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Transformation of metals and metal ions by hydrogenases from phototrophic bacteria

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Abstract

The ability of hydrogenases isolated from Thiocapsa roseopersicina and Lamprobacter modestohalophilus to reduce metal ions and oxidize metals has been studied. Hydrogenases from both phototrophic bacteria oxidized metallic Fe, Cd, Zn and Ni into their ionic forms with simultaneous evolution of molecular hydrogen. The metal oxidation rate decreased in the series Zn>Fe>Cd>Ni and depended on the pH. The presence of methyl viologen in the reaction system accelerated this process. T. roseopersicina and L. modestohalophilus cells and their hydrogenases reduced Ni(II), Pt(IV), Pd(II) or Ru(III) to their metallic forms under H2 atmosphere. These results suggest that metals or metal ions can serve as electron donors or acceptors for hydrogenases from phototrophic bacteria.

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References

  • Albracht SP (1994) Nickel hydrogenases: in search of the active site. Biochim Biophys Acta 1188:167–204

    Article  PubMed  Google Scholar 

  • Bogorov LA (1974) Properties of Thiocapsa roseopersicina BBS isolated from the estuary of White Sea. Microbiologiya 43:326–332

    CAS  Google Scholar 

  • Bryant RD, Laishley EJ (1990) The role of hydrogenase in anaerobic biocorrosion. Can J Microbiol 36:259–264

    Article  CAS  Google Scholar 

  • Bryant R, Laishley EJ (1993) The effect of inorganic phosphate and hydrogenase on the corrosion of mild steel. Appl Microbiol Biotechnol 38:824–827

    Article  CAS  Google Scholar 

  • Da Silva S, Basseguy R, Bergel A (2002) The role of hydrogenases in the anaerobic microbiologically influenced corrosion of steels. Bioelectrochemistry 56:77–79

    Article  PubMed  CAS  Google Scholar 

  • De Luca G, de Philip P, Dermoun Z, Rousset M, Vermeglio A (2001) Reduction of technetium(VII) by Desulfovibrio fructosovorans is mediated by the nickel–iron hydrogenase. Appl Environ Microbiol 67:4583–4587

    Article  PubMed  Google Scholar 

  • Dobos D (1980) Electrochemical data. A handbook for electrochemists in industry and universities. Mir, Moscow

    Google Scholar 

  • Dorohova EN, Prohorova GV (1991) Analytical chemistry. Visshaya Shkola, Moscow

    Google Scholar 

  • Eskandari H, Karkaragh GI (2003) Highly selective and simple zero and first order derivative spectrophotometric determination of palladium by using α-benzilmonoxime in Triton X-100 micellar solution. Bull Korean Chem Soc 24:1731–1736

    Article  CAS  Google Scholar 

  • Georgieva M, Andonovski B. (2003) Determination of platinum(IV) by UV spectrophotometry. Ann Bioanal Chem 375:836–839

    CAS  Google Scholar 

  • Gogotov IN, Rao KK, Hall DO (1995) Hydrogen production in systems containing metal iron and hydrogenase preparation. Prikladnaya Biokhimia Microbiologiya 31:387–392

    CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Lloyd JR (2003) Microbial reduction of metals and radionuclides. FEMS Microbiol Rev 27:411–425

    Article  PubMed  CAS  Google Scholar 

  • Lloyd JR, Macaskie LE (1996) A novel phosphorimager-based technique for monitoring the microbial reduction of technetium. Appl Environ Microbiol 65:578–582

    Google Scholar 

  • Lloyd JR, Cole JA, Macaskie LE (1997) Reduction and removal of heptavalent technetium from solution by Escherichia coli. J Bacteriol 179:2014–2021

    PubMed  CAS  Google Scholar 

  • Lloyd JR, Nolting H-F, Sole VA, Bosecker K, Macaskie LE (1998a) Technetium reduction and precipitation by sulfate reducing bacteria. Geomicrobiol J 15:43–56

    Article  Google Scholar 

  • Lloyd JR, Yong P, Macaskie LE (1998b) Enzymatic recovery of elemental palladium by using sulfate-reducing bacteria. Appl Environ Microbiol 64:4607–4609

    PubMed  CAS  Google Scholar 

  • Lloyd JR, Sole VA, Van Praagh CV, Lovley DR (2000) Direct and Fe(II)-mediated reduction of technetium by Fe(III)-reducing bacteria. Appl Environ Microbiol 66:3743–3749

    Article  PubMed  CAS  Google Scholar 

  • Lloyd JR, Mabbett AN, Williams DR, Macaskie LE (2001) Metal reduction by sulphate-reducing bacteria: physiological diversity and metal specificity. Hydrometallurgy 59:327–337

    Article  CAS  Google Scholar 

  • Lojou E, Bianco P, Bruschi M (1998) Kinetic studies on the electron transfer between bacterial c-type cytochromes and metal oxides. J Electroanal Chem 452:167–177

    Article  CAS  Google Scholar 

  • Lovley DR (1993) Dissimilatory metal reduction. Annu Rev Microbiol 47:263–290

    Article  PubMed  CAS  Google Scholar 

  • Lovley DR, Phillips EJP (1994) Reduction of chromate by Desulfovibrio vulgaris and its c3 cytochrome. Appl Environ Microbiol 60:726–728

    PubMed  CAS  Google Scholar 

  • Lovley DR, Widman PK, Woodward JC, Phillips EJ (1993) Reduction of uranium by cytochrome c3 of Desulfovibrio vulgaris. Appl Environ Microbiol 59:3572–3576

    PubMed  CAS  Google Scholar 

  • Michel C, Brugna M, Aubert C, Bernadac A, Bruschi M (2001) Enzymatic reduction of chromate: comparative studies using sulfate-reducing bacteria. Key role of polyheme cytochromes c and hydrogenases. Appl Microbiol Biotechnol 55:95–100

    Article  PubMed  CAS  Google Scholar 

  • Moore MD, Kaplan S (1994) Members of the family Rhodospirillaceae reduce heavy-metal oxyanions to maintain redox poise during photosynthetic growth. ASM News 60:17–23

    Google Scholar 

  • Nedoluzhko AI, Shumilin IA, Mazhorova LE, Popov VO, Nikandrov VV (2000) Enzymatic oxidation of cadmium and lead metals photodeposited on cadmium sulfide. Bioelectrochemistry 53:61–71

    Article  Google Scholar 

  • Payne RB, Gentry DM, Rapp-Giles BJ, Casalot L, Wall JD (2002) Uranium reduction by Desulfovibrio desulfuricans strain G20 and a cytochrome c3 mutant. Appl Environ Microbiol 68:3129–3132

    Article  PubMed  CAS  Google Scholar 

  • Peters JW, Lanzilotta WN, Lemon BJ, Seefeldt LC (1998) X-ray crystal structure of the Fe-only hydrogenase (CpI) from Clostridium pasteurianum to 1.8 angstrom resolution. Science 282:1853–1858

    Article  PubMed  CAS  Google Scholar 

  • Prokhorov AM (1992) Physical encyclopedia. Bolshaya Rossiyskaya Enciklopedia, Moscow

    Google Scholar 

  • Pumpel T, Macaskie LE, Finlay JA, Diels L, Tsezos M (2003) Nickel removal from nickel plating waste water using a biologically active moving-bed sand filter. Biometals 16:567–581

    Article  PubMed  Google Scholar 

  • Serebryakova LT, Zorin NA, Karpilova IF, Gogotov IN (1997) Temperature dependence of anaerobic oxidation of metals by bacterial hydrogenases. Prikladnaya Biokhimiya Microbiologiya 33:317–320

    CAS  Google Scholar 

  • Sherman MB, Orlova EV, Smirnova EA, Hovmoller S, Zorin NA (1991) Three-dimensional structure of the nickel-containing hydrogenase from Thiocapsa roseopersicina. J Bacteriol 173:2576–2580

    PubMed  CAS  Google Scholar 

  • Vignais PM, Billoud B, Meyer J (2001) Classification and phylogeny of hydrogenases. FEMS Microbiol Rev 25:455–501

    Article  PubMed  CAS  Google Scholar 

  • Williams JW, Silver S (1984) Bacterial resistance and detoxification of heavy metals. Enzyme Microb Technol 6:530–537

    Article  CAS  Google Scholar 

  • Woolfolk CA, Whiteley HR (1962) Reduction of inorganic compounds with molecular hydrogen by Micrococcus lactilyticus. I. Stoichiometry with compounds of arsenic, selenium, tellurium, transition and other elements. J Bacteriol 84:647–658

    PubMed  CAS  Google Scholar 

  • Zadvorny OA, Zorin NA, Gogotov IN (2000) Influence of metal ions on hydrogenase from the purple sulfur bacterium Thiocapsa roseopersicina. Biochemistry (Mosc) 65:1287–1291

    CAS  Google Scholar 

  • Zadvorny OA, Zorin NA, Gogotov IN, Gorlenko VM (2004) Properties of stable hydrogenase from the purple sulfur bacterium Lamprobacter modestohalophilus. Biochemistry (Mosc) 69:164–169

    Article  CAS  Google Scholar 

  • Zorin NA (1986) Redox properties and active center of phototrophic bacteria hydrogenases. Biochimie 68:97–101

    Article  PubMed  CAS  Google Scholar 

  • Zorin NA, Lindblad P (1993) Localization of hydrogenase in the purple sulphur bacterium Thiocapsa roseopersicina. Arch Microbiol 160:1–5

    Article  PubMed  Google Scholar 

  • Zorin NA, Dimon B, Gagnon J, Gaillard J, Carrier P, Vignais PM (1996) Inhibition by iodoacetamide and acetylene of the H-D-exchange reaction catalyzed by Thiocapsa roseopersicina hydrogenase. Eur J Biochem 241:675–681

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

We thank Dr. N.E. Suzina and T.N. Abashina for help with electron microscopy. We gratefully acknowledge the participation of prof. P.M. Vignais and prof. J.W. Peters in the critical reading of the manuscript and helpful discussion.

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Authors and Affiliations

  1. Institute of Basic Biological Problems of RAS, 142290, Pushchino, Russia

    Oleg A. Zadvorny, Nikolay A. Zorin & Ivan N. Gogotov

  2. Chemistry and Biochemistry Department, Montana State University, 108 Gains Hall, Bozeman, MT, 59717, USA

    Oleg A. Zadvorny

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  1. Oleg A. Zadvorny
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  2. Nikolay A. Zorin
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  3. Ivan N. Gogotov
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Zadvorny, O.A., Zorin, N.A. & Gogotov, I.N. Transformation of metals and metal ions by hydrogenases from phototrophic bacteria. Arch Microbiol 184, 279–285 (2006). https://doi.org/10.1007/s00203-005-0040-1

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  • DOI: https://doi.org/10.1007/s00203-005-0040-1

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