Skip to main content Accessibility help

We use cookies to distinguish you from other users and to provide you with a better experience on our websites. Close this message to accept cookies or find out how to manage your cookie settings.

Close cookie message
×
Hostname: page-component-cd9895bd7-p9bg8 Total loading time: 0 Render date: 2024-12-22T02:32:50.217Z Has data issue: false hasContentIssue false

15 - Enzymatic and genomic studies on the reduction of mercury and selected metallic oxyanions by sulphate-reducing bacteria

Published online by Cambridge University Press:  22 August 2009

By
Mireille Bruschi ,
Larry L. Barton ,
Florence Goulhen  and
Richard M. Plunkett
Edited by
Larry L. Barton  and
W. Allan Hamilton
Larry L. Barton
Affiliation:
University of New Mexico
W. Allan Hamilton
Affiliation:
University of Aberdeen
Get access

Summary

INTRODUCTION

Toxic heavy metals and metalloids constitute an international pollution problem that not only impacts public health but also is of environmental and economic importance. Prokaryotes with the physiological activity of sulphate reduction are found in a number of environmental sites containing toxic metals and these microorganisms have developed several different strategies for resistance to toxic elements. Some bacteria have developed detoxification strategies that are potentially useful for bioremediation. Since sulphate-reducing bacteria (SRB) are found in a large number of contaminated sites containing toxic metals, it is apparent that these organisms have a functional defence system that enables them to persist and even grow under metal stress. The enzymatic metal reduction by SRB offers an alternative to chemical processes to remediate environments containing redox-active toxic metals and metalloids. While Hockin and Gadd discuss in Chapter 14 the bioremediation activities of sulphate-reducing bacteria, this chapter focuses on the enzymatic processes associated with metal reduction. We review results obtained with isolated proteins and discuss the potential of sulphate-reducers by reviewing putative proteins found in their genomes. Reference is made to putative genes present in Desulfovibrio (D.) vulgaris strain Hildenborough (Heidelberg et al., 2004), D. desulfuricans strain G20 (http://www.jgi.doe.gov), Desulfotalea (Des.) psychrophila (Rabus et al., 2004) and Archaeoglobus (A.) fulgidus (Klenk et al., 1997).

ENZYMATIC ACTIVITIES INVOLVING REDOX-ACTIVE ELEMENTS

The detoxification of an environment arising from SRB reductions is considered by many as an important event for bioremediation of various polluted environments In addition to precipitation of metals by biogenic hydrogen sulfide, the SRB are highly capable of reducing many soluble redox-active elements.

Type
Chapter
Information
Sulphate-Reducing Bacteria
Environmental and Engineered Systems
 , pp. 435 - 458
Publisher: Cambridge University Press
Print publication year: 2007

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abdelous, A., Gong, W. L., Lutze, W.et al. (2000). Using cytochrome c3 to make selenium wires. Chem Mat, 12, 1510–12CrossRefGoogle Scholar
Assfalg, M., Bertini, I., Bruschi, M., Michel, C. and 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, 9750–4CrossRefGoogle Scholar
Aubert, C., Lojou, E., Bianco, P.et al. (1998). The Desulfuromonas acetoxidans triheme cytochrome c7 produced in Desulfovibrio desulfuricans retains its metal reductase activity. Environ Microbiol, 64, 1308–12Google ScholarPubMed
Barkay, T. and Smets, B. F. (2005). Horizontal gene flow in microbial communities. ASM News, 71, 412–19Google Scholar
Bruschi, M., Bertrand, P., More, C.et al. (1992). Biochemical and spectroscopic characterization of the high molecular weight cytochrome c from Desulfovibrio vulgaris Hildenborough expressed in Desulfovibrio desulfuricans G200. Biochem, 31, 3281–8CrossRefGoogle ScholarPubMed
Bruschi, M. (1994). Cytochrome c3 (Mr26000) isolated from sulphate-reducing bacteria and its relationships to other polyhemic cytochromes from Desulfovibrio. Meth Enzymol, 243, 140–55CrossRefGoogle Scholar
Bruschi, M., Leroy, G., Guerlesquin, F. and Bonicel, J. (1994). Amino-acid sequence of the cytochrome c3 (M(r) 26,000) from Desulfovibrio desulfuricans Norway and a comparison with those of the other polyhemic cytochromes from Desulfovibrio. Biochim Biophys Acta, 1205, 123–31CrossRefGoogle Scholar
Barton, L. L., Plunkett, R. M. and Thomson, B. M. (2003). Reduction of metals and nonessential elements by anaerobes. In Ljungdahl, L. G., Adams, M. W., Barton, L. L., Ferry, J. G. and Johnson, M. K. (eds.), Biochemistry and Physiology of Anaerobic Bacteria. New York: Springer-Verlag. pp. 220–34.CrossRefGoogle Scholar
Chang, Y. J., Peacock, A. D., Long, P. E.et al. (2001). Diversity and characterization of sulphate-reducing bacteria in groundwater at a uranium mill tailing site. Appl Environ Microbiol, 67, 3149–60CrossRefGoogle Scholar
Chardin, B., Dolla, A., Chaspoul, F.et al. (2002). Bioremediation of chromate: thermodynamic analysis of the effects of Cr(VI) on sulphate-reducing bacteria. Appl Microbiol Biotechnol, 60, 352–60Google Scholar
Chardin, B., Giudici-Orticoni, M. T., Luca, G., Guigliarelli, B. and Bruschi, M. (2003). Hydrogenases in sulphate-reducing bacteria function as chromium reductase. Appl Microbiol Biotechnol, 63, 315–21CrossRefGoogle Scholar
Choi, S. C., Chase, T. Jr. and Bartha, R. (1994). Enzymatic catalysis of mercury methylation by Desulfovibrio desulfuricans LS. Appl Environ Microbiol, 60, 1342–6Google ScholarPubMed
Czjzek, M., Guerlesquin, F., Bruschi, M. and Haser, R. (1996). Crystal structure of a dimeric octaheme cytochrome c3 (M(r) 26,000) from Desulfovibrio desulfuricans Norway. Structure, 4, 395–404CrossRefGoogle ScholarPubMed
Czjzek, M., ElAntak, L., Zamboni, V.et al. (2002). The crystal structure of the hexadeca-heme cytochrome Hmc and a structural model of its complex with cytochrome c3. Structure, 10, 1677–86CrossRefGoogle Scholar
Luca, G., Philip, P., Dermoun, Z., Rousset, M. and Vermeglio, A. (2001). Reduction of technetium (VII) by Desulfovibrio fructosovorans is mediated by the nickel-iron hydrogenase. Appl Environ Microbiol, 67, 4583–7CrossRefGoogle ScholarPubMed
Fauque, G. D. (1994). Sulfur reductase form thiophilic sulphate-reducing bacteria. Meth Enzymol, 243, 353–67CrossRefGoogle Scholar
Fauque, G., Herve, D. and LeGall, J. (1979). Structure–function relationship in hemoproteins: The role of cytochrome c3 in the reduction of colloidal sulfur by sulphate-reducing bacteria. Arch Microbiol, 121, 261–4CrossRefGoogle Scholar
Fauque, G., Peck, H. D. Jr., Moura, J. J. G.et al. (1988). The three classes of hydrogenases from sulphate-reducing bacteria of the genus Desulfovibrio. FEMS Microbiol Rev, 54, 299–344CrossRefGoogle Scholar
Gilmore, C. C., Henry, E. A. and Mitchell, R. (1992). Sulphate stimulation of mercury methylation in fresh-water sediments. Environ Sci Technol, 26, 2281–7CrossRefGoogle Scholar
Goulhen, F., Gloter, A., Guyot, F. and Bruschi, M. (2006). Desulfovibrio vulgaris strain Hildenborough: Microbe–metal interactions studies. Appl Microbiol Biotechnol, 71, 892–7CrossRefGoogle ScholarPubMed
Heidelberg, J. F., Seshadri, R., Haveman, S. A.et al. (2004). The genome sequence of the anaerobic, sulphate-reducing bacterium Desulfovibrio vulgaris Hildenborough. Nat Biotechnol, 22, 554–9CrossRefGoogle Scholar
Hobman, J. L., Wilson, J. R. and Brown, N. L. (2000). Microbial mercury reduction. In Lovley, D. R. (ed.), Environmental metal–microbe interactions. Washington, DC: ASM Press. pp. 177–98.CrossRefGoogle Scholar
Humphries, A. C. and Macaskie, L. E. (2002). Reduction of Cr(VI) by Desulfovibrio vulgaris and Microbacterium sp. Biotechnol Lett, 24, 1261–7CrossRefGoogle Scholar
Ishimoto, M., Kondo, Y., Kameyama, T., Yagi, T. and Shirak, M. (1958). The role of cytochrome in the enzyme system of sulphate-reducing bacteria. In Science Council of Japan (ed.), Proceedings of the International Symposium on Enzyme Chemistry. Tokyo and Kyoto: Marüzen. pp. 229–34.Google Scholar
Kesen, M. A., Schicho, R. N., Kelly, R. M. and Adams, M. W. W. (1993). Hydrogenase of the hyperthermophile Pyrococcus furiosus is an elemental sulfur reductase or sulfurylase: Evidence for a sulfur-reducing hydrogenase ancestor. Proc Nat Acad Sci USA, 90, 5341–4Google Scholar
King, J. K., Kosta, J. E., Frischer, M. E. and Saunders, F. M. (2000). Sulphate-reducing bacteria methylate mercury at variable rates in pure culture and in marine sediments. Appl Environ Microbiol, 66, 2430–7CrossRefGoogle Scholar
Kirk, M. F., Holm, T. R., Park, J.et al. (2004). Bacterial sulphate reduction limits natural arsenic contamination in groundwater. Geol, 32, 953–6CrossRefGoogle Scholar
Klenk, H. P., Clayton, R. A., Tomb, J. F.et al. (1997). The complete genome sequence of the hyperthermophilic, sulphate-reducing archaeon Archaeoglobus fulgidus. Nature, 390, 364–70CrossRefGoogle ScholarPubMed
Korthals, E. T. and Winfrey, M. R. (1987). Seasonal and spatial variations in mercury methylation and demethylation in an oligotrophic lake. Appl Environ Microbiol, 53, 2397–404Google Scholar
Lloyd, J. R., Mabbett, A. N., Williams, D. R. and Macaskie, L. E. (2001). Metal reduction by sulphate-reducing bacteria: physiological diversity and metal specificity. Hydrometallurgy, 59, 327–37CrossRefGoogle Scholar
Lloyd, J. R. and Macaskie, L. E. (2000). Bioremediation of radionuclide-containing wastewaters. In Lovley, D. R. (ed.), Environmental metal–microbe interactions. Washington, DC: ASM Press. pp. 277–329.CrossRefGoogle Scholar
Lloyd, J. R., Ridley, J., Khizniak, T., Lyalikova, N. N. and Macaskie, L. E. (1999). Reduction of technetium by Desulfovibrio desulfuricans: biocatalyst characterization and use in a flowthrough bioreactor. Appl Environ Microbiol, 65, 2691–6Google Scholar
Lloyd, J. R., Yong, P. and Macaskie, L. E. (1998). Enzymatic recovery of elemental palladium by using sulphate-reducing bacteria. Appl Environ Microbiol 64, 4607–9Google Scholar
Lojou, E., Bianco, P. and Bruschi, M. (1998 a). Kinetic studies on the electron transfer between bacterial c-type cyrochromes and metal oxides. J Electroanal Chem, 452, 167–77CrossRefGoogle Scholar
Lojou, E., Bianco, P. and Bruschi, M. (1998 b). Kinetic studies on the electron transfer between various c-type cytochromes and iron (III) using a voltametric approach. Electrochim Acta, 43, 2005–13CrossRefGoogle Scholar
Lojou, E. and Bianco, P. (1999). Electrocatalytic reduction of uranium by bacterial cytochromes: biochemical factors influencing the catalytic process. J Electroanal Chem, 471, 96–104CrossRefGoogle Scholar
Lovley, D. R., Giovannoni, S. J., White, D. C.et al. (1993 a). Geobacter metallireducens 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, 336–44CrossRefGoogle ScholarPubMed
Lovley, D. R. and Phillips, E. J. P. (1992). Reduction of uranium by Desulfovibrio desulfuricans. Appl Microbiol Microbiol, 58, 850–6Google ScholarPubMed
Lovley, D. R. and Phillips, E. J. P. (1994). Reduction of chromate by Desulfovibrio vulgaris and its c3 cytochrome. Appl Environ Microbiol, 60, 726–8Google Scholar
Lovley, D. R., Widman, P. K., Woodward, J. C. and Phillips, E. J. (1993 b). Reduction of uranium by cytochrome c3 of Desulfovibrio vulgaris. Appl Environ Microbiol, 59, 3572–6Google ScholarPubMed
Mabbett, A. N., Lloyd, J. R. and Macaskie, L. E. (2002). Effect of complexing agents on reduction of Cr(VI) by Desulfovibrio vulgaris ATCC 29579. Biotechnol Bioengineering, 79, 389–397CrossRefGoogle Scholar
Macalady, J. L., Mack, E. E., Nelson, D. C. and Scow, K. M. (2000). Sediment microbial community structure and mercury methylation in mercury-polluted Clear Lake, California. Appl Environ Microbiol, 66, 1479–88CrossRefGoogle ScholarPubMed
Macy, J. M., Santini, J. M., Pauling, B. V., O'Neill, A. H. and Sly, L. I. (2000). Two new arsenate/sulphate-reducing bacteria: mechanisms of arsenate reduction. Arch Microbiol, 173, 49–57CrossRefGoogle Scholar
Marvin-DiPasquale, M., Agee, J., McGowan, C.et al. (2000). Methyl-mercury degradation pathways: a comparison among three mercury-impacted ecosystems. Environ Sci Technol, 34, 4908–16CrossRefGoogle Scholar
Marvin-DiPasquale, M. and Agee, M. (2003). Microbial mercury cycling in sediments of the San Francisco bay-delta. Estuaries, 26, 1517–28CrossRefGoogle Scholar
Michel, C., Brugna, M., Aubert, C., Bernadac, A. and Bruschi, M. (2001). Enzymatic reduction of chromate: comparative studies using sulphate-reducing bacteria. Key role of polyheme cytochromes c and hydrogenases. Appl Microbiol Biotechnol, 55, 95–100CrossRefGoogle Scholar
Newman, D. K., Kennedy, E. K., Coates, J. D.et al. (1997). Dissimilatory arsenate and sulphate reduction in Desulfotomaculum auripigmentum sp. nov. Arch Microbiol, 168, 380–8CrossRefGoogle ScholarPubMed
Nies, D. H. (1999). Microbial heavy-metal resistance. Appl Microbiol Biotechnol, 51, 730–50CrossRefGoogle ScholarPubMed
Nies, D. H., Koch, S., Shinichiro, W., Peitzch, N. and Saier, M. H. (1998). CHR, a novel family of prokaryotic proton motive force-driven transporters probably containing chromate/sulphate antiporters. J Bacteriol, 180, 5799–802Google ScholarPubMed
Oremland, R. S. and Stolz, J. (2000). Dissimilatory reduction of selenate and arsenate in nature. In Lovley, D. R. (ed.), Environmental Metal–Microbe Interactions. Washington, DC: ASM Press. pp. 199–224.CrossRefGoogle Scholar
Oremland, R. S. and Stolz, J. F. (2003). The ecology of arsenic. Science, 300, 939–44CrossRefGoogle ScholarPubMed
Osborn, A. M., Bruce, K. D., Strike, P. and Ritchie, D. A. (1997). Distribution, diversity and evolution of the bacterial mercury resistance (mer) operon. FEMS Microbiol Rev, 19, 239–62CrossRefGoogle ScholarPubMed
Pak, K.-R. and Bartha, R. (1998a). Mercury methylation and demethylation in anoxic lake sediments and by strictly anaerobic bacteria. Appl Environ Microbiol, 64, 1013–17Google Scholar
Pak, K.-R. and Bartha, R. (1998 b). Products of mercury demethylation of sulfidogens and methanogens. Bull Environ Con Toxicol 61, 690–4CrossRefGoogle ScholarPubMed
Pak, K.-R. and Bartha, R. (1998 c). Mercury methylation by interspecies hydrogen and acetate transfer between sulfidogens and methogens. Appl Environ Microbiol, 64, 1987–90Google Scholar
Payne, R. B., Casalot, L., Rivere, T.et al. (2004). Interaction between uranium and the cytochrome c3 of Desulfovibrio desulfuricans G20. Arch Microbiol, 181, 398–406CrossRefGoogle Scholar
Payne, R. B., Gentry, D. M., Rapp-Giles, B. J., Casalot, L. and Wall, J. D. (2002). Uranium reduction by Desulfovibrio desulfuricans strain G20 and a cytochrome c3 mutant. Appl Environ Microbiol, 68, 3129–32CrossRefGoogle Scholar
Rabus, R., Ruepp, A., Frickey, T.et al. (2004).The genome of Desulfotalea psychrophila, a sulphate-reducing bacterium from permanently cold Arctic sediments. Environ Microbiol, 6, 887–902CrossRefGoogle Scholar
Saltikov, C. W. and Newman, D. K. (2003). Genetic identification of a respiratory arsenate reductase. Proc Nat Acad Sci USA, 100, 10983–8CrossRefGoogle ScholarPubMed
Sani, R. K., Peyton, B. M.Smith, W. A., Apel, W. A. and Petersen, J. N. (2002). Dissimilatory reduction of Cr(VI), Fe(III), and U(VI) by Cellulomonas isolates. Appl Microbiol Biotechnol, 60, 192–9Google ScholarPubMed
Silver, S. and Phung, L. T. (2005). Genes and enzymes involved in bacterial oxidation and reduction of inorganic arsenic. Appl Environ Microbiol, 71, 599–608CrossRefGoogle ScholarPubMed
Susuki, Y., Kelly, S. D., Kemner, K. M. and Banfield, J. F. (2004). Enzymatic U(VI) reduction by Desulfosporosinus species. Radiochim Acta, 92, 11–16Google Scholar
Tomei, F. A., Barton, L. L., Lemanski, C. L.et al. (1995). Transformation of selenate and selenite to elemental selenium by Desulfovibrio desulfuricans. J Indust Microbiol, 14, 329–36CrossRefGoogle Scholar
Tucker, M. D., Barton, L. L. and Thomson, B. M. (1998). Reduction of Cr, Mo, Se and U by Desulfovibrio desulfuricans immobilized in polyacrylamide gels. J Industr Microbiol Biotechnol, 20, 13–19CrossRefGoogle ScholarPubMed
Turner, R. J., Weiner, J. H. and Taylor, D. E. (1998). Selenium metabolism inEscherichia coli. BioMetals, 11, 223–7Google ScholarPubMed
Vignais, P. M., Billoud, B. and Meyer, J. (2001). Classification and phylogeny of hydrogenases. FEMS Microbiol Rev, 25, 455–501CrossRefGoogle ScholarPubMed
Wang, Y.-T. (2000). Microbial reduction of chromate. In Lovley, D. R. (ed.), Environmental Metal–Microbe Interactions. Washington, DC: ASM Press. pp. 225–6.CrossRefGoogle Scholar
Warner, K. A., Roden, E. E. and Bonzongo, J. C. (2003). Microbial mercury transformation in anoxic freshwater sediments under iron-reducing and other electron-accepting conditions. Environ Sci Technol, 37, 2159–65CrossRefGoogle ScholarPubMed
Yanke, L. J., Bryant, R. D. and Laishley, E. J. (1995). Hydrogenase I of Clostridium pasteuranium functions as a novel selenite reductase. Anaerobe, 1, 61–7CrossRefGoogle Scholar

Save book to Kindle

To save this book to your Kindle, first ensure [email protected] is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×