Anaerobic degradation of hydrocarbons with sulphate as electron acceptor

doi:10.1017/CBO9780511541490.010

9 - Anaerobic degradation of hydrocarbons with sulphate as electron acceptor

Published online by Cambridge University Press: 22 August 2009

Friedrich Widdel ,

Florin Musat ,

Katrin Knittel and

Alexander Galushko

Edited by

Larry L. Barton and

W. Allan Hamilton

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Larry L. Barton: Affiliation:
University of New Mexico
W. Allan Hamilton: Affiliation:
University of Aberdeen

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Summary

INTRODUCTION

Sulphate-reducing bacteria (SRB), or more generally speaking sulphate-reducing prokaryotes (SRP), are terminal oxidizers in the natural recycling of bio-organic compounds to CO2 in anoxic environments, in particular in marine sediments. SRP play this geochemically important role because they make use of a globally abundant electron acceptor, sulphate (in seawater up to 28 mM), and possess numerous degradative (oxidative) capacities with respect to electron donors. The study of the degradative potentials of SRP via de novo enrichment (including direct counting) and isolation from natural samples has been of interest over some decades and formed the basis for our knowledge of the phylogenetic diversity of SRP. Common electron donors and carbon sources of SRP are the low-molecular mass products from the primary anaerobic (fermentative) breakdown of polysaccharides, proteins, lipids and other substances of dead biomass. Several of the involved degradative capacities, for instance complete oxidation or the channelling of branched-chain fatty acids or aromatic compounds into the central metabolism, require special enzymatic reactions (for overview see Rabus et al., 2000) which are not encountered in fermentative bacteria. The study of such and other metabolic capacities in SRP has led to the recognition of principles of general importance or heuristic value in our understanding of the biochemistry and energetics of anaerobes.

A chemical class of organic substrates which have become of interest relatively recently in the study of SRP (and other anaerobes) are hydrocarbons, in particular those from crude oil (petroleum).

Type: Chapter
Information: Sulphate-Reducing Bacteria
Environmental and Engineered Systems
, pp. 265 - 304

DOI: https://doi.org/10.1017/CBO9780511541490.010 [Opens in a new window]

Publisher: Cambridge University Press

Print publication year: 2007

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References

Aeckersberg, F., Bak, F. and Widdel, F. (1991). Anaerobic oxidation of saturated hydrocarbons to CO2 by a new type of sulphate-reducing bacteria. Arch Microbiol, 156, 5–14CrossRef Google Scholar

Aeckersberg, F., Rainey, F. A. and Widdel, F. (1998). Growth, natural relationships, cellular fatty acids and metabolic adaptation of sulphate-reducing bacteria that utilize long-chain alkanes under anoxic conditions. Arch Microbiol, 170, 361–9CrossRef Google Scholar

Aitken, C. M., Jones, D. M. and Larter, S. R. (2004). Anaerobic hydrocarbon biodegradation in deep subsurface oil reservoirs. Nature, 431, 291–4CrossRef Google Scholar PubMed

Alperin, M. J. and Reeburgh, W. S. (1985). Inhibition experiments on anaerobic methane oxidation. Appl Environ Microbiol, 50, 940–5Google Scholar PubMed

Annweiler, E., Materna, A., Safinowski, M.et al. (2000). Anaerobic degradation of 2-methylnaphthalene by a sulphate-reducing enrichment culture. Appl Environ Microbiol, 66, 5329–33CrossRef Google Scholar

Annweiler, E., Michaelis, W. and Meckenstock, R. U. (2002). Identical ring cleavage products during anaerobic degradation of naphthalene, 2-methylnaphthalene, and tetralin indicate a new metabolic pathway. Appl Environ Microbiol, 68, 852–8CrossRef Google Scholar PubMed

Bak, F. and Widdel, F. (1986). Anaerobic degradation of phenol and phenol derivates by Desulfobacterium phenolicum sp. nov. Arch Microbiol, 146, 177–80CrossRef Google Scholar

Barnes, R. O. and Goldberg, E. D. (1976). Methane production and consumption in anoxic marine sediments. Geology, 4, 297–3002.0.CO;2>CrossRef Google Scholar

Bastin, E. S., Greer, F. E., Merritt, C. A. and Moulton, G. (1926). The presence of sulphate reducing bacteria in oil field waters. Science, 63, 21–4CrossRef Google Scholar PubMed

Beller, H. R., Reinhard, M. and Grbic'-Galic', D. (1992). Metabolic by-products of anaerobic toluene degradation by sulphate-reducing enrichment cultures. Appl Environ Microbiol, 58, 3192–5Google Scholar

Beller, H. and Spormann, A. (1997). Benzylsuccinate formation as a means of anaerobic toluene activation by sulphate-reducing strain PRTOL1. Appl Environ Microbiol, 63, 3729–31Google Scholar

Beller, H., Spormann, A., Sharma, P., Cole, J. and Reinhard, M. (1996). Isolation and characterization of a novel toluene-degrading, sulphate-reducing bacterium. Appl Environ Microbiol, 62, 1188–96Google Scholar

Boetius, A., Ravenschlag, K., Schubert, C. J.et al. (2000). A marine microbial consortium apparently mediating anaerobic oxidation of methane. Nature, 407, 623–6CrossRef Google Scholar PubMed

Boll, M. (2005). Key enzymes in the anaerobic aromatic metabolism catalysing Birch-like reductions. Biochim Biophys Acta (BBA) – Bioenergetics, 1707, 34–50CrossRef Google Scholar PubMed

Boll, M., Fuchs, G. and Heider, J. (2002). Anaerobic oxidation of aromatic compounds and hydrocarbons. Curr Opin Chem Biol, 6, 604–11CrossRef Google Scholar PubMed

Caldwell, M. E. and Suflita, J. M. (2000). Detection of phenol and benzoate as intermediates of anaerobic benzene biodegradation under different terminal electron-accepting conditions. Environ Sci Technol, 34, 1216–20CrossRef Google Scholar

Coates, J., Anderson, R. and Lovley, D. (1996). Oxidation of polycyclic aromatic hydrocarbons under sulphate-reducing conditions. Appl Environ Microbiol, 62, 1099–101Google Scholar

Coates, J. D., Chakraborty, R. and McInerney, M. J. (2002). Anaerobic benzene degradation – a new era. Res Microbiol, 153, 621–8CrossRef Google Scholar PubMed

Coates, J., Woodward, J., Allen, J., Philp, P. and Lovley, D. (1997). Anaerobic degradation of polycyclic aromatic hydrocarbons and alkanes in petroleum-contaminated marine harbor sediments. Appl Environ Microbiol, 63, 3589–93Google Scholar PubMed

Connan, J., Lacrampe-Coulome, G. and Magot, M. (1996). Origin of gases in reservoirs. In Dolenc, D. (ed.), Proceedings of the 1995 International Gas Research Conference Vol. 1. Rockville: Government Institutes. pp. 21–62.Google Scholar

Cravo-Laureau, C., Grossi, V., Raphel, D., Matheron, R. and Hirschler-Rea, A. (2005). Anaerobic n-alkane metabolism by a sulphate-reducing bacterium, Desulfatibacillum aliphaticivorans strain CV2803T. Appl Environ Microbiol, 71, 3458–67CrossRef Google Scholar

Cravo-Laureau, C., Hirschler-Rea, A., Matheron, R. and Grossi, V. (2004a). Growth and cellular fatty-acid composition of a sulphate-reducing bacterium, Desulfatibacillum aliphaticivorans strain CV2803T, grown on n-alkenes. Comptes Rendus Biologies, 327, 687–94CrossRef Google Scholar

Cravo-Laureau, C., Matheron, R., Cayol, J.-L., Joulian, C. and Hirschler-Rea, A. (2004b). Desulfatibacillum aliphaticivorans gen. nov., sp. nov., an n-alkane- and n-alkene-degrading, sulphate-reducing bacterium. Int J Syst Evol Microbiol, 54, 77–83CrossRef Google Scholar

Cravo-Laureau, C., Matheron, R., Joulian, C., Cayol, J.-L. and Hirschler-Rea, A. (2004c). Desulfatibacillum alkenivorans sp. nov., a novel n-alkene-degrading, sulphate-reducing bacterium, and emended description of the genus Desulfatibacillum. Int J Syst Evol Microbiol, 54, 1639–42CrossRef Google Scholar

d'Ans, J. and Lax, E. (1983). Taschenbuch für Chemiker und Physiker, Bd. 2 (Ed, Synowietz, C.). Berlin: Springer.Google Scholar

Davico, G. E. B., Veronica, M., DePuy, C. H., Ellison, G. B. and Squires, R. R. (1995). The C–H bond energy of benzene. J Am Chem Soc, 117, 2590–9CrossRef Google Scholar

Davidova, I. A., Gieg, L. M., Nanny, M.et al., (2005). Stable isotope studies of n-alkane metabolism by a sulphate-reducing bacteria enrichment culture. Appl Environ Microbiol, 71, 8174–82CrossRef Google Scholar

Davidova, I. A. and Suflita, J. M. (2005). In Leadbetter, J. R. (ed.), Methods in enzymology, Vol. 397. Amsterdam and London: Elsevier Academic Press. pp. 17–34.Google Scholar

Dean, J. A. (1992). Lange's handbook of chemistry. New York: McGraw-Hill.Google Scholar

Edwards, E. A. and Grbić-Galić, D. (1992). Complete mineralization of benzene by aquifer microorganisms under strictly anaerobic conditions. Appl Environ Microbiol, 58, 2663–6Google Scholar PubMed

Elshahed, M. S., Gieg, L. M., McInerney, M. J. and Suflita, J. M. (2001). Signature metabolites attesting to the in situ attenuation of alkylbenzenes in anaerobic environments. Environ Sci Technol, 35, 682–9CrossRef Google Scholar PubMed

Elvert, M., Suess, E. and Whiticar, M. J. (1999). Anaerobic methane oxidation associated with marine gas hydrates: superlight C-isotopes from saturated and unsaturated C20 and C25 irregular isoprenoids. Naturwissenschaften, 86, 295–300CrossRef Google Scholar

Fischer-Romero, C., Tindall, B. and Jüttner, F. (1996). Tolumonas auensis gen. nov., sp. nov., a toluene-producing bacterium from anoxic sediments of a freshwater lake. Int J Syst Bacteriol, 46, 183–8CrossRef Google Scholar PubMed

Flesher, J. W. and Myers, S. R. (1991). Methyl-substitution of benzene and toluene in preparations of human bone marrow. Life Sci, 48, 843–50CrossRef Google Scholar PubMed

Galushko, A. S., Kiesele-Lang, U. and Kappler, A. (2003). Degradation of 2-methylnaphthalene by a sulphate-reducing enrichment culture of mesophilic freshwater bacteria. Polyc Arom Comp, 23, 207–18CrossRef Google Scholar

Galushko, A., Minz, D., Schink, B. and Widdel, F. (1999). Anaerobic degradation of naphthalene by a pure culture of a novel type of marine sulphate-reducing bacterium. Environ Microbiol, 1, 415–20CrossRef Google Scholar PubMed

Galushko, A. S. and Rozanova, E. P. (1991). Desulfobacterium cetonicum sp. nov. – a sulphate–reducing bacterium which oxidizes fatty acids and ketones. Microbiol (Engl.Transl. Mikrobiologiya (USSR)), 60, 742–6Google Scholar

Gieg, L. M. and Suflita, J. M. (2002). Detection of anaerobic metabolites of saturated and aromatic hydrocarbons in petroleum-contaminated aquifers. Environ Sci Technol, 36, 3755–62CrossRef Google Scholar PubMed

Grogan, D. W. and Cronan, J. E. Jr. (1997). Cyclopropane ring formation in membrane lipds of bacteria. Microbiol Mol Biol Rev, 61, 429–41Google Scholar

Girguis, P. R., Cozen, A. E. and DeLong, E. F. (2005). Growth and population dynamics of anaerobic methane-oxidizing archaea and sulphate-reducing bacteria in a continuous-flow bioreactor. Appl Environ Microbiol, 71, 3725–33CrossRef Google Scholar

Groves, J. T. (2006). High-valent iron in chemical and biological oxidations. J Inorg Biochem, 100, 434–47CrossRef Google Scholar PubMed

Habicht, K. S., Gade, M., Thamdrup, B., Berg, P. and Canfield, D. E. (2002). Calibration of sulphate levels in the Archaean ocean. Science, 298, 2372–4CrossRef Google Scholar

Hallam, S. J., Girguis, P. R., Preston, C. M., Richardson, P. M. and DeLong, E. F. (2003). Identification of methyl coenzyme M reductase A (mcrA) genes associated with methane-oxidizing Archaea. Appl Environ Microbiol, 69, 5483–91CrossRef Google Scholar PubMed

Hallam, S. J., Putnam, N., Preston, C. M.et al. (2004). Reverse methanogenesis: testing the hypothesis with environmental genomics. Science, 305, 1457–62CrossRef Google Scholar PubMed

Harder, J. (1997). Anaerobic methane oxidation by bacteria employing 14C-methane uncontaminated with 14C-carbon monoxide. Marine Geol, 137, 13–23CrossRef Google Scholar

Harms, G., Zengler, K., Rabus, R.et al. (1999). Anaerobic oxidation of o-xylene, m-xylene, and homologous alkylbenzenes by new types of sulphate-reducing bacteria. Appl Environ Microbiol, 65, 999–1004Google Scholar

Hayes, L. A., Nevin, K. P. and Lovley, D. R. (1999). Role of prior exposure on anaerobic degradation of naphthalene and phenanthrene in marine harbor sediments. Org Geochem, 30, 937–45CrossRef Google Scholar

Head, I. M., Jones, D. M. and Larter, S. R. (2003). Biological activity in the deep subsurface and the origin of heavy oil. Nature, 426, 344–52CrossRef Google Scholar PubMed

Hedderich, R. and Whitman, W. B. (2006). Physiology and biochemistry of the methane-producing archaea. In Dworkin, M., Rosenberg, E., Schleifer, K.-H. and Stackebrandt, E. (eds.), The prokaryotes, electronic edition. New York: Springer. (URL: http://141.150.157.117:8080/prokPUB/index.htm).Google Scholar

Hinrichs, K. U. and Boetius, A. B. (2002). In Wefer, G., Hebbeln, D., Jørgensen, B. B., Schlüter, M. and Weering, T. (eds.), Ocean margin systems, Heidelberg: Springer-Verlag. pp. 457–77.Google Scholar

Hinrichs, K. U., Hayes, J. M., Sylva, S. P., Brewer, P. G. and DeLong, E. F. (1999). Methane-consuming archaebacteria in marine sediments. Nature, 398, 802–5CrossRef Google Scholar PubMed

Hoehler, T. M., Alperin, M. J., Albert, D. B. and Martens, C. S. (1994). Field and laboratory studies of methane oxidation in an anoxic marine sediment: evidence for a methanogen-sulphate reducer consortium. Global Biogeochem Cycles, 8, 451–63CrossRef Google Scholar

Holm, N. G. and Charlou, J. L. (2001). Initial indications of abiotic formation of hydrocarbons in the Rainbow ultramafic hydrothermal system, Mid-Atlantic Ridge. Earth Planet Sci Lett, 191, 1–8CrossRef Google Scholar

Horng, Y.-C., Becker, D. F. and Ragsdale, S. W. (2001). Mechanistic studies of methane biogenesis by methyl-coenzyme M reductase: evidence that coenzyme B participates in cleaving the C–S bond of methyl-coenzyme M. Biochemistry, 40, 12875–85CrossRef Google Scholar

Hunkeler, D., Höhener, P. and Zeyer, J. (2002). Engineered and subsequent intrinsic in situ bioremediation of a diesel fuel contaminated aquifer. J Contam Hydrol, 59, 231–45CrossRef Google Scholar PubMed

Hylemon, P. B. and Harder, J. (1998). Biotransformation of monoterpenes, bile acids, and other isoprenoids in anaerobic ecosystems. FEMS Microbiol Rev, 22, 475–88CrossRef Google Scholar PubMed

Iversen, N. and Jørgensen, B. B. (1985). Anaerobic methane oxidation rates at the sulphate methane transition in marine-sediments from Kattegat and Skagerrak (Denmark). Limnol Oceanogr, 30, 944–55CrossRef Google Scholar

Johnson, H. A. and Spormann, A. M. (1999). In vitro studies on the initial reactions of anaerobic ethylbenzene mineralization. J Bacteriol, 181, 5662–8Google Scholar PubMed

Jones, W. D. (2000). Conquering the carbon–hydrogen bond. Science, 287, 1942–3CrossRef Google Scholar

Kniemeyer, O., Fischer, T., Wilkes, H., Glöckner, F. O. and Widdel, F. (2003). Anaerobic degradation of ethylbenzene by a new type of marine sulphate-reducing bacterium. Appl Environ Microbiol, 69, 760–8CrossRef Google Scholar

Kniemeyer, O. and Heider, J. (2001). Ethylbenzene dehydrogenase, a novel hydrocarbon-oxidizing molybdenum/iron-sulfur/heme enzyme. J Biol Chem, 276, 21381–6CrossRef Google Scholar PubMed

Knittel, K., Boetius, A., Lemke, A.et al. (2003). Activity, distribution, and diversity of sulphate reducers and other bacteria in sediments above gas hydrates (Cascadia Margin, Oregon). Geomicrobiol J, 20, 269–94CrossRef Google Scholar

Knittel, K., Lösekann, T., Boetius, A., Kort, R. and Amann, R. (2005). Diversity and distribution of methanotrophic Archaea at cold seeps. Appl Environ Microbiol, 71, 467–79CrossRef Google Scholar PubMed

Kropp, K. G., Davidova, I. A. and Suflita, J. M. (2000). Anaerobic oxidation of n-dodecane by an addition reaction in a sulphate-reducing bacterial enrichment culture. Appl Environ Microbiol, 66, 5393–8CrossRef Google Scholar

Krüger, M., Meyerdierks, A., Glöckner, F. O.et al. (2003). A conspicuous nickel protein in microbial mats that oxidize methane anaerobically. Nature, 426, 878–81CrossRef Google Scholar PubMed

Kvenvolden, K. A. (1999). Potential effects of gas hydrate on human welfare. PNAS, 96, 3420–6CrossRef Google Scholar PubMed

Lovley, D. R., Coates, J. D., Woodward, J. C. and Phillips, E. J. P. (1995). Benzene oxidation coupled to sulphate reduction. Appl Environ Microbiol, 61, 953–8Google Scholar

Martens, C. S. and Berner, R. A. (1974). Methane production in the interstitial waters of sulphate-depleted marine sediment. Science, 185, 1167–9CrossRef Google Scholar

Mavrovounoitis, M. L. (1991). Estimation of standard Gibbs energy changes of biotransformations. J Biol Chem, 266, 14440–5Google Scholar

McGillen, D. F. and Golden, D. M. (1982). Hydrocarbon bond dissociation energies. Ann Rev Phys Chem, 33, 493–532CrossRef Google Scholar

Meckenstock, R. U., Annweiler, E., Michaelis, W., Richnow, H. H. and Schink, B. (2000). Anaerobic naphthalene degradation by a sulphate-reducing enrichment culture. Appl Environ Microbiol, 66, 2743–7CrossRef Google Scholar

Meckenstock, R. U., Morasch, B., Griebler, C. and Richnow, H. H. (2004). Stable isotope analysis as a tool to monitor biodegradation in contaminated aquifers. J Contam Hydrol, 75, 215–55CrossRef Google Scholar

Meckenstock, R. U., Morasch, B., Warthmann, R.et al. (1999). 13C/12C isotope fractionation of aromatic hydrocarbons during microbial degradation. Environ Microbiol, 1, 409–14CrossRef Google Scholar PubMed

Michaelis, W., Seifert, R., Nauhaus, K.et al. (2002). Microbial reefs in the Black Sea fueled by anaerobic oxidation of methane. Science, 297, 1013–15CrossRef Google Scholar PubMed

Moran, J. J., House, C., Freeman, K. H. and Ferry, J. J. (2005). Trace methane oxidation studied in several Euryarchaeota under diverse conditions. Archaea, 1, 303–9CrossRef Google Scholar PubMed

Morasch, B. and Meckenstock, R. U. (2005). Anaerobic degradation of p-xylene by a sulphate-reducing enrichment culture. Curr Microbiol, 51, 127–30CrossRef Google Scholar

Morasch, B., Schink, B., Tebbe, C. and Meckenstock, R. U. (2004). Degradation of o-xylene and m-xylene by a novel sulphate-reducer belonging to the genus Desulfotomaculum. Arch Microbiol, 181, 407–17CrossRef Google Scholar

Mrowiec, B., Suschka, J. and Keener, T. C. (2005). Formation and biodegradation of toluene in the anaerobic sludge digestion process. Water Environ Res, 77, 274–8CrossRef Google Scholar PubMed

Nauhas, K., Albrecht, M. and Elvert, M.et al. (2007). In vitro cell growth of marine archaeal-bacterial consortia during anaerobic oxidation of methane with sulfate. Environ Microbiol, 9, 187–96CrossRef Google Scholar

Nauhaus, K., Boetius, A., Kruger, M. and Widdel, F. (2002). In vitro demonstration of anaerobic oxidation of methane coupled to sulphate reduction in sediment from a marine gas hydrate area. Environ Microbiol, 4, 296–305CrossRef Google Scholar PubMed

Nauhaus, K., Treude, T., Boetius, A. and Krüger, M. (2005). Environmental regulation of the anaerobic oxidation of methane: a comparison of ANME-I and ANME-II communities. Environ Microbiol, 7, 98–106CrossRef Google Scholar PubMed

Orphan, V. J., House, C. H., Hinrichs, K. U., McKeegan, K. D. and DeLong, E. F. (2002). Multiple archaeal groups mediate methane oxidation in anoxic cold seep sediments. PNAS, 99, 7663–8CrossRef Google Scholar PubMed

Pancost, R. D., Sinninghe Damste, J. S., Lint, S., Maarel, M. J. E. C., Gottschal, J. C. and The Medinaut Shipboard Scientific Party. (2000). Biomarker evidence for widespread anaerobic methane oxidation in Mediterranean sediments by a consortium of methanogenic Archaea and Bacteria. Appl Environ Microbiol, 66, 1126–32CrossRef Google Scholar PubMed

Paull, C. K., Chanton, J., Neumann, A. C.et al. (1992). Indicators of methane-derived carbonates and chemosynthetic organic carbon deposits: examples from the Florida Escarpment. Palaios, 7, 361–75CrossRef Google Scholar

Pelmenschikov, V., Blomberg, M. R. A., Siegbahn, P. E. M. and Crabtree, R. H. (2002). A mechanism from quantum chemical studies for methane formation in methanogenesis. J Am Chem Soc, 124, 4039–49CrossRef Google Scholar PubMed

Peters, F., Rother, M. and Boll, M. (2004). Selenocysteine-containing proteins in anaerobic benzoate metabolism of Desulfococcus multivorans. J Bacteriol, 186, 2156–63CrossRef Google Scholar PubMed

Phelps, C. D., Kazumi, J. and Young, L. Y. (1996). Anaerobic degradation of benzene in BTX mixtures dependent on sulphate reduction. FEMS Microbiol Lett, 145, 433–7CrossRef Google Scholar

Phelps, C. D., Kerkhof, L. J. and Young, L. Y. (1998). Molecular characterization of a sulphate-reducing consortium which mineralizes benzene. FEMS Microbiol Ecol, 27, 269–79CrossRef Google Scholar

Phelps, C. D., Zhang, X. and Young, L. Y. (2001). Use of stable isotopes to identify benzoate as a metabolite of benzene degradation in a sulphidogenic consortium. Environ Microbiol, 3, 600–3CrossRef Google Scholar

Postgate, J. R. (1984). The sulphate-reducing bacteria. Cambridge, UK: Cambridge University Press.Google Scholar

Rabus, R., Hansen, T. and Widdel, F. (2000). Dissimilatory sulphate- and sulfur-reducing prokaryotes. In Dworkin, M., Rosenberg, E., Schleifer, K.-H. and Stackebrandt, E. (eds.), The prokaryotes, electronic edition. New York: Springer. (URL: http://141.150.157.117:8080/prokPUB/index.htm).Google Scholar

Rabus, R. and Heider, J. (1998). Initial reactions of anaerobic metabolism of alkylbenzenes in denitrifying and sulphate-reducing bacteria. Arch Microbiol, 170, 377–84CrossRef Google Scholar

Rabus, R., Nordhaus, R., Ludwig, W. and Widdel, F. (1993). Complete oxidation of toluene under strictly anoxic conditions by a new sulphate-reducing bacterium. Appl Environ Microbiol, 59, 1444–51Google Scholar

Rabus, R., Wilkes, H., Behrends, A.et al. (2001). Anaerobic initial reaction of n-alkanes in a denitrifying bacterium: evidence for (1-methylpentyl)succinate as initial product and for involvement of an organic radical in n-hexane metabolism. J Bacteriol, 183, 1707–15CrossRef Google Scholar

Raghoebarsing, A. A., Pol, A., Pas-Schoonen, K. T.et al. (2006). A microbial consortium couples anaerobic methane oxidation to denitrification. Nature, 440, 918–21CrossRef Google Scholar PubMed

Reeburgh, W. S. (1976). Methane consumption in Cariaco Trench waters and sediments. Earth Planet Sci Lett, 28, 337–44CrossRef Google Scholar

Reeburgh, W. S. (1980). Anaerobic methane oxidation: rate depth distributions in Skan Bay sediments. Earth Planet Sci Lett, 47, 345–52CrossRef Google Scholar

Reed, D. R. and Kass, S. R. (2000). Experimental determination of the α and β C–H bond dissociation energies in naphthalene. J Mass Spectr, 35, 534–93.0.CO;2-T>CrossRef Google Scholar PubMed

Reguera, G., McCarthy, K. D., Mehta, T.et al. (2005). Extracellular electron transfer via microbial nanowires. Nature, 435, 1098–101CrossRef Google Scholar PubMed

Reusser, D. E., Istok, J. D., Beller, H. R. and Field, J. A. (2002). In situ transformation of deuterated toluene and xylene to benzylsuccinic acid analogues in BTEX-contaminated aquifers. Environ Sci Technol, 36, 4127–34CrossRef Google Scholar PubMed

Richnow, H. H., Annweiler, E., Michaelis, W. and Meckenstock, R. U. (2003). Microbial in situ degradation of aromatic hydrocarbons in a contaminated aquifer monitored by carbon isotope fractionation. J Contam Hydrol, 65, 101–20CrossRef Google Scholar

Ritger, S., Carson, B. and Suess, E. (1987). Methane-derived authigenic carbonates formed by subduction-induced pore-water expulsion along the Oregon/Washington margin. Geol Soc Am Bull, 98, 147–562.0.CO;2>CrossRef Google Scholar

Ruckmick, J. C., Wimberly, B. H. and Edwards, A. F. (1979). Classification and genesis of biogenic sulfur deposits. Econ Geol, 74, 469–74CrossRef Google Scholar

Rueter, P., Rabus, R., Wilkes, H.et al. (1994). Anaerobic oxidation of hydrocarbons in crude oil by new types of sulphate-reducing bacteria. Nature, 372, 455–8CrossRef Google Scholar PubMed

Safinowski, M. and Meckenstock, R. U. (2004). Enzymatic reactions in anaerobic 2-methylnaphthalene degradation by the sulphate-reducing enrichment culture N 47. FEMS Microbiol Lett, 240, 99–104CrossRef Google Scholar PubMed

Safinowski, M. and Meckenstock, R. U. (2006). Methylation is the initial reaction in anaerobic naphthalene degradation by a sulphate-reducing enrichment culture. Environ Microbiol, 8, 347–52CrossRef Google Scholar

Schink, B. (1985). Degradation of unsaturated hydrocarbons by methanogenic enrichment cultures. FEMS Microbiol Lett, 31, 69–77CrossRef Google Scholar

Schink, B. and Stams, A. F. (2002). Structure and growth dynamics of syntrophic associations. In Dworkin, M., Rosenberg, E., Schleifer, K.-H. and Stackebrandt, E. (eds.), The prokaryotes, electronic edition. New York: Springer. (URL: http://141.150.157.117:8080/prokPUB/index.htm).Google Scholar

Schmitt, R., Langguth, H. R. and Püttmann, W. (1998). Abbau aromatischer Kohlenwasserstoffe und Metabolitenbildung im Grundwasserleiter eines ehemaligen GaswerkstandortsGrundwasser, 3, 78–86CrossRef Google Scholar

Selmer, T. and Andrei, P. I. (2001). p-Hydroxyphenylacetate decarboxylase from Clostridium difficile: a novel glycyl radical enzyme catalysing the formation of p-cresol. Eur J Biochem, 268, 1363–72CrossRef Google Scholar PubMed

Selmer, T., Pierik, A. and Heider, J. (2005). New glycyl radical enzymes catalysing key metabolic steps in anaerobic bacteria. Biol Chem, 386, 981–8CrossRef Google Scholar PubMed

Shen, Y., Buick, R. and Canfield, D. E. (2001). Isotopic evidence for microbial sulphate reduction in the early Archaean era. Nature, 410, 77–81CrossRef Google Scholar PubMed

Shilov, A. E. and Shul'pin, B. (1997). Activation of C−H bonds by metal complexes. Chem Rev, 97, 2879–932CrossRef Google Scholar

Shima, S. and Thauer, R. K. (2005). Methyl-coenzyme M reductase and the anaerobic oxidation of methane in methanotrophic Archaea. Curr Opin Microbiol, 8, 643–8CrossRef Google Scholar PubMed

So, C. M., Phelps, C. D. and Young, L. Y. (2003). Anaerobic transformation of alkanes to fatty acids by a sulphate-reducing bacterium, strain Hxd3. Appl Environ Microbiol, 69, 3892–900CrossRef Google Scholar

So, C. M. and Young, L. Y. (1999). Isolation and characterization of a sulphate-reducing bacterium that anaerobically degrades alkanes. Appl Environ Microbiol, 65, 2969–76Google Scholar

Sørensen, K. B., Finster, K. and Ramsing, N. B. (2001). Thermodynamic and kinetic requirements in anaerobic methane oxidizing consortia exclude hydrogen, acetate and methanol as possible shuttles. Microbial Ecol, 42, 1–10Google Scholar PubMed

Spormann, A. M. and Widdel, F. (2000). Metabolism of alkylbenzenes, alkanes, and other hydrocarbons in anaerobic bacteria. Biodegradation, 11, 85–105CrossRef Google Scholar PubMed

Stumm, W. and Morgan, J. J. (1981). Aquatic Chemistry, 2nd edn. New York: John Wiley & Sons.Google Scholar

Sullivan, E. R., Zhang, X., Phelps, C. and Young, L. Y. (2001). Anaerobic mineralization of stable-isotope-labeled 2-methylnaphthaleneAppl Environ Microbiol, 67, 4353–7CrossRef Google Scholar PubMed

Tauson, V. O., Veselov, I. Ya. (1934). O bakterialnom razlozhenii tsiklicheskikh soyedineniy pri vosstanovlenii sulfatov. (On the bacteriology of the decomposition of cyclical compounds at the reduction of sulphates.) Mikrobiologiya (in Russian), 3, 360–9Google Scholar

Tissot, B. P. and Welte, D. H. (1984). Petroleum formation and occurrence. Berlin: Springer.CrossRef Google Scholar

Thauer, R. K., Jungermann, K. and Decker, K. (1977). Energy conservation in anaerobic bacteria. Bacteriol Rev, 41, 100–80Google Scholar PubMed

Thauer, R. K. (1998). Biochemistry of methanogenesis: a tribute to Marjory Stephenson. Microbiology, 144, 2377–406CrossRef Google Scholar PubMed

Townsend, G. T., Prince, R. C. and Suflita, J. M. (2003). Anaerobic oxidation of crude oil hydrocarbons by the resident microorganisms of a contaminated anoxic aquifer. Environ Sci Technol, 37, 5213–18CrossRef Google Scholar PubMed

Ulrich, A. C., Beller, H. R. and Edwards, E. A. (2005). Metabolites detected during biodegradation of 13C6-benzene in nitrate-reducing and methanogenic enrichment cultures. Environ Sci Technol, 39, 6681–91CrossRef Google Scholar PubMed

Weast, R. C. (1989). Handbook of chemistry and physics. Boca Raton, USA: CRC Press.Google Scholar

Widdel, F. (1988). Microbiology and ecology of sulphate- and sulfur-reducing bacteria. In Zehnder, A. J. B. (ed.), Biology of anaerobic microorganisms. New York: John Wiley & Sons. pp 469–585.Google Scholar

Widdel, F.Boetius, A. and Rabus, R. (2004). Anaerobic biodegradation of hydrocarbons including methane. In Dworkin, M., Rosenberg, E., Schleifer, K.-H. and Stackebrandt, E. (eds.), The prokaryotes, electronic edition. New York: Springer. (URL: http://141.150.157.117:8080/prokPUB/index.htm).Google Scholar

Widdel, F. and Rabus, R. (2001). Anaerobic biodegradation of saturated and aromatic hydrocarbons. Curr Opin Biotechnol, 12, 259–76CrossRef Google Scholar PubMed

Wilkes, H., Rabus, R., Fischer, T.et al. (2002). Anaerobic degradation of n-hexane in a denitrifying bacterium: Further degradation of the initial intermediate (1-methylpentyl) succinate via c-skeleton rearrangement. Arch Microbiol, 177, 235–43CrossRef Google Scholar

Wischgoll, S., Heintz, D., Peters, F.et al. (2005). Gene clusters involved in anaerobic benzoate degradation of Geobacter metallireducens. Mol Microbiol, 58, 1238–52CrossRef Google Scholar PubMed

Wolfe, R. S. (1991). My kind of biology. Annu Rev Microbiol, 45, 1–35CrossRef Google Scholar PubMed

Zehnder, A. J. and Brock, T. D. (1979). Methane formation and methane oxidation by methanogenic bacteria. J Bacteriol, 137, 420–32Google Scholar PubMed

Zengler, K., Richnow, H. H., Rosselló-Mora, R., Michaelis, W. and Widdel, F. (1999). Methane formation from long-chain alkanes by anarobic microorganisms. Nature, 401, 266–9CrossRef Google Scholar

Zhang, X. and Young, L. Y. (1997). Carboxylation as an initial reaction in the anaerobic metabolism of naphthalene and phenanthrene by sulfidogenic consortia. Appl Environ Microbiol, 63, 4759–64Google Scholar PubMed

ZoBell, C. E. (1946). Action of microörganisms on hydrocarbons. Bacteriol Rev, 10, 1–49Google Scholar PubMed

ZoBell, C. E. (1959). Ecology of sulphate reducing bacteria. Prod Mon, 22: 12–29Google Scholar