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1 - Energy metabolism and phylogenetic diversity of sulphate-reducing bacteria



Sulphate-reducing bacteria (SRB) are those prokaryotic microorganisms, both bacteria and archaea, that can use sulphate as the terminal electron acceptor in their energy metabolism, i.e. that are capable of dissimilatory sulphate reduction. Most of the SRB described to date belong to one of the four following phylogenetic lineages (with some examples of genera): (i) the mesophilic δ-proteobacteria with the genera Desulfovibrio, Desulfobacterium, Desulfobacter, and Desulfobulbus; (ii) the thermophilic Gram-negative bacteria with the genus Thermodesulfovibrio; (iii) the Gram-positive bacteria with the genus Desulfotomaculum; and (iv) the Euryarchaeota with the genus Archaeoglobus (Castro et al., 2000). A fifth lineage, the Thermodesulfobiaceae, has been described recently (Mori et al., 2003).

Many SRB are versatile in that they can use electron acceptors other than sulphate for anaerobic respiration. These include elemental sulphur (Bottcher et al., 2005; Finster et al., 1998), fumarate (Tomei et al., 1995), nitrate (Krekeler and Cypionka, 1995), dimethylsulfoxide (Jonkers et al., 1996), Mn(IV) (Myers and Nealson, 1988) and Fe(III) (Lovley et al., 1993; 2004). Some SRB are even capable of aerobic respiration (Dannenberg et al., 1992; Lemos et al., 2001) although this process appears not to sustain growth, and probably provides these organisms only with energy for maintenance. Since dissimilatory sulphate reduction is inhibited under oxic conditions, SRB can grow at the expense of sulphate reduction only in the complete absence of molecular oxygen. SRB are thus considered to be strictly anaerobic microorganisms and are mainly found in sulphate-rich anoxic habitats (Cypionka, 2000; Fareleira et al., 2003; Sass et al., 1992).

Akagi, J. M. (1995). Respiratory sulphate reduction. In Barton, L. L. (ed.), Sulphate-Reducing Bacteria, Vol. 8. New York: Plenum Press. pp. 89–111.
Badziong, W. and Thauer, R. K. (1978). Growth yields and growth rates of Desulfovibrio vulgaris (Marburg) growing on hydrogen plus sulphate and hydrogen plus thiosulphate as the sole energy sources. Arch Microbiol, 117, 209–14
Bak, F. and Cypionka, H. (1987). A novel type of energy-metabolism involving fermentation of inorganic sulfur-compounds. Nature, 326, 891–2
Baron, E. J., Summanen, P., Downes, al. (1989). Bilophila wadsworthia, gen. nov. and sp. nov., a unique gram-negative anaerobic rod recovered from appendicitis specimens and human faeces. J Gen Microbiol, 135, 3405–11
Beijerinck, M. W. (1895). Über Spirillum desulfuricans als Ursache von Sulfatreduktion. Zentralbl Bakteriol Parasitkd Infekt Abt II, 1, 49–59
Bottcher, M. E., Thamdrup, B., Gehre, M. and Theune, A. (2005). S-34/S-32 and O-18/O-16 fractionation during sulfur disproportionation by Desulfobulbus propionicus. Geomicrobiol J, 22, 219–26
Broco, M., Rousset, M., Oliveira, S. and Rodrigues-Pousada, C. (2005). Deletion of flavoredoxin gene in Desulfovibrio gigas reveals its participation in thiosulphate reduction. FEBS Lett, 579, 4803–7
Castro, H., Reddy, K. R. and Ogram, A. (2002). Composition and function of sulphate-reducing prokaryotes in eutrophic and pristine areas of the Florida Everglades. Appl Environ Microbiol, 68, 6129–37
Castro, H. F., Williams, N. H. and Ogram, A. (2000). Phylogeny of sulphate-reducing bacteria. FEMS Microbiol Ecol, 31, 1–9
Conrad, R., Phelps, T. J. and Zeikus, J. G. (1985). Gas metabolism evidence in support of the juxtaposition of hydrogen-producing and methanogenic bacteria in sewage sludge and lake sediments. Appl Environ Microbiol, 50, 595–601
Crane, B. R., Siegel, L. M. and Getzoff, E. D. (1997). Structures of the siroheme- and Fe4S4-containing active center of sulfite reductase in different states of oxidation: Heme activation via reduction-gated exogenous ligand exchange. Biochemistry, 36, 12101–19
Cypionka, H. (1987). Uptake of sulphate, sulfite and thiosulphate by proton-anion symport in Desulfovibrio desulfuricans. Arch Microbiol, 148, 144–9
Cypionka, H. (2000). Oxygen respiration by Desulfovibrio species. Annu Rev Microbiol, 54, 827–48
Dannenberg, S., Kroder, M., Dilling, W. and Cypionka, H. (1992). Oxidation of H2, organic-compounds and inorganic sulfur-compounds coupled to reduction of O2 or nitrate by sulphate-reducing bacteria. Arch Microbiol, 158, 93–9
Dehning, I. and Schink, B. (1989). Malonomonas rubra gen. nov. sp. nov., a microaerotolerant anaerobic bacterium growing by decarboxylation of malonate. Arch Microbiol, 151, 427–33
Dimroth, P. and Cook, G. M. (2004). Bacterial Na+- or H+-coupled ATP synthases operating at low electrochemical potential. Adv Microb Physiol, 49, 175–218
Dolla, A., Pohorelic, B. K. J., Voordouw, J. K. and Voordouw, G. (2000). Deletion of the hmc operon of Desulfovibrio vulgaris subsp vulgaris Hildenborough hampers hydrogen metabolism and low-redox-potential niche establishment. Arch Microbiol, 174, 143–51
Ehrenreich, A. and Widdel, F. (1994). Anaerobic oxidation of ferrous iron by purple bacteria, a new-type of phototrophic metabolism. Appl Environ Microb, 60, 4517–26
Ehrlich, H. L. (1999). Microbes as geologic agents: their role in mineral formation. Geomicrobiol J, 16, 135–53
Fareleira, P., Santos, B. S., Antonio, al. (2003). Response of a strict anaerobe to oxygen: survival strategies in Desulfovibrio gigas. Microbiolog-SGM, 149, 1513–22
Farquhar, J. and Wing, B. A. (2003). Multiple sulfur isotopes and the evolution of the atmosphere. Earth and Planetary Science Letters, 213, 1–13
Finster, K., Liesack, W. and Thamdrup, B. (1998). Elemental sulfur and thiosulphate disproportionation by Desulfocapsa sulfoexigens sp nov, a new anaerobic bacterium isolated from marine surface sediment. Appl Environ Microbiol, 64, 119–25
Fitz, R. M. and Cypionka, H. (1990). Formation of thiosulphate and trithionate during sulfite reduction by washed cells of Desulfovibrio desulfuricans. Arch Microbiol, 154, 400–6
Forzi, L., Koch, J., Guss, A. al. (2005). Assignment of the 4Fe-4S clusters of Ech hydrogenase from Methanosarcina barkeri to individual subunits via the characterization of site-directed mutants. FEBS J, 272, 4741–53
Frederiksen, T. M. and Finster, K. (2003). Sulfite-oxido-reductase is involved in the oxidation of sulfite in Desulfocapsa sulfoexigens during disproportionation of thiosulphate and elemental sulfur. Biodegradation, 14, 189–98
Fricke, W. F., Seedorf, H., Henne, al. (2006). The genome sequence of Methanosphaera stadtmanae reveals why this human intestinal archaeon is restricted to methanol and H2 for methane formation and ATP synthesis. J Bacteriol, 188, 642–58
Friedrich, M. W. (2002). Phylogenetic analysis reveals multiple lateral transfers of adenosine-5′-phosphosulphate reductase genes among sulphate-reducing microorganisms. J Bacteriol, 184, 278–89
Fritz, G., Roth, A., Schiffer, al. (2002). Structure of adenylylsulphate reductase from the hyperthermophilic Archaeoglobus fulgidus at 1.6-A resolution. Proc Natl Acad Sci USA, 99, 1836–41
Galouchko, A. S. and Rozanova, E. P. (1996). Sulfidogenic oxidation of acetate by a syntrophic association of anaerobic mesophilic bacteria. Microbiology, 65, 134–9
Garrity, G. M., Bell, J. A. and Lilburn, T. G. (2003). Taxonomic outline of the procaryotes. Bergey's Manual of Systematic Bacteriology. Second Edition. Release 5.0, New York: Springer Verlag 401 pages. DOI: 10.1007/bergeysoutline200405 ( New York: Springer-Verlag.
Ghiorse, W. C. (1984). Biology of iron- and manganese-depositing bacteria. Annu Rev Microbiol, 38, 515–50
Goenka, A., Voordouw, J. K., Lubitz, W., Gartner, W. and Voordouw, G. (2005). Construction of a NiFe-hydrogenase deletion mutant of Desulfovibrio vulgaris Hildenborough. Biochem Soc Trans, 33, 59–60
Hamilton, W. A. (2003). Microbially influenced corrosion as a model system for the study of metal microbe interactions: a unifying electron transfer hypothesis. Biofouling, 19, 65–76
Hansen, T. A. (1994). Metabolism of sulphate-reducing prokaryotes. Antonie Van Leeuwenhoek International Journal of General and Molecular Microbiology, 66, 165–85
Haveman, S. A., Brunelle, V., Voordouw, J. al. (2003). Gene expression analysis of energy metabolism mutants of Desulfovibrio vulgaris Hildenborough indicates an important role for alcohol dehydrogenase. J Bacteriol, 185, 4345–53
Haynes, T. S., Klemm, D. J., Ruocco, J. J. and Barton, L. L. (1995). Formate dehydrogenase activity in cells and outer-membrane blebs of Desulfovibrio gigas. Anaerobe, 1, 175–82
Hedderich, R. (2004). Energy-converting NiFe hydrogenases from archaea and extremophiles: ancestors of complex I. J Bioenerg Biomembr, 36, 65–75
Hedderich, R., Klimmek, O., Kroeger, al. (1998). Anaerobic respiration with elemental sulfur and with disulfides. FEMS Microbiol Rev, 22, 353–81
Heidelberg, J. F., Seshadri, R., Haveman, S. al. (2004). The genome sequence of the anaerobic, sulphate-reducing bacterium Desulfovibrio vulgaris Hildenborough. Nat Biotechnol, 22, 554–9
Hemme, C. L. and Wall, J. D. (2004). Genomic insights into gene regulation of Desulfovibrio vulgaris Hildenborough. Omics, 8, 43–55
Hines, M. E., Evans, R. S., Sharak Genthner, B. al. (1999). Molecular phylogenetic and biogeochemical studies of sulphate-reducing bacteria in the rhizosphere of Spartina alterniflora. Appl Environ Microbiol, 65, 2209–16
Hoehler, T., Alperin, M. J., Albert, D. B. and Martens, C. S. (2001). Apparent minimum free energy requirements for methanogenic Archaea and sulphate-reducing bacteria in an anoxic marine sediment. FEMS Microbiol Ecol, 38, 33–41
Holmer, M. and Storkholm, P. (2001). Sulphate reduction and sulphur cycling in lake sediments: a review. Freshwater Biol, 46, 431–51
Houwen, F. P., Dijkema, C., Stams, A. J. M. and Zehnder, A. J. B. (1991). Propionate metabolism in anaerobic bacteria – determination of carboxylation reactions with C-13-NMR spectroscopy. Biochim Biophys Acta, 1056, 126–32
Johnston, D. T., Wing, B. A., Farquhar, al. (2005). Active microbial sulfur disproportionation in the Mesoproterozoic. Science, 310, 1477–9
Jonkers, H. M., Maarel, M. J. E. C., Gemerden, H. and Hansen, T. A. (1996). Dimethylsulfoxide reduction by marine sulphate-reducing bacteria. FEMS Microbiol Lett, 136, 283–7
Jorgensen, B. B. (1982). Ecology of the bacteria of the sulfur cycle with special reference to anoxic oxic interface environments. Philo Trans Roy Soc Ser B, 298, 543–61
Keon, R. G. and Voordouw, G. (1996). Identification of the HmcF and topology of the HmcB subunit of the Hmc complex of Desulfovibrio vulgaris. Anaerobe, 2, 231–8
Klenk, H. P., Clayton, R. A., Tomb, J. al. (1997). The complete genome sequence of the hyperthermophilic, sulphate-reducing archaeon Archaeoglobus fulgidus. Nature, 390, 364–70
Kobayashi, K., Morisawa, Y., Ishituka, T. and Ishimoto, M. (1975). Biochemical studies on sulphate-reducing bacteria. 14. Enzyme levels of adenylylsulphate reductase, inorganic pyrophosphatase, sulfite reductase, hydrogenase, and adenosine-triphosphatase in cells grown on sulphate, sulfite, and thiosulphate. J Biochem (Tokyo), 78, 1079–85
Kopp, R. E., Kirschvink, J. L., Hilburn, I. A. and Nash, C. Z. (2005). The paleoproterozoic snowball Earth: a climate disaster triggered by the evolution of oxygenic photosynthesis. Proc Natl Acad Sci USA, 102, 11131–6
Koizumi, Y., Kelly, J. J., Nakagawa, al. (2002). Parallel characterization of anaerobic toluene- and ethylbenzene-degrading microbial consortia by PCR-denaturing gradient gel electrophoresis, RNA-DNA membrane hybridization, and DNA microarray technology. Appl Environ Microbiol, 68, 3215–25
Kramer, M. and Cypionka, H. (1989). Sulphate formation via ATP sulfurylase in thiosulphate-disproportionating and sulfite-disproportionating bacteria. Arch Microbiol, 151, 232–7
Kreke, B. and Cypionka, H. (1992). Proton motive force in fresh-water sulphate-reducing bacteria, and its role in sulphate accumulation in Desulfobulbus propionicus. Arch Microbiol, 158, 183–7
Kreke, B. and Cypionka, H. (1994). Role of sodium-ions for sulphate transport and energy-metabolism in Desulfovibrio salexigens. Arch Microbiol, 161, 55–61
Krekeler, D. and Cypionka, H. (1995). The preferred electron-acceptor of Desulfovibrio desulfuricans Csn. FEMS Microbiol Ecol, 17, 271–7
Kremer, D. R. and Hansen, T. A. (1988). Pathway of propionate degradation in Desulfobulbus propionicus. FEMS Microbiol Lett, 49, 273–7
Larsen, O., Lien, T. and Birkeland, N. K. (1999). Dissimilatory sulfite reductase from Archaeoglobus profundus and Desulfotomaculum thermocisternum: phylogenetic and structural implications from gene sequences. Extremophiles, 3, 63–70
Leaphart, A. B., Friez, M. J. and Lovell, C. R. (2003). Formyltetrahydrofolate synthetase sequences from salt marsh plant roots reveal a diversity of acetogenic bacteria and other bacterial functional groups. Appl Environ Microbiol, 69, 693–6
Le, M. J. and Zinder, S. H. (1988). Isolation and characterization of a thermophilic bacterium which oxidizes acetate in syntrophic association with a methanogen and which grows acetogenically on H2-CO2. Appl Environ Microbiol, 54, 124–9
Lemos, R. S., Gomes, C. M., Santana, al. (2001). The “strict” anaerobe Desulfovibrio gigas contains a membrane-bound oxygen respiratory chain. J Inorg Biochem, 86, 314
Liu, M. Y. and Legall, J. (1990). Purification and characterization of 2 proteins with inorganic pyrophosphatase activity from Desulfovibrio vulgaris – rubrerythrin and a new, highly-active,enzyme. Biochem Biophys Res Commun, 171, 313–18
Lopez-Cortes, A., Bursakov, S., Figueiredo, al. (2005). Purification and preliminary characterization of tetraheme cytochrome c(3) and adenylylsulphate reductase from the peptidolytic sulphate-reducing bacterium Desulfovibrio aminophilus DSM 12254. Bioinorg Chem Appl, 3, 81–91
Lovley, D. R., Holmes, D. E. and Nevin, K. P. (2004). Dissimilatory Fe(III) and Mn(IV) reduction. Adv Microb Physiol, 49, 221–86
Lovley, D. R., Roden, E. E., Phillips, E. J. P. and Woodward, J. C. (1993). Enzymatic iron and uranium reduction by sulphate-reducing bacteria. Mar Geol, 113, 41–53
Malki, S., DeLuca, G., Fardeau, M. al. (1997). Physiological characteristics and growth behavior of single and double hydrogenase mutants of Desulfovibrio fructosovorans. Arch Microbiol, 167, 38–45
Mander, G. J., Duin, E. C., Linder, D., Stetter, K. O. and Hedderich, R. (2002). Purification and characterization of a membrane-bound enzyme complex from the sulphate-reducing archaeon Archaeoglobus fulgidus related to heterodisulfide reductase from methanogenic archaea. Eur J Biochem, 269, 1895–904
Mander, G. J., Pierik, A. J., Huber, H. and Hedderich, R. (2004). Two distinct heterodisulfide reductase-like enzymes in the sulphate-reducing archaeon Archaeoglobus profundus. Eur J Biochem, 271, 1106–16
Matias, P. M., Pereira, I. A. C., Soares, C. M. and Carrondo, M. A. (2005). Sulphate respiration from hydrogen in Desulfovibrio bacteria: a structural biology overview. Prog Biophys Mol Biol, 89, 292–329
McOrist, S., Gebhart, C. J., Boid, R. and Barns, S. M. (1995). Characterization of Lawsonia intracellularis gen. nov., sp. nov., the obligately intracellular bacterium of porcine proliferative enteropathy. Int J Syst Bacteriol, 45, 820–5
Meier, T., Polzer, P., Diederichs, K., Welte, W. and Dimroth, P. (2005). Structure of the rotor ring of F-type Na+-ATPase from Ilyobacter tartaricus. Science, 308, 659–62
Meuer, J., Kuettner, H. C., Zhang, J. K., Hedderich, R. and Metcalf, W. W. (2002). Genetic analysis of the archaeon Methanosarcina barkeri Fusaro reveals a central role for Ech hydrogenase and ferredoxin in methanogenesis and carbon fixation. Proc Natl Acad Sci USA, 99, 5632–7
Molitor, M., Dahl, C., Molitor, al. (1998). A dissimilatory sirohaem-sulfite-reductase-type protein from the hyperthermophilic archaeon Pyrobaculum islandicum. Microbiology-SGM, 144, 529–41
Monster, J., Appel, P. W. U., Thode, H. al. (1979). Sulfur isotope studies in early archaean sediments from Isua, West Greenland – implications for the antiquity of bacterial sulphate reduction. Geochim Cosmochim Acta, 43, 405–13
Mori, K., Kim, H., Kakegawa, T. and Hanada, S. (2003). A novel lineage of sulphate-reducing microorganisms: Thermodesulfobiaceae fam. nov., Thermodesulfobium narugense, gen. nov., sp nov., a new thermophilic isolate from a hot spring. Extremophiles, 7, 283–90
Mueller, V. (2004). An exceptional variability in the motor of archaeal A(1)A(0) ATPases: from multimeric to monomeric rotors comprising 6–13 ion binding sites. J Bioenerg Biomembr, 36, 115–25
Murata, T., Yamato, I., Kakinuma, Y., Leslie, A. G. W. and Walker, J. E. (2005). Structure of the rotor of the V-type Na+-ATPase from Enterococcus hirae. Science, 308, 654–9
Myers, C. R. and Nealson, K. H. (1988). Bacterial manganese reduction and growth with manganese oxide as the sole electron-acceptor. Science, 240, 1319–21
Nealson, K. H. and Saffarini, D. (1994). Iron and manganese in anaerobic respiration – environmental significance, physiology, and regulation. Annu Rev Microbiol, 48, 311–43
Nielsen, P. H., Lee, W., Lewandowski, Z., Morrison, M. and Characklis, W. G. (1993). Corrosion of mild steel in an alternating oxic and anoxic biofilm system. Biofouling, 7, 267–84
Odom, J. M. and Peck, H. D. (1984). Hydrogenase, electron-transfer proteins, and energy coupling in the sulphate-reducing bacteria Desulfovibrio. Annu Rev Microbiol, 38, 551–92
Ogata, M., Arihara, K. and Yagi, T. (1981). D-Lactate dehydrogenase of Desulfovibrio vulgaris. J Biochem (Tokyo), 89, 1423–31
Pankhania, I. P., Spormann, A. M., Hamilton, W. A. and Thauer, R. K. (1988). Lactate conversion to acetate, CO2 and H2 in cell suspensions of Desulfovibrio vulgaris (Marburg): indications for the involvement of an energy driven reaction. Arch Microbiol, 150, 26–31
Paulsen, J., Kröger, A. and Thauer, R. K. (1986). ATP-driven succinate oxidation in the catabolism of Desulfuromonas acetoxidans. Arch Microbiol, 144, 78–83
Peck, H. D. (1993). Bioenergetic strategies of the sulphate-reducing bacteria. In Odom, J. M. and Singleton, J. Rivers (eds.), The Sulphate-Reducing Bacteria: Contemporary Perspectives. New York, London: Springer-Verlag. pp. 41–76.
Pires, R. H., Lourenco, A. I., Morais, al. (2003). A novel membrane-bound respiratory complex from Desulfovibrio desulfuricans ATCC 27774. Biochim Biophys Acta-Bioenergetics, 1605, 67–82
Pohorelic, B. K. J., Voordouw, J. K., Lojou, al. (2002). Effects of deletion of genes encoding Fe-only hydrogenase of Desulfovibrio vulgaris Hildenborough on hydrogen and lactate metabolism. J Bacteriol, 184, 679–86
Rabus, R., Fukui, M., Wilkes, H. and Widdel, F. (1996). Degradative capacities and 16S rRNA-targeted whole-cell hybridization of sulphate-reducing bacteria in an anaerobic enrichment culture utilizing alkylbenzenes from crude oil. Appl Environ Microbiol, 62, 3605–13
Rabus, R., Hansen, T., and Widdel, F. (2001). An evolving electronic resource for the microbiological community. In Dworkin, S., Falkow, M., Rosenberg, E., Schleifer, K.-H. and Stackebrandt, E. (eds.), The Prokaryotes. New York: Springer-Verlag. pp. release 3.3,
Rabus, R., Ruepp, A., Frickey, al. (2004). The genome of Desulfotalea psychrophila, a sulphate-reducing bacterium from permanently cold Arctic sediments. Environ Microbiol, 6, 887–902
Reed, D. W. and Hartzell, P. L. (1999). The Archaeoglobus fulgidus D-lactate dehydrogenase is a Zn2+ flavoprotein. J Bacteriol, 181, 7580–7
Reguera, G., McCarthy, K. D., Mehta, al. (2005). Extracellular electron transfer via microbial nanowires. Nature, 435, 1098–101
Rodrigues, R., Valente, F. M. A., Pereira, I. A. C., Oliveira, S. and Rodrigues-Pousada, C. (2003). A novel membrane-bound Ech NiFe hydrogenase in Desulfovibrio gigas. Biochem Biophys Res Commun, 306, 366–75
Rossi, M., Pollock, W. B. R., Reij, M. al. (1993). The Hmc operon of Desulfovibrio vulgaris Subsp vulgaris Hildenborough encodes a potential transmembrane redox protein complex. J Bacteriol, 175, 4699–711
Sapra, R., Bagramyan, K. and Adams, M. W. W. (2003). A simple energy-conserving system: proton reduction coupled to proton translocation. Proc Natl Acad Sci USA, 100, 7545–50
Sass, H., Steuber, J., Kroder, M., Kroneck, P. M. H. and Cypionka, H. (1992). Formation of thionates by fresh-water and marine strains of sulphate-reducing bacteria. Arch Microbiol, 158, 418–21
Sato, K., Nishina, Y., Setoyama, C., Miura, R. and Shiga, K. (1999). Unusually high standard redox potential of acrylyl-CoA/propionyl-CoA couple among enoyl-CoA/acyl-CoA couples: a reason for the distinct metabolic pathway of propionyl-CoA from longer acyl-CoAs. J Biochem (Tokyo), 126, 668–75
Schiffers, A. and Jorgensen, B. B. (2002). Biogeochemistry of pyrite and iron sulfide oxidation in marine sediments. Geochim Cosmochim Acta, 66, 85–92
Schink, B. (1992). The genus Pelobacter. In Balows, A., Trüper, H. G., Dworkin, M., Harder, W. and Schleifer, K.-H. (eds.), The Prokaryotes. New York: Springer-Verlag. pp. 3393–9.
Schink, B. and Stams, A. J. (2002). Syntrophism among Prokaryotes. In Dworkin, M. (ed.), The Prokaryotes (electronic version). New York: Springer Verlag. pp. 309–35.
Shen, Y. N. and Buick, R. (2004). The antiquity of microbial sulphate reduction. Earth-Science Reviews, 64, 243–72
Shigematsu, T., Tang, Y. Q. Kobayashi, T. et al. (2004). Effect of dilution rate on metabolic pathway shift between aceticlastic and nonaceticlastic methanogenesis in chemostat cultivation. Appl Environ Microbiol, 70, 4048–52
Shima, S. and Thauer, R. K. (2005). Methyl-coenzyme M reductase (MCR) and the anaerobic oxidation of methane (AOM) in methanotrophic archaea. Curr Opin Microbiol, 8, 643–8
Soboh, B., Linder, D. and Hedderich, R. (2002). Purification and catalytic properties of a CO-oxidizing: H2-evolving enzyme complex from Carboxydothermus hydrogenoformans. Eur J Biochem, 269, 5712–21
Sperling, D., Kappler, U., Wynen, A., Dahl, C. and Truper, H. G. (1998). Dissimilatory ATP sulfurylase from the hyperthermophilic sulphate reducer Archaeoglobus fulgidus belongs to the group of homo-oligomeric ATP sulfurylases. FEMS Microbiol Lett, 162, 257–64
Stackebrandt, E. (1995). Origin and evolution of prokaryotes. In Gibbs, A. J., Calisher, C. H. and Garcia-Arenal, F. (eds.), Molecular Basis of Virus Evolution. Cambridge: Cambridge University Press, pp. 224–52.
Stackebrandt, E. (2004). The phylogeny and classification of anaerobic bacteria. In Nakano, M. M. and Zuber, P. (eds.), Strict and Facultative Anaerobes. Medical and Environmental Aspects. Wymondham, UK: Horizon Bioscience. pp. 1–25.
Steger, J. L., Vincent, C., Ballard, J. D. and Krumholz, L. R. (2002). Desulfovibrio sp genes involved in the respiration of sulphate during metabolism of hydrogen and lactate. Appl Environ Microbiol, 68, 1932–7
Taguchi, Y., Sugishima, M. and Fukuyama, K. (2004). Crystal structure of a novel zinc-binding ATP sulfurylase from Thermus thermophilus HB8. Biochemistry, 43, 4111–18
Thamdrup, B. and Canfield, D. E. (1996). Pathways of carbon oxidation in continental margin sediments off central Chile. Limnol Oceanogr, 41, 1629–50
Thamdrup, B., Fossing, H. and Jorgensen, B. B. (1994). Manganese, iron and sulfur cycling in a coastal marine sediment, Aarhus Bay, Denmark. Geochim Cosmochim Acta, 58, 5115–29
Thauer, R. K. (1988). Citric acid cycle, 50 years on: modifications and an alternative pathway in anaerobic bacteria. Eur. J. Biochem., 176, 497–508
Thauer, R. K., Jungermann, K. and Decker, K. (1977). Energy conservation in chemotrophic anaerobic bacteria. Bacteriol. Rev. 41, 100–80
Thauer, R. K. and Kunow, J. (1995). Sulphate reducing Archaea. In Clark, N. (ed.), Biotechnology Handbook. London: Plenum Publishing. pp. 33–48.
Thauer, R. K., Möller-Zinkhan, D. and Spormann, A. (1989). Biochemistry of acetate catabolism in anaerobic chemotrophic bacteria. Annu. Rev. Microbiol., 43, 43–67
Thauer, R. K. and Morris, J. G. (1984). Metabolism of chemotrophic anaerobes: old views and new aspects. In Kelly, D. P. and Carr, N. G. (eds.), The Microbe: 1984 Part II: Prokaryotes and Eukaryotes. Society for General Microbiology Symposium 36. Cambridge: Cambridge University Press. pp. 123–68.
Tomei, F. A., Barton, L. L., Lemanski, C. al. (1995). Transformation of selenate and selenite to elemental selenium by Desulfovibrio desulfuricans. J Ind Microbiol, 14, 329–36
Venter, J. C., Remington, K., Heidelberg, J. al. (2004). Environmental genome shotgun sequencing of the Sargasso Sea. Science, 304, 66–74
Voordouw, G. (2002). Carbon monoxide cycling by Desulfovibrio vulgaris Hildenborough. J Bacteriol, 184, 5903–11
Voordouw, G., Armstrong, S. M., Reimer, M. al. (1996). Characterization of 16S rRNA genes from oil field microbial communities indicates the presence of a variety of sulphate-reducing, fermentative, and sulfide-oxidizing bacteria. Appl Environ Microb, 62, 1623–9
Wächtershäuser, G. (1992). Groundworks for an evolutionary biochemistry: the iron-sulphur world. Prog Biophys Mol Biol, 58, 85–201
Ware, D. A. and Postgate, J. R. (1971). Physiological and chemical properties of a reductant-activated inorganic pyrophosphatase from Desulfovibrio desulfuricans. J Gen Microbiol, 67, 145–60
Weinberg, M. V., Jenney, F. E., Cui, X. Y. and Adams, M. W. W. (2004). Rubrerythrin from the hyperthermophilic archaeon Pyrococcus furiosus is a rubredoxin-dependent, iron-containing peroxidase. J Bacteriol, 186, 7888–95
Widdel, F. and Bak, F. (1992). Gram-negative mesophilic sulphate-reducing bacteria. In Balows, A., Trüper, H. G., Dworkin, M., Harder, W. and Schleifer, K.-H. (eds.), The Prokaryotes. New York: Springer-Verlag. pp. 3352–78.
Widdel, F. and Pfennig, N. (1982). Studies on dissimilatory sulphate-reducing bacteria that decompose fatty-acids. 2. Incomplete oxidation of propionate by Desulfobulbus propionicus Gen-Nov, Sp-Nov. Arch Microbiol, 131, 360–5
Widdel, F. and Pfennig, N. (1984). Dissimilatory sulphate- and sulfur-reducing bacteria. In Krieg, N. R. and Holt, J. G. (eds.), Bergey's Manual of Systematic Bacteriology. Baltimore, MD: Williams and Wilkins. pp. 663–79.
Winogradsky, S. (1890). Recherches sur les organismes de la nitrification. Compt Rendue, 110, 1013–16. In Brock, T. D. (ed.), Milestones in Microbiology: 1556 to 1940. ASM Press: Washington DC (1998). pp. 231–33.
Yagi, T. and Ogata, M. (1996). Catalytic properties of adenylylsulphate reductase from Desulfovibrio vulgaris Miyazaki. Biochimie, 78, 838–46
Zengler, K., Richnow, H. H., Rossello-Mora, R., Michaelis, W. and Widdel, F. (1999). Methane formation from long-chain alkanes by anaerobic microorganisms. Nature, 401, 266–9
Zverlov, V., Klein, M., Lucker, al. (2005). Lateral gene transfer of dissimilatory (bi)sulfite reductase revisited. J Bacteriol, 187, 2203–8