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Cr(VI) detoxification by Desulfovibrio vulgaris strain Hildenborough: microbe–metal interactions studies

  • Applied Microbial and Cell Physiology
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Abstract

Toxic heavy metals constitute a worldwide environmental pollution problem. Bioremediation technologies represent efficient alternatives to the classic cleaning-up of contaminated soil and ground water. Most toxic heavy metals such as chromium are less soluble and toxic when reduced than when oxidized. Sulfate-reducing bacteria (SRB) are able to reduce heavy metals by a chemical reduction via the production of H2S and by a direct enzymatic process involving hydrogenases and c3 cytochromes. We have previously reported the effects of chromate [Cr(VI)] on SRB bioenergetic metabolism and the molecular mechanism of the metal reduction by polyhemic cytochromes. In the current work, we pinpoint the bacteria–metal interactions using Desulfovibrio vulgaris strain Hildenborough as a model. The bacteria were grown in the presence of high Cr(VI) concentration, where they accumulated precipitates of a reduced form of chromium, trivalent chromium [Cr(III)], on their cell surfaces. Moreover, the inner and outer membranes exhibited precipitates that shared the spectroscopic signature of trivalent chromium. This subcellular localization is consistent with enzymatic metal reduction by cytochromes and hydrogenases. Regarding environmental significance, our findings point out the Cr(VI) immobilization mechanisms of SRB; suggesting that SRB are highly important in metal biogeochemistry.

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References

  • Assfalg M, Bertini I, Bruschi M, Michel C, Turano P (2002) The metal reductase activity of some multiheme cytochromes c: NMR structural characterization of the reduction of chromium(VI) to chromium(III) by cytochrome c7. Proc Natl Acad Sci USA 99:9750–9754

    Article  CAS  Google Scholar 

  • Beveridge TJ, Meloche JD, Fyfe WS, Murray GE (1983) Diagenesis of metals chemically complexed to bacteria: laboratory formation of metal phosphates, sulfides, and organic condensates in artificial sediments. Appl Environ Microbiol 45:1094–1108

    Article  CAS  Google Scholar 

  • Brugna M, Giudici-Orticoni MT, Spinelli S, Brown K, Tegoni M, Bruschi M (1998) Kinetics and interaction studies between cytochrome c3 and Fe-only hydrogenase from Desulfovibrio vulgaris Hildenborough. Proteins 33:590–600

    Article  CAS  Google Scholar 

  • Chardin B, Dolla A, Chaspoul F, Fardeau ML, Gallice P, Bruschi M (2002) Bioremediation of chromate: thermodynamic analysis of the effects of Cr(VI) on sulfate-reducing bacteria. Appl Microbiol Biotechnol 60:352–360

    Article  CAS  Google Scholar 

  • Chardin B, Giudici-Orticoni MT, De Luca G, Guigliarelli B, Bruschi M (2003) Hydrogenases in sulfate-reducing bacteria function as chromium reductase. Appl Microbiol Biotechnol 63:315–321

    Article  CAS  Google Scholar 

  • Cotter-Howells J (1996) Lead phosphate formation in soils. Environ Pollut 93:9–16

    Article  CAS  Google Scholar 

  • Daulton TL, Little BJ, Lowe K, Jones-Meehan J (2002) EELS techniques for the study of microbial chromium(VI) reduction. J Microbiol Methods 50:39–54

    Article  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  Google Scholar 

  • Enterline PE (1974) Respiratory cancer among chromate workers. J Occup Med 16:523–526

    PubMed  CAS  Google Scholar 

  • Kucheyev SO, Borstedt C, Van Buuren T, Willey TM, Land TA, Terminello LJ, Felter TE, Hamza AV, Demos SG, Nelson AJ (2004) Electronic structure of KD2(1−x)H2(1−x)PO4 studied by soft X-ray absorption and emission spectroscopies. Phys Rev B 70:245106–245116

    Article  CAS  Google Scholar 

  • Levinson HS, Mahler I (1998) Phosphatase activity and lead resistance in Citrobacterfreundii and Staphylococcus aureus. FEMS Microbiol Lett 161:135–138

    Article  Google Scholar 

  • Lloyd JR, Nolting HF, Solé VA, Bosecker K, Macaskie LE (1998a) Technicium reduction and precipitation by sulfate reducing bacteria. Geomicrobiol J 15:45–58

    Article  CAS  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

    Article  CAS  Google Scholar 

  • Lloyd JR, Ridley J, Khizniak T, Lyalikova NN, Macaskie LE (1999) Reduction of technetium by Desulfovibrio desulfuricans: biocatalyst characterization and use in a flowthrough bioreactor. Appl Environ Microbiol 65:2691–2696

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Lojou E, Bianco P, Bruschi M (1998b) Kinetic studies on the electron transfer between various c-type cytochromes and iron (III) using a voltametric approach. Electrochim Acta 43:2005–2013

    Article  CAS  Google Scholar 

  • Lovley DR, Phillips EJP (1992) Reduction of uranium by Desulfovibriodesulfuricans. Appl Environ Microbiol 58:850–856

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Lovley DR, Giovannoni SJ, White DC, Champine JE, Phillips EJ, Gorby YA, Goodwin S (1993a) Geobactermetallireducens gen. nov. sp. nov., a microorganism capable of coupling the complete oxidation of organic compounds to the reduction of iron and other metals. Arch Microbiol 159:336–344

    Article  Google Scholar 

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

    Article  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  CAS  Google Scholar 

  • Michel C, Giudici-Orticono MT, Baymann F, Bruschi M (2003) Bioremediation of chromate by sulfate-reducing bacteria cytochromes c3 and hydrogenases. Water, Air and Soil Pollution: Focus 3:161–169

    Article  CAS  Google Scholar 

  • O’Brien GW, Harris JR, Milnes AR, Veeh HH (1981) Bacterial origin of east Australian continental margin phosphorites. Nature 294:442–444

    Article  Google Scholar 

  • Ohtake H, Cervantes C, Silver S (1987) Decreased chromate uptake in Pseudomonas fluorescens carrying a chromate resistance plasmid. J Bacteriol 169:3853–3856

    Article  CAS  Google Scholar 

  • Renninger N, McMahon KD, Knopp R, Nitsche H, Clark DS, Keasling JD (2001) Uranyl precipitation by biomass from an enhanced biological phosphorus removal reactor. Biodegradation 12:401–410

    Article  CAS  Google Scholar 

  • Roden EC, Lovley DR (1993) Dissimilatory Fe(III) reduction by the marine microorganism Desulfuromonas acetoxidans. Appl Environ Microbiol 59:734–742

    Article  CAS  Google Scholar 

  • Smith AD, Schofield PF, Scholl A, Pattrick RAD, Bridges JC (2003) XPEEM valence state imaging of mineral micro-intergrowths with a spatial resolution of 100 nm. J Phys, IV 104:373–376

    CAS  Google Scholar 

  • Southam G (2000) Bacterial surface-mediated mineral formation. In: Lovley DR (ed) Environmental microbe–metal interactions. ASM, Washington DC, pp 257–275

    Google Scholar 

  • Sutherland DGJ, Kasrai M, Bancroft GM, Liu ZF, Tan KH (1993) Si–L and K edge X-ray absorption near-edge spectroscopy of gas-phase Si(CH3)x(OCH3)4−x: models for solid state storage. Phys Rev B 48:14989–15001

    Article  CAS  Google Scholar 

  • Starkey RL (1938) A study of spore formation and other morphological characteristics of Vibriodesulfuricans. Arch Microbiol 8:268–304

    Google Scholar 

  • Templeton AS, Trainor TP, Spormann AM, Newville M, Sutton SR, Dohnalkova A, Gorby Y, Brown GE Jr (2003) Sorption versus biomineralization of Pb(II) with Burkholderia cepacia biofilms. Environ Sci Technol 37:300–307

    Article  CAS  Google Scholar 

  • Toulemonde O, Studer F, Banrabe A, Raveau B, Goedkoop JB (2000) Chromium doped manganite: evidence for electronically phase separated systems. Eur Phys J, B Cond Matter Phys 18:233–240

    CAS  Google Scholar 

  • Van Veen HW, Abee T, Kortstee GJ, Pereira H, Konings WN, Zehnder AJ (1994) Generation of a proton motive force by the excretion of metal-phosphate in the polyphosphate-accumulating Acinetobacter johnsonii strain 210A. J Biol Chem 269:29509–29510

    PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by CNRS interdisciplinarity Geomicrobiology Program. We are very grateful to Alain Bernadac and Marielle Bauzan who performed transmission electron microscopy and microorganism cultures, respectively, at the IBSM Institute, CNRS, Marseille, France.

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Authors and Affiliations

  1. Institut de Biologie Structurale et Microbiologie, Unité de Bioénergétique et Ingénierie des Protéines, Centre National de la Recherche Scientifique, 31 chemin Joseph Aiguier, 13402, Marseille cedex 20, France

    Florence Goulhen & Mireille Bruschi

  2. Laboratoire de physique des solides, CNRS-UMR 8502, Université Paris sud, Bat. 510, 91405, Orsay cedex, France

    Alexandre Gloter

  3. Département de Minéralogie, IMPMC et IPGP, CNRS UMR 7590, 140 rue de Lourmel, 75015, Paris, France

    Francois Guyot

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  1. Florence Goulhen
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  2. Alexandre Gloter
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  3. Francois Guyot
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  4. Mireille Bruschi
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Correspondence to Mireille Bruschi.

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Goulhen, F., Gloter, A., Guyot, F. et al. Cr(VI) detoxification by Desulfovibrio vulgaris strain Hildenborough: microbe–metal interactions studies. Appl Microbiol Biotechnol 71, 892–897 (2006). https://doi.org/10.1007/s00253-005-0211-7

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  • DOI: https://doi.org/10.1007/s00253-005-0211-7

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