Biofabrication of gold nanoparticles by Shewanella species

Abstract

Background

Shewanella oneidensis MR-1 (MR-1) and Shewanella xiamenensis BC01 (SXM) are facultative anaerobic bacteria that exhibit outstanding performance in the dissimilatory reduction of metal ions. Shewanella species have been reported to produce metal nanoparticles, but the mechanism and optimization are still not extensively studied and clearly understood. Herein, the effects of pH, biomass, gold ion concentration, and photoinduction are evaluated to optimize gold nanoparticle (Au@NP) production by Shewanella.

Results

The highest amount of Au@NPs produced by SXM and MR-1 were 108 and 62 ppm, respectively, at pH 5 when 2.4 g/L biomass was immersed in 300 ppm gold ions and 50 mM lactate under a light intensity of 100 µmol/m²/s. By scanning election microscopy and zeta potential analysis, the proposed mechanism of Au@NP formation was that Shewanella used lactate as electron donors for the Mtr pathway, stimulated by photosensitive proteins resulting in the nucleation of NPs on the cell membrane. Besides, the resting cells retained the ability for biofabrication of nanoparticles for nearly 25 days.

Conclusions

The optimal conditions evaluated for Au@NPs production by Shewanella were biomass, pH, ions concentration, and photoinduction. To the best of our knowledge, this is the first attempt to explore a two-step mechanism for Au@NPs formation in Shewanella. First, the HAuCl₄ solution reacted with sodium lactate to form metallic gold ions. Second, the metallic gold ions were adsorbed onto the outer membrane of cell, and the formation of Au@NPs at the surface was triggered. Shewanella-based Au@NPs production could be a potential ecofriendly solution for the recovery of Au ions from secondary resources like industrial waste.

Keywords

Shewanella / Gold nanoparticle / Resting cell / Optimization / Photoinduction

References

[1] Bai H, Zhang Z, Guo Y, Jia W. Biological synthesis of size-controlled cadmium sulfide nanoparticles using immobilized Rhodobacter sphaeroides. Nanoscale Res Lett, 2009, 4(7): 717-723.

[2] Binupriya A, Sathishkumar M, Vijayaraghavan K, Yun SI. Bioreduction of trivalent aurum to nano-crystalline gold particles by active and inactive cells and cell-free extract of Aspergillus oryzae var. viridis. J Hazard Mater, 2010, 177(1): 539-545.

[3] Chen T, Zhou Y, Ng IS, Yang CS, Wang HY. Formation and characterization of extracellular polymeric substance from Shewanella xiamenensis BC01 under calcium stimulation. J Taiwan Inst Chem Eng, 2015, 57: 175-181.

[4] Coursolle D, Gralnick JA. Modularity of the Mtr respiratory pathway of Shewanella ondeidensis strain MR-1. Mol Microbiol, 2010, 77(4): 995-1008.

[5] Dodson JR, Parker HL, Muñoz García A, Hicken A, Asemave K, Farmer TJ, He H, Clark JH, Hunt AJ. Bio-derived materials as a green route for precious & critical metal recovery and re-use. Green Chem, 2015, 17(4): 1951-1965.

[6] Farooq U, Kozinski JA, Khan MA, Athar M. Biosorption of heavy metal ions using wheat based biosorbents—a review of the recent literature. Bioresour Technol, 2010, 101(14): 5043-5053.

[7] Fredrickson JK, Romine MF, Beliaev AS, Auchtung JM, Driscoll ME, Gardner TS, Nealson KH, Osterman AL, Pinchuk G, Reed JL, Rodionov DA, Rodrigues JLM, Saffarini DA, Serres MH, Spormann AM, Zhulin IB, Tiedje JM. Towards environmental systems biology of Shewanella. Nat Rev Microbiol, 2008, 6(8): 592-603.

[8] He YR, Cheng YY, Wang WK, Yu HQ. A green approach to recover Au(III) in aqueous solution using biologically assembled rGO hydrogels. Chem Eng J, 2015, 270: 476-484.

[9] Huang J, Sun B, Zhang X. Shewanella xiamenensis sp. nov., isolated from coastal sea sediment. Int J Syst Evol Microbiol, 2010, 60(7): 1585-1589.

[10] Ishiki K, Okada K, Le DQ, Shiigi H, Nagaoka T. Investigation concerning the formation process of gold nanoparticles by Shewanella oneidensis MR-1. Anal Sci, 2017, 33(2): 129-131.

[11] Kashefi K, Tor JM, Nevin KP, Lovley DR. Reductive precipitation of gold by dissimilatory Fe(III)-reducing bacteria and archaea. Appl Environ Microbiol, 2001, 67(7): 3275-3279.

[12] Klaus T, Joerger R, Olsson E, Granqvist CG. Bacteria as workers in the living factory: metal-accumulating bacteria and their potential for materials science. Trends Biotechnol, 2001, 19(1): 15-20.

[13] Konishi Y, Ohno K, Saitoh N, Nomura T, Nagamine S, Hishida H, Takahashi Y, Uruga T. Bioreductive deposition of platinum nanoparticles on the bacterium Shewanella algae. J Biotechnol, 2007, 128(3): 648-653.

[14] Kumar SA, Peter YA, Nadeau JL. Facile biosynthesis, separation and conjugation of gold nanoparticles to doxorubicin. Nanotechnology, 2008, 19(49): 495101.

[15] Levskaya A, Chevalier AA, Tabor JJ, Simpson ZB, Lavery LA, Levy M, Davidson EA, Scouras A, Ellington AD, Marcotte EM, Voigt CA. Synthetic biology: engineering Escherichia coli to see light. Nature, 2005, 438(7067): 441-442.

[16] Liu H, Logan BE. Electricity generation using an air-cathode single chamber microbial fuel cell in the presence and absence of a proton exchange membrane. Environ Sci Technol, 2004, 38(14): 4040-4046.

[17] Liu DF, Min D, Cheng L, Zhang F, Li DB, Xiao X, Sheng GP, Yu HQ. Anaerobic reduction of 2,6-dinitrotoluene by Shewanella oneidensis MR-1: roles of Mtr respiratory pathway and NfnB. Biotechnol Bioeng, 2017, 114(4): 761-768.

[18] Lo YC, Cheng CL, Han YL, Chen BY, Chang JS. Recovery of high-value metals from geothermal sites by biosorption and bioaccumulation. Bioresour Technol, 2014, 160: 182-190.

[19] Mata YN, Torres E, Blazquez ML, Ballester A, Gonzalez F, Munoz JA. Gold(III) biosorption and bioreduction with the brown alga Fucus vesiculosus. J Hazard Mater, 2009, 166(2–3): 612-618.

[20] Mishra A, Tripathy SK, Yun SI. Fungus mediated synthesis of gold nanoparticles and their conjugation with genomic DNA isolated from Escherichia coli and Staphylococcus aureus. Process Biochem, 2012, 47(5): 701-711.

[21] Mishra A, Kumari M, Pandey S, Chaudhry V, Gupta KC, Nautiyal CS. Biocatalytic and antimicrobial activities of gold nanoparticles synthesized by Trichoderma sp. Bioresour Technol, 2014, 166: 235-242.

[22] Myers CR, Nealson KH. Bacterial manganese reduction and growth with manganese oxide as the sole electron acceptor. Science, 1988, 240(4857): 1319.

[23] Narayanan KB, Sakthivel N. Biological synthesis of metal nanoparticles by microbes. Adv Colloid Interface Sci, 2010, 156(1): 1-13.

[24] Ng WO, Zentella R, Wang Y, Taylor AJS, Pakrasi BH. PhrA, the major photoreactivating factor in the cyanobacterium Synechocystis sp. strain PCC 6803 codes for a cyclobutane-pyrimidine-dimer-specific DNA photolyase. Arch Microbiol, 2000, 173: 412-417.

[25] Ng CK, Sivakumar K, Liu X, Madhaiyan M, Ji L, Yang L, Tang C, Song H, Kjelleberg S, Cao B. Influence of outer membrane c-type cytochromes on particle size and activity of extracellular nanoparticles produced by Shewanella oneidensis. Biotechnol Bioeng, 2013, 110(7): 1831-1837.

[26] Ng IS, Xu F, Zhang X, Ye C. Enzymatic exploration of catalase from a nanoparticle producing and biodecolorizing algae Shewanella xiamenensis BC01. Bioresour Technol, 2015, 184: 429-435.

[27] Ng IS, Ndive CI, Zhou Y, Wu X. Cultural optimization and metal effects of Shewanella xiamenensis BC01 growth and swarming motility. Bioresour Bioprocess, 2015, 2(1): 28.

[28] Ramesh A, Hasegawa H, Sugimoto W, Maki T, Ueda K. Adsorption of gold(III), platinum(IV) and palladium(II) onto glycine modified crosslinked chitosan resin. Bioresour Technol, 2008, 99(9): 3801-3809.

[29] Sancar A. Structure and function of DNA photolyase and cryptochrome blue-light photoreceptors. Chem Rev, 2003, 103: 2203-2237.

[30] Sathishkumar M, Sneha K, Yun YS. Immobilization of silver nanoparticles synthesized using Curcuma longa tuber powder and extract on cotton cloth for bactericidal activity. Bioresour Technol, 2010, 101(20): 7958-7965.

[31] Sathishkumar M, Mahadevan A, Vijayaraghavan K, Pavagadhi S, Balasubramanian R. Green recovery of gold through biosorption, biocrystallization, and pyro-crystallization. Ind Eng Chem Res, 2010, 49(16): 7129-7135.

[32] Schmitz O, Katayama M, Williams BS, Kondo T, Golden SS. CikA, a bacteriophytochrome that resets the cyanobacterial circadian clock. Science, 2000, 289: 765-768.

[33] Shedbalkar U, Singh R, Wadhwani S, Gaidhani S, Chopade BA. Microbial synthesis of gold nanoparticles: current status and future prospects. Adv Colloid Interface Sci, 2014, 209: 40-48.

[34] Shi L, Rosso KM, Clarke TA, Richardson DJ, Zachara JM, Fredrickson JK. Molecular underpinnings of Fe(III) oxide reduction by Shewanella oneidensis MR-1. Front Microbiol, 2012, 3: 50.

[35] Spitzer M, Bertazzoli R. Selective electrochemical recovery of gold and silver from cyanide aqueous effluents using titanium and vitreous carbon cathodes. Hydrometallurgy, 2004, 74(3): 233-242.

[36] Suresh AK, Pelletier DA, Wang W, Broich ML, Moon JW, Gu B, Allison DP, Joy DC, Phelps TJ, Doktycz MJ. Biofabrication of discrete spherical gold nanoparticles using the metal-reducing bacterium Shewanella oneidensis. Acta Biomater, 2011, 7(5): 2148-2152.

[37] Tan SI, Ng IS, Yu YY. Heterologous expression of an acidophilic multicopper oxidase in Escherichia coli and its applications in biorecovery of gold. Bioresour Bioprocess, 2017, 4: 20.

[38] Wang G, Zhang B, Li S, Yang M, Yin C. Simultaneous microbial reduction of vanadium(V) and chromium(VI) by Shewanella loihica PV-4. Bioresour Technol, 2017, 227: 353-358.

[39] Wu C, Cheng YY, Li BB, Li WW, Li DB, Yu HQ. Electron acceptor dependence of electron shuttle secretion and extracellular electron transfer by Shewanella oneidensis MR-1. Bioresour Technol, 2013, 136: 711-714.

[40] Wu R, Cui L, Chen L, Wang C, Cao C, Sheng G, Yu H, Zhao F. Effects of bio-Au nanoparticles on electrochemical activity of Shewanella oneidensis wild type and ∆omcA/mtrC mutant. Sci Rep, 2013, 3: 3307.

[41] Xu M, Guo J, Zeng G, Zhong X, Sun G. Decolorization of anthraquinone dye by Shewanella decolorationis S12. Appl Microbiol Biotechnol, 2006, 71(2): 246-251.

[42] Yeh KC, Wu SH, Murphy JT, Lagarias JC. A cyanobacterial phytochrome two-component light sensory system. Science, 1997, 277: 1505-1508.

[43] Zhu N, Cao Y, Shi C, Wu P, Ma H. Biorecovery of gold as nanoparticles and its catalytic activities for p-nitrophenol degradation. Environ Sci Pollut Res Int, 2016, 23(8): 7627-7638.

Funding

Ministry of Science and Technology, Taiwan(105-2221-E-006-225-MY3)