556ndash3561 1995

[107] D Lovley ldquoFe (III) and Mn (IV) reductionrdquo in EnvironmentalMicrobe-Metal Interactions D Lovley Ed pp 3ndash30 ASMPressWashington DC USA 2000

[108] R Oremland ldquoBiogeochemical transformations of selenium inanoxic environmentsrdquo in Selenium in the Environment W T JFrankenberger and S Benson Eds pp 389ndash419MareelDekkerNew York NY USA 1994

[109] D L J Thorek A K Chen J Czupryna and A TsourkasldquoSuperparamagnetic iron oxide nanoparticle probes for molec-ular imagingrdquo Annals of Biomedical Engineering vol 34 no 1pp 23ndash38 2006

[110] W J Rogers and P Basu ldquoFactors regulating macrophage endo-cytosis of nanoparticles implications for targeted magneticresonance plaque imagingrdquo Atherosclerosis vol 178 no 1 pp67ndash73 2005

[111] P Moroz S K Jones and B N Gray ldquoTumor responseto arterial embolization hyperthermia and direct injectionhyperthermia in a rabbit liver tumor modelrdquo Journal of SurgicalOncology vol 80 no 3 pp 149ndash156 2002

[112] P Moroz S K Jones and B N Gray ldquoMagnetically mediatedhyperthermia current status and future directionsrdquo Interna-tional Journal of Hyperthermia vol 18 no 4 pp 267ndash284 2002

[113] L J Love J F Jansen T E McKnight et al ldquoFerrofluidfield induced flow for microfluidic applicationsrdquo IEEEASMETransactions on Mechatronics vol 10 no 1 pp 68ndash76 2005

[114] L J Love J F Jansen T E McKnight Y Roh and T J PhelpsldquoA magnetocaloric pump for microfluidic applicationsrdquo IEEETransactions on Nanobioscience vol 3 no 2 pp 101ndash110 2004

[115] J R Lloyd P Yong and L E Macaskie ldquoEnzymatic recoveryof elemental palladium by using sulfate-reducing bacteriardquoApplied and Environmental Microbiology vol 64 no 11 pp4607ndash4609 1998

[116] W de Windt P Aelterman and W Verstraete ldquoBioreductivedeposition of palladium (0) nanoparticles on Shewanella onei-densis with catalytic activity towards reductive dechlorinationof polychlorinated biphenylsrdquo Environmental Microbiology vol7 no 3 pp 314ndash325 2005

[117] P Yong N A Rowson J P G Farr I R Harris and LMacaskieldquoBioaccumulation of palladium by Desulfovibrio desulfuricansrdquoJournal of Chemical Technology and Biotechnology vol 77 pp593ndash601 2002

[118] M F Lengke M E Fleet and G Southam ldquoSynthesis of plat-inum nanoparticles by reaction of filamentous cyanobacteriawith platinum(IV)-chloride complexrdquo Langmuir vol 22 no 17pp 7318ndash7323 2006

[119] K B Narayanan andN Sakthivel ldquoBiological synthesis of metalnanoparticles by microbesrdquo Advances in Colloid and InterfaceScience vol 156 no 1-2 pp 1ndash13 2010

[120] W J Hunter and D K Manter ldquoBio-reduction of seleniteto elemental red selenium by Tetrathiobacter kashmirensisrdquoCurrent Microbiology vol 57 no 1 pp 83ndash88 2008

[121] V Yadav N Sharma R Prakash K K Raina L M Bharadwajand N T Prakash ldquoGeneration of selenium containing nano-structures by soil bacterium Pseudomonas aeruginosardquoBiotech-nology vol 7 no 2 pp 299ndash304 2008

[122] R S Oremland M J Herbel J S Blum et al ldquoStructuraland spectral features of selenium nanospheres produced by Se-respiring bacteriardquo Applied and Environmental Microbiologyvol 70 no 1 pp 52ndash60 2004

[123] S Dwivedi A A AlKhedhairy M Ahamed and J MusarratldquoBiomimetic synthesis of selenium nanospheres by bacterial


strain JS-11 and its role as a biosensor for nanotoxicity assess-ment a novel se-bioassayrdquo PLoS ONE vol 8 no 3 Article IDe57404 2013

[124] S M Baesman T D Bullen J Dewald et al ldquoFormation oftelluriumnanocrystals during anaerobic growth of bacteria thatuse Te oxyanions as respiratory electron acceptorsrdquoApplied andEnvironmental Microbiology vol 73 no 7 pp 2135ndash2143 2007

[125] B Zare M A Faramarzi Z Sepehrizadeh M Shakibaie SRezaie and A R Shahverdi ldquoBiosynthesis and recovery of rod-shaped telluriumnanoparticles and their bactericidal activitiesrdquoMaterials Research Bulletin vol 47 no 11 pp 3719ndash3725 2012

[126] C Jayaseelan A A Rahuman A V Kirthi et al ldquoNovel micro-bial route to synthesize ZnO nanoparticles using Aeromonashydrophila and their activity against pathogenic bacteria andfungirdquo Spectrochimica Acta A Molecular and BiomolecularSpectroscopy vol 90 pp 78ndash84 2012

[127] S Babitha and P S Korrapati ldquoBiosynthesis of titanium dioxidenanoparticles using a probiotic from coal fly ash effluentrdquoMaterials Research Bulletin vol 48 pp 4738ndash4742 2013

[128] A Vishnu Kirthi A Abdul Rahuman G Rajakumar et alldquoBiosynthesis of titanium dioxide nanoparticles using bac-terium Bacillus subtilisrdquoMaterials Letters vol 65 no 17-18 pp2745ndash2747 2011

[129] C T Dameron R N Reese R K Mehra et al ldquoBiosynthesisof cadmium sulphide quantum semiconductor crystallitesrdquoNature vol 338 no 6216 pp 596ndash597 1989

[130] P Williams E Keshavarz-Moore and P Dunnill ldquoProductionof cadmium sulphide microcrystallites in batch cultivation bySchizosaccharomyces pomberdquo Journal of Biotechnology vol 48no 3 pp 259ndash267 1996

[131] W C W Chan D J Maxwell X Gao R E Bailey M Han andS Nie ldquoLuminescent quantum dots for multiplexed biologicaldetection and imagingrdquo Current Opinion in Biotechnology vol13 no 1 pp 40ndash46 2002

[132] D P Barondeau and P A Lindahl ldquoMethylation of carbonmonoxide dehydrogenase from Clostridium thermoaceticumand mechanism of acetyl coenzyme A synthesisrdquo Journal of theAmerican Chemical Society vol 119 no 17 pp 3959ndash3970 1997

[133] H Bai and Z Zhang ldquoMicrobial synthesis of semiconductorlead sulfide nanoparticles using immobilized Rhodobactersphaeroidesrdquo Materials Letters vol 63 no 9-10 pp 764ndash7662009

[134] J T Beveridge M N Hughes H Lee et al ldquoMetal-microbeinteractions contemporary approachesrdquo Advances in MicrobialPhysiology vol 38 pp 178ndash243 1997

[135] D A Rouch B T O Lee and A P Morby ldquoUnderstandingcellular responses to toxic agents A model for mechanism-choice in bacterial metal resistancerdquo Journal of IndustrialMicrobiology vol 14 no 2 pp 132ndash141 1995

[136] P Mohanpuria N K Rana and S K Yadav ldquoBiosynthesis ofnanoparticles technological concepts and future applicationsrdquoJournal of Nanoparticle Research vol 10 no 3 pp 507ndash517 2008

[137] P Angell ldquoUnderstanding microbially influenced corrosionas biofilm-mediated changes in surface chemistryrdquo CurrentOpinion in Biotechnology vol 10 no 3 pp 269ndash272 1999

[138] R A Zierenberg and P Schiffman ldquoMicrobial control of silvermineralization at a sea-floor hydrothermal site on the northernGorda Ridgerdquo Nature vol 348 no 6297 pp 155ndash157 1990

[139] P I Harvey and F K Crundwell ldquoGrowth of Thiobacillusferrooxidans a novel experimental design for batch growthand bacterial leaching studiesrdquo Applied and EnvironmentalMicrobiology vol 63 no 7 pp 2586ndash2592 1997

[140] J R Stephen and S J Macnaughton ldquoDevelopments in ter-restrial bacterial remediation of metalsrdquo Current Opinion inBiotechnology vol 10 no 3 pp 230ndash233 1999

[141] S H Kang K N Bozhilov N V Myung A Mulchandani andW Chen ldquoMicrobial synthesis of CdS nanocrystals in genet-ically engineered E colirdquo Angewandte ChemiemdashInternationalEdition vol 47 no 28 pp 5186ndash5189 2008

[142] Y Chen H Tuan C Tien W Lo H Liang and Y HuldquoAugmented biosynthesis of cadmium sulfide nanoparticles bygenetically engineered Escherichia colirdquo Biotechnology Progressvol 25 no 5 pp 1260ndash1266 2009

[143] K Kalishwaralal S Gopalram R Vaidyanathan V Deepak SR K Pandian and S Gurunathan ldquoOptimization of 120572-amylaseproduction for the green synthesis of gold nanoparticlesrdquoColloids and Surfaces B Biointerfaces vol 77 no 2 pp 174ndash1802010

[144] T J Park S Y Lee N S Heo and T S Seo ldquoIn vivo synthesisof diverse metal nanoparticles by recombinant Escherichia colirdquoAngewandte ChemiemdashInternational Edition vol 49 no 39 pp7019ndash7024 2010

[145] K Deplanche I Caldelari I P Mikheenko F Sargent and LE Macaskie ldquoInvolvement of hydrogenases in the formation ofhighly catalytic Pd(0) nanoparticles by bioreduction of Pd(II)using Escherichia colimutant strainsrdquoMicrobiology vol 156 no9 pp 2630ndash2640 2010

[146] I P Mikheenko M Rousset S Dementin and L E MacaskieldquoBioaccumulation of palladium by Desulfovibrio fructosivoranswild-type and hydrogenase-deficient strainsrdquoApplied and Envi-ronmental Microbiology vol 74 no 19 pp 6144ndash6146 2008

[147] M F Lengke and G Southam ldquoThe effect of thiosulfate-oxidizing bacteria on the stability of the gold-thiosulfate com-plexrdquo Geochimica et Cosmochimica Acta vol 69 no 15 pp3759ndash3772 2005

[148] M Lengke and G Southam ldquoBioaccumulation of gold bysulfate-reducing bacteria cultured in the presence of gold(I)-thiosulfate complexrdquoGeochimica et Cosmochimica Acta vol 70no 14 pp 3646ndash3661 2006

[149] M F Lengke and G Southam ldquoThe deposition of elementalgold from gold(I)-thiosulfate complexes mediated by sulfate-reducing bacterial conditionsrdquo Economic Geology vol 102 no1 pp 109ndash126 2007

[150] C A Woolfolk and H R Whiteley ldquoReduction of inorganiccompounds with molecular hydrogen by Micrococcus lactilyti-cus I Stoichiometry with compounds of arsenic selenium tel-lurium transition and other elementsrdquo Journal of bacteriologyvol 84 pp 647ndash658 1962

[151] L J Yanke R D Bryant and E J Laishley ldquoHydrogenaseI of Clostridium pasteurianum functions as a novel selenitereductaserdquo Anaerobe vol 1 no 1 pp 61ndash67 1995

[152] C Michel M Brugna C Aubert A Bernadac andM BruschildquoEnzymatic reduction of chromate comparative studies usingsulfate-reducing bacteria key role of polyheme cytochromes candhydrogenasesrdquoAppliedMicrobiology andBiotechnology vol55 no 1 pp 95ndash100 2001

[153] O A Zadvorny N A Zorin and I N Gogotov ldquoTrans-formation of metals and metal ions by hydrogenases fromphototrophic bacteriardquo Archives of Microbiology vol 184 no 5pp 279ndash285 2006

[154] T Matsunaga and H Takeyama ldquoBiomagnetic nanoparticleformation and applicationrdquo Supramolecular Science vol 5 no3-4 pp 391ndash394 1998


[155] D Schuler ldquoFormation of magnetosomes in magnetotacticbacteriardquo Journal of Molecular Microbiology and Biotechnologyvol 1 pp 79ndash86 1999

[156] K Grunberg C Wawer B M Tebo and D Schuler ldquoA largegene cluster encoding several magnetosome proteins is con-served in different species of magnetotactic bacteriardquo Appliedand Environmental Microbiology vol 67 no 10 pp 4573ndash45822001

[157] A Arakaki H Nakazawa M Nemoto T Mori and T Mat-sunaga ldquoFormation of magnetite by bacteria and its applica-tionrdquo Journal of the Royal Society Interface vol 5 no 26 pp977ndash999 2008

[158] C Moisescu S Bonneville D Tobler I Ardelean and L GBenning ldquoControlled biomineralization of magnetite (Fe

3O4)

byMagnetospirillum gryphiswaldenserdquoMineralogical Magazinevol 72 no 1 pp 333ndash336 2008

[159] T L Riddin Y GovenderM Gericke andC GWhiteley ldquoTwodifferent hydrogenase enzymes from sulphate-reducing bacte-ria are responsible for the bioreductive mechanism of platinuminto nanoparticlesrdquo Enzyme and Microbial Technology vol 45no 4 pp 267ndash273 2009

[160] J W Moreau P K Weber M C Martin B Gilbert I DHutcheon and J F Banfield ldquoExtracellular proteins limit thedispersal of biogenic nanoparticlesrdquo Science vol 316 no 5831pp 1600ndash1603 2007

[161] Y Amemiya A Arakaki S S Staniland T Tanaka and T Mat-sunaga ldquoControlled formation of magnetite crystal by partialoxidation of ferrous hydroxide in the presence of recombinantmagnetotactic bacterial protein Mms6rdquo Biomaterials vol 28no 35 pp 5381ndash5389 2007

[162] T Prozorov S K Mallapragada B Narasimhan et al ldquoProtein-mediated synthesis of uniform superparamagnetic magnetitenanocrystalsrdquo Advanced Functional Materials vol 17 no 6 pp951ndash957 2007

[163] T Prozorov P Palo L Wang et al ldquoCobalt ferrite nanocrystalsout-performing magnetotactic bacteriardquo ACS Nano vol 1 no3 pp 228ndash233 2007


[165] S Iravani H Korbekandi S V Mirmohammadi and BZolfaghari ldquoSynthesis of silver nanoparticles chemical phys-ical and biological methodsrdquo Research in Pharmaceutical Sci-ences vol 9 pp 385ndash406 2014

[166] S S Shankar A Rai A Ahmad andM Sastry ldquoRapid synthesisof Au Ag and bimetallic Au core-Ag shell nanoparticles usingNeem (Azadirachta indica) leaf brothrdquo Journal of Colloid andInterface Science vol 275 no 2 pp 496ndash502 2004

Submit your manuscripts athttpwwwhindawicom

ScientificaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

CorrosionInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Polymer ScienceInternational Journal of



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Materials Science and EngineeringHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Smart Materials Research



MetallurgyJournal of


BioMed Research International

MaterialsJournal of


Nano

materials


Journal ofNanomaterials


bacteria used in nanoparticle biosynthesis are shownThe aimof this paper is therefore to make a reflection on the currentstate and future prospects and especially the possibilities andlimitations of the above mentioned bio-based technique forindustries

2 Bacteria in Nanoparticle Synthesis

Bacteriapossess remarkable ability to reduce heavy metalions and are one of the best candidates for nanoparticlesynthesis For instance somebacterial species have developedthe ability to resort to specific defense mechanisms to quellstresses like toxicity of heavy metal ions or metals It wasobserved that some of them could survive and grow evenat high metal ion concentrations (eg Pseudomonas stutzeriand Pseudomonas aeruginosa) [47 55] Moreover Brock andGustafson [56] reported that Thiobacillus ferrooxidans Tthiooxidans and Sulfolobus acidocaldariuswere able to reduceferric ion to the ferrous state when growing on elementalsulfur as an energy source T thiooxidans was able to reduceferric iron at low pH medium aerobically The ferrous ironformed was stable to autoxidation and T thiooxidans wasunable to oxidize ferrous iron but the bioreduction of ferriciron using T ferrooxidans was not aerobic because of therapid bacterial reoxidation of the ferrous iron in the presenceof oxygen [56] Other biomineralization phenomena suchas the formation of tellurium (Te) in Escherichia coli K12[57] the direct enzymatic reduction of Tc (VII) by restingcells of Shewanella (previouslyAlteromonas) putrefaciens andGeobactermetallireducens (previously known as strainGS-15)[58] and the reduction of selenite to selenium by Enterobac-ter cloacae Desulfovibrio desulfuricans and Rhodospirillumrubrum [26] have been reported as well Mullen et al [14]examined the ability of Bacillus cereus B subtilis E coliand P aeruginosa for removing Ag+ Cd2+ Cu2+ and La3+from solutionThey found that bacterial cells were capable ofbinding large quantities of metallic cations Moreover someof these bacteria are able to synthesize inorganicmaterials likethe magnetotactic bacteria which synthesize intracellularmagnetite NPs [53] In this section most of the bacterialspecies used in nanoparticle biosynthesis are shown (Table 1)

21 Silver NPs Saifuddin et al [22] have described a novelcombinational synthesis approach for green biosynthesis ofsilver NPs using a combination of culture supernatant ofBacillus subtilis and microwave irradiation in water Theyreported the extracellular biosynthesis of monodispersedsilver NPs (sim5ndash50 nm) using supernatants of B subtilisbut in order to increase the rate of reaction and reducethe aggregation of the produced NPs they used microwaveradiation which might provide uniform heating around theNPs and could assist the digestive ripening of particles withno aggregation [22] Kalishwaralal et al [59] reported extra-cellular synthesis of silver NPs (sim40 nm) by bioreduction ofaqueous Ag+ ions with the culture supernatant of Bacilluslicheniformis Moreover well-dispersed silver nanocrystals(sim50 nm)were synthesized usingB licheniformis [60] In caseof Bacillus flexus spherical and triangular shaped silver NPs

(sim12ndash65 nm) were successfully biosynthesized The NPs werestable in aqueous solution in five-month period of storageat room temperature in the dark These NPs showed efficacyon antibacterial property against clinically isolatedmultidrugresistant (MDR)microorganisms [61]Wei et al [62] reportedthe synthesis of circular and triangular crystalline silver NPs(sim146 nm) by solar irradiation of cell-free extracts of Bacillusamyloliquefaciens and silver nitrate (AgNO

3) Light intensity

extract concentration and NaCl addition influenced thesynthesis of silver NPs Under optimized conditions (solarintensity 70000 lx extract concentration 3mgmL andNaClcontent 2mM) 9823 plusmn 006 of the Ag+ (1mM) wasreduced to silver NPs within 80min Since heat-inactivatedextracts also mediated the formation of silver NPs enzymaticreactions are likely not involved in silver NPs formationThe produced NPs showed antimicrobial activity againstB subtilis and Escherichia coli in liquid and solid medium[62] Furthermore Bacillus cereus isolated from the Garciniaxanthochymus was used for green biosynthesis of silver NPs(sim20ndash40 nm) [18] The produced NPs showed antibacterialactivity against pathogenic bacteria like E coli Pseudomonasaeruginosa Salmonella typhi and Klebsiella pneumoniae

Pseudomonas stutzeriAG259 the silver-resistant bacterialstrain isolated from a silver mine intracellularly accumu-lated silver NPs along with some silver sulfide ranging in sizefrom 35 to 46 nm [63] Larger particles were formed whenP stutzeri AG259 challenged high concentrations of silverions during culturing resulting in intracellular formationof silver NPs ranging in size from a few nm to 200 nm[13 64] P stutzeri AG259 detoxificated silver through itsprecipitation in the periplasmic space and its bioreduction toelemental silver with a variety of crystal typologies such ashexagons and equilateral triangles as well as three differenttypes of particles elemental crystalline silver monoclinicsilver sulfide acanthite (Ag

2S) and a further undetermined

structure [64]The periplasmic space limited the thickness ofthe crystals but not their width which could be rather large(sim100ndash200 nm) [13]

Cell-free culture supernatants of five psychrophilicbacteria Phaeocystis antarctica Pseudomonas proteolyticaPseudomonas meridiana Arthrobacter kerguelensis andArthrobacter gangotriensis and two mesophilic bacteriaBacillus indicus and Bacillus cecembensis have been used tobiosynthesize silver NPs (sim6ndash13 nm) These NPs were stablefor 8 months in the dark The synthesis and stability of silverNPs appeared to depend on the temperature pH or thespecies of bacteria from which the supernatant was used Itwas observed that the A kerguelensis supernatant could notproduce silver NPs at the temperature where P antarcticacould synthesize silver NPs Therefore this study providedimportant evidence that the factors in the cell-free culturesupernatants which facilitated the synthesis of silver NPsvaried from bacterial species to species [65]

Our research group demonstrated the green biosynthesisof silver NPs using Lactobacillus casei subsp casei at roomtemperature [12] (Figure 1) Previous researchers reportedqualitative synthesis of silver NPs by Lactobacillus sp butthey did not optimize the reaction mixture The biosynthe-sized NPs were almost spherical single (sim25ndash50 nm) or in











Spherical [37]





ring) [40]






up to 200


[47]




Table 1 Continued

















2O which






4 monodis-



2as the


4


2gas



2gas however S






4



4



4


4



2O3)

2

3minus andAuCl4



Au (S2O3)

2


4






3O4) NPs













6

2minus


6


6




3



3

2minus)



3


3


3


3

2minus







2(titanium




3)2



2and H





















2O3








2 It







AuCl4

minus






4













4 Future Prospects











5 Conclusion







Acknowledgment


References











































































































































































3O4)

















CeramicsJournal of







Biomaterials




Journal of


Journal of





CoatingsJournal of

Advances in








MaterialsJournal of


Nano

materials













Spherical [37]





ring) [40]






up to 200


[47]




Table 1 Continued

















2O which






4 monodis-



2as the


4


2gas



2gas however S






4



4



4


4



2O3)

2

3minus andAuCl4



Au (S2O3)

2


4






3O4) NPs













6

2minus


6


6




3



3

2minus)



3


3


3


3

2minus







2(titanium




3)2



2and H





















2O3








2 It







AuCl4

minus






4













4 Future Prospects











5 Conclusion







Acknowledgment


References











































































































































































3O4)

















CeramicsJournal of







Biomaterials




Journal of


Journal of





CoatingsJournal of

Advances in








MaterialsJournal of


Nano

materials




Table 1 Continued

















2O which






4 monodis-



2as the


4


2gas



2gas however S






4



4



4


4



2O3)

2

3minus andAuCl4



Au (S2O3)

2


4






3O4) NPs













6

2minus


6


6




3



3

2minus)



3


3


3


3

2minus







2(titanium




3)2



2and H





















2O3








2 It







AuCl4

minus






4













4 Future Prospects











5 Conclusion







Acknowledgment


References











































































































































































3O4)

















CeramicsJournal of







Biomaterials




Journal of


Journal of





CoatingsJournal of

Advances in








MaterialsJournal of


Nano

materials






4 monodis-



2as the


4


2gas



2gas however S






4



4



4


4



2O3)

2

3minus andAuCl4



Au (S2O3)

2


4






3O4) NPs













6

2minus


6


6




3



3

2minus)



3


3


3


3

2minus







2(titanium




3)2



2and H





















2O3








2 It







AuCl4

minus






4













4 Future Prospects











5 Conclusion







Acknowledgment


References











































































































































































3O4)

















CeramicsJournal of







Biomaterials




Journal of


Journal of





CoatingsJournal of

Advances in








MaterialsJournal of


Nano

materials




Au (S2O3)

2


4






3O4) NPs













6

2minus


6


6




3



3

2minus)



3


3


3


3

2minus







2(titanium




3)2



2and H





















2O3








2 It







AuCl4

minus






4













4 Future Prospects











5 Conclusion







Acknowledgment


References











































































































































































3O4)

















CeramicsJournal of







Biomaterials




Journal of


Journal of





CoatingsJournal of

Advances in








MaterialsJournal of


Nano

materials








6

2minus


6


6




3



3

2minus)



3


3


3


3

2minus







2(titanium




3)2



2and H





















2O3








2 It







AuCl4

minus






4













4 Future Prospects











5 Conclusion







Acknowledgment


References











































































































































































3O4)

















CeramicsJournal of







Biomaterials




Journal of


Journal of





CoatingsJournal of

Advances in








MaterialsJournal of


Nano

materials







2(titanium




3)2



2and H





















2O3








2 It







AuCl4

minus






4













4 Future Prospects











5 Conclusion







Acknowledgment


References











































































































































































3O4)

















CeramicsJournal of







Biomaterials




Journal of


Journal of





CoatingsJournal of

Advances in








MaterialsJournal of


Nano

materials













2O3








2 It







AuCl4

minus






4













4 Future Prospects











5 Conclusion







Acknowledgment


References











































































































































































3O4)

















CeramicsJournal of







Biomaterials




Journal of


Journal of





CoatingsJournal of

Advances in








MaterialsJournal of


Nano

materials













4 Future Prospects











5 Conclusion







Acknowledgment


References











































































































































































3O4)

















CeramicsJournal of







Biomaterials




Journal of


Journal of





CoatingsJournal of

Advances in








MaterialsJournal of


Nano

materials










5 Conclusion







Acknowledgment


References











































































































































































3O4)

















CeramicsJournal of







Biomaterials




Journal of


Journal of





CoatingsJournal of

Advances in








MaterialsJournal of


Nano

materials







Acknowledgment


References











































































































































































3O4)

















CeramicsJournal of







Biomaterials




Journal of


Journal of





CoatingsJournal of

Advances in








MaterialsJournal of


Nano

materials

















































































































































3O4)

















CeramicsJournal of







Biomaterials




Journal of


Journal of





CoatingsJournal of

Advances in








MaterialsJournal of


Nano

materials










CeramicsJournal of







Biomaterials




Journal of


Journal of





CoatingsJournal of

Advances in








MaterialsJournal of


Nano

materials



review article bacteria in nanoparticle synthesis:...

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