Skip to main content
SpringerLink
Log in

Metabolism of sulfate-reducing prokaryotes

  • Research Articles
  • Published:
Antonie van Leeuwenhoek Aims and scope Submit manuscript

Abstract

Dissimilatory sulfate reduction is carried out by a heterogeneous group of bacteria and archaea that occur in environments with temperatures up to 105 °C. As a group together they have the capacity to metabolize a wide variety of compounds ranging from hydrogen via typical organic fermentation products to hexadecane, toluene, and several types of substituted aromatics. Without exception all sulfate reducers activate sulfate to APS; the natural electron donor(s) for the ensuing APS reductase reaction is not known. The same is true for the reduction of the product bisulfite; in addition there is still some uncertainty as to whether the pathway to sulfide is a direct six-electron reduction of bisulfite or whether it involves trithionate and thiosulfate as intermediates. The study of the degradation pathways of organic substrates by sulfate-reducing prokaryotes has led to the discovery of novel non-cyclic pathways for the oxidation of the acetyl moiety of acetyl-CoA to CO2. The most detailed knowledge is available on the metabolism ofDesulfovibrio strains, both on the pathways and enzymes involved in substrate degradation and on electron transfer components and terminal reductases. Problems encountered in elucidating the flow of reducing equivalents and energy transduction are the cytoplasmic localization of the terminal reductases and uncertainties about the electron donors for the reactions catalyzed by these enzymes. New developments in the study of the metabolism of sulfate-reducing bacteria and archaea are reviewed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Abdollahi H & Wimpenny JWT (1990) Effects of oxygen on the growth ofDesulfovibrio desulfuricans. J. Gen. Microbiol. 136: 1025–1030

    Google Scholar 

  • Aeckersberg F, Bak F & Widdel F (1991) Anaerobic oxidation of saturated hydrocarbons to CO2 by a new type of sulfate-reducing bacterium. Arch. Microbiol. 156: 5–14

    Google Scholar 

  • Aeckersberg F & Widdel F (1993) First investigation into the mechanism of anaerobic alkane activation. Bioengineering 9: 26

    Google Scholar 

  • Altenschmidt U & Fuchs G (1991) Anaerobic degradation of toluene in denitrifyingPseudomonas sp.: indication of toluene methylhydroxylation and benzoyl-CoA as central aromatic intermediate. Arch. Microbiol. 156: 152–158

    Google Scholar 

  • Arendsen AF, Verhagen MFJM, Wolbert RBG, Pierik AJ, Stams AJM, Jetten MSM & Hagen WR (1993) The dissimilatory sulfite reductase fromDesulfosarcina variabilis is a desulforubidin containing uncoupled metalated sirohemes andS=9/2 iron-sulfur clusters. Biochemistry 32: 10323–10330

    Google Scholar 

  • Badziong W & Thauer RK (1978) Growth yields and growth rates ofDesulfovibrio vulgaris (Marburg) growing on hydrogen plus sulfate and hydrogen plus thiosulfate as sole energy sources. Arch. Microbiol. 117: 209–214

    Google Scholar 

  • Badziong W & Thauer RK (1980) Vectorial electron transport inDesulfovibrio vulgaris (Marburg) growing on hydrogen and sulfate as sole energy source. Arch. Microbiol. 125: 167–184

    Google Scholar 

  • Barata B, Liang J, LeGall J, Moura JJG & Hanh Huynh B (1992) Mössbauer study of the native, reduced and substrate-reactedDesulfovibrio gigas aldehyde oxido-reductase. Eur. J. Biochem. 204: 773–778

    Google Scholar 

  • Barton LL, LeGall J, Odom JM & Peck HD Jr (1983) Energy coupling to nitrite respiration in the sulfate-reducing bacteriumDesulfovibrio gigas. J. Bacteriol. 153: 867–871

    Google Scholar 

  • Boopathy R & Daniels L (1991) Isolation and characterization of a furfural degrading sulfate-reducing bacterium form an anaerobic digester. Curr. Microbiol. 23: 327–332

    Google Scholar 

  • Boopathy R & Kulpa CF (1992) Trinitrotoluene as a sole nitrogen source for a sulfate-reducing bacteriumDesulfovibrio sp. (B strain) isolated from an anaerobic digester. Curr. Microbiol. 25: 235–241

    Google Scholar 

  • Boopathy R & Kulpa CF (1993) Nitroaromatic compounds serve as nitrogen source forDesulfovibrio sp. (B strain). Can. J. Microbiol. 39: 430–433

    Google Scholar 

  • Boopathy R, Kulpa CF & Wilson M (1993) Metabolism of 2,4,6-trinitrotoluene (TNT) byDesulfovibrio sp. (B strain). Appl. Microbiol. Biotechnol. 39: 270–275

    Google Scholar 

  • Bramlett RN & Peck HD Jr (1975) Some physical and kinetic properties of adenylyl sulfate reductase fromDesulfovibrio vulgaris. J. Biol. Chem. 250: 2979–2986

    Google Scholar 

  • Brandis-Heep A, Gebhardt NA, Thauer RK, Widdel F & Pfennig N (1983) Anaerobic acetate oxidation to CO2 byDesulfobacter postgatei. 1. Demonstration of all enzymes required for the operation of the citric acid cycle. Arch. Microbiol. 136: 222–229

    Google Scholar 

  • Brittain T, Blackmore R, Greenwood C & Thomson AJ (1992) Bacterial nitrite-reducing enzymes. Eur. J. Biochem. 209: 793–802

    Google Scholar 

  • Burggraf S, Jannasch HW, Nicolaus B & Stetter KO (1990)Archaeoglobus profundus sp. nov., represents a new species within the sulfate-reducing archaebacteria. Syst. Appl. Microbiol. 13: 14–28

    Google Scholar 

  • Buschhorn H, Dürre P & Gottschalk G (1992) Purification and properties of the coenzyme A-linked acetaldehyde dehydrogenase ofAcetobacterium woodii. Arch. Microbiol. 158: 132–138

    Google Scholar 

  • Bystrykh LV, Vonck J, van Bruggen EFJ, Van Beeumen J, Samyn B, Govorukhina NI, Arfman N, Duine JA & Dijkuizen L (1993) Electron microscopic analysis of novel NADP(H-containing methanol:N,N′-dimethyl-4-nitroaniline oxidoreductase from the gram-positive methylotrophic bacteriaAmycolatopsis methanolica andMycobacterium gastri MB19. J. Bacteriol. 175: 1814–1822

    Google Scholar 

  • Calhoun MW & Gennis RB (1993) Demonstration of separate genetic loci encoding distinct membrane-bound respiratory NADH dehydrogenases inEscherichia coli. J. Bacteriol. 175: 3013–3019

    Google Scholar 

  • Canfield DE & DesMarais DJ (1991) Aerobic sulfate reduction. Science 251: 1471–1473

    Google Scholar 

  • Caumette P, Cohen Y & Matheron R (1991) Isolation and characterization ofDesulfovibrio halophilus sp. nov., a halophilic sulfate-reducing bacterium isolated from Solar Lake (Sinai). System. Appl. Microbiol. 14: 33–38

    Google Scholar 

  • Chen L, Liu MY & LeGall J (1993a) Isolation and characterization of flavoredoxin, a new flavoprotein that permitsin vitro reconstitution of an electron transfer chain from molecular hydrogen to sulfite reduction in the bacteriumDesulfovibrio gigas. Arch. Biochem. Biophys. 303: 44–50

    Google Scholar 

  • Chen L, Liu MY, LeGall J, Fareleira P, Santos H, & Xavier A (1993b) Rubredoxin oxidase, a new flavo-hemo-protein, is the site of oxygen reduction to water by the “strict anaerobe”Desulfovibrio gigas. Biochem. Biophys. Res. Comm. 193: 100–105

    Google Scholar 

  • Chen L, Liu MY, LeGall J, Fareleira P, Santos H, & Xavier A (1993c) Purification and characterization of an NADH-rubredoxin oxidoreductase involved in the utilization of oxygen byDesulfovibrio gigas. Eur. J. Biochem. 216: 443–448

    Google Scholar 

  • Choi S-C & Bartha R (1993) Cobalamin-mediated mercury methylation byDesulfovibrio desulfuricans LS. Appl. Environ. Microbiol. 59: 290–295

    Google Scholar 

  • Coleman ML, Hedrick DB, Lovley DR, White DC, & Pye K (1993) Reduction of Fe(III) in sediments by sulphate-reducing bacteria. Nature 361: 436–438

    Google Scholar 

  • Compeau GC & Bartha R (1985) Sulfate-reducing bacteria: principal methylators of mercury in anoxic estuarine sediment. Appl. Environ. Microbiol. 50: 498–502

    Google Scholar 

  • Cypionka H (1987) Uptake of sulfate, sulfite and thiosulfate by proton-anion symport inDesulfovibrio desulfuricans. Arch. Microbiol. 148: 144–149

    Google Scholar 

  • Cypionka H (1989) Characterization of sulfate transport inDesulfovibrio desulfuricans. Arch. Microbiol. 152: 237–243

    Google Scholar 

  • Cypionka H (1991) Der Transport von Sulfat bei sulfatreduzierenden Bakterien. BIOforum 14: 207–210

    Google Scholar 

  • Cypionka H, Widdel F & Pfennig N (1985) Survival of sulfate-reducing bacteria after oxygen stress, and growth in sulfate-free oxygen-sulfide gradients. FEMS Microbiol. Ecol. 31: 39–45

    Google Scholar 

  • Dahl C, Kredich NM, Deutzmann R & Trüper HG (1993) Dissimilatory sulphite reductase fromArchaeoglobus fulgidus: physicochemical properties of the enzyme and cloning, sequencing and analysis of the reductase genes. J. Gen. Microbiol. 139: 1817–1828

    Google Scholar 

  • Dannenberg S, Kroder M, Dilling W & Cypionka H (1992) Oxidation of H2, organic compounds and inorganic sulfur compounds coupled to the reduction of O2 or nitrate by sulfate-reducing bacteria. Arch. Microbiol. 158: 93–99

    Google Scholar 

  • Darwin A, Hussain H, Griffiths L, Grove J, Sambongi Y, Busby S & Cole J (1993) Regulation and sequence of the structural gene for cytochromec 552 fromEscherichia coli: not a hexahaem but a 50 kDa tetrahaem nitrite reductase. Mol. Microbiol. 9: 1255–1265

    Google Scholar 

  • DeWeerd KA, Mandelco L, Tanner RS, Woese CR & Suflita JM (1990)Desulfomonile tiedjei gen. nov. and sp. nov., a novel anaerobic, dehalogenating, sulfate-reducing bacterium. Arch. Microbiol. 154: 23–30

    Google Scholar 

  • Devereux R & Stahl DA (1993) Phylogeny of sulfate-reducing bacteria and a perspective for analyzing their natural communities. In: Odom JM & Singleton R (Eds) The sulfate-reducing bacteria: contemporary perspectives (pp 131–161). Springer-Verlag, New York

    Google Scholar 

  • Dilling W & Cypionka H (1990) Aerobic respiration in sulfate-reducing bacteria. FEMS Microbiol. Lett. 71: 123–128

    Google Scholar 

  • Dolfing J, Zeyer P, Binder-Eicher P & Schwarzenbach RP (1990) Isolation and characterisation of a bacterium that mineralizes toluene in the absence of molecular oxygen. Arch. Microbiol. 154: 336–341

    Google Scholar 

  • Drake HL & Akagi JM (1977a) Bisulfite reductase ofDesulfovibrio vulgaris: explanation for product formation. J. Bacteriol. 132: 139–143

    Google Scholar 

  • Drake HL & Akagi JM (1977b) Characterization of a novel thiosulfate-forming enzyme isolated fromDesulfovibrio vulgaris. J. Bacteriol. 132: 132–138

    Google Scholar 

  • Esnault G, Caumette P & Garcia J-L (1988) Characterization ofDesulfovibrio giganteus sp. nov., a sulfate-reducing bacterium isolated from a brackish coastal lagoon. Syst. Appl. Micriobiol. 10: 147–151

    Google Scholar 

  • Evans PJ, Mang DT, Kim KS & Young LY (1991) Anaerobic degradation of toluene by a denitrifying bacterium. Appl. Environ. Microbiol. 57: 1139–1145

    Google Scholar 

  • Fauque G, LeGall J & Barton L (1991) Sulfate-reducing and sulfur-reducing bacteria. In: Shively JM & Barton LL (Eds) Variations in autotrophic life (pp 271–337). Academic Press, London

    Google Scholar 

  • Fauque G, Peck HD Jr, Moura JJG, Huynh BH, Berlier Y, Dervartanian DV, Texeira M, Przybyla AE, Lespinat PA, Moura I, & LeGall J (1988) The three classes of hydrogenases from sulfate-reducing bacteria of the genusDesulfovibrio. FEMS Microbiol. Rev. 54: 299–344

    Google Scholar 

  • Fitz R & Cypionka H (1989) A study on electron transport-driven proton translocation inDesulfovibrio desulfuricans. Arch. Microbiol. 152: 369–376

    Google Scholar 

  • Fitz R & Cypionka H (1990) Formation of thiosulfate and thrithionate during sulfite erduction by washed cells ofDesulfovibrio desulfuricans. Arch. Microbiol. 154: 400–406

    Google Scholar 

  • Fitz R & Cypionka H (1991) Generation of a proton gradient inDesulfovibrio vulgaris. Arch. Microbiol. 155: 444–448

    Google Scholar 

  • Folkerts M, Ney U, Kneifel H, Stackebrandt E, Witte EG, Förstel H, Schoberth SM & Sahm H (1989)Desulfovibrio furfuralis sp. nov., a furfural degrading strictly anaerobic bacterium. Syst. Appl. Microbiol. 11: 161–169

    Google Scholar 

  • Fründ C & Cohen Y (1992) Diurnal cycles of sulfate reduction under anoxic conditions in cyanobacterial mats. Appl. Environ. Microbiol. 58: 70–77

    Google Scholar 

  • Gebhardt NA, Linder D & Thauer RK (1983) Anaerobic acetate oxidation to CO2 byDesulfobacter postgatei. 2. Evidence from14C-labelling studies for the operation of the citric acid cycle. Arch. Microbiol. 136: 230–233

    Google Scholar 

  • Gibson GR, Macfarlane GT & Cummings JH (1988) Occurrence of sulphate-reducing bacteria in human faeces and the relationship of dissimilatory sulphate reduction to methanogenesis in the large gut. J. Appl. Bacteriol. 65: 103–111

    Google Scholar 

  • Gibson GR, Macfarlane S & Macfarlane GT (1993) Metabolic interactions involving sulphate-reducing and methanogenic bacteria in the human large intestine. FEMS Microbiol. Ecol. 12: 117–125

    Google Scholar 

  • Gorontzy T, Küver J & Blotevogel K-H (1993) Microbial transformation of nitroaromatic compounds under anaerobic conditions. J. Gen. Microbiol. 139: 12331–1336

    Google Scholar 

  • Hamilton WA (1985) Sulphate-reducing bacteria and anaerobic corrosion. Ann. Rev. Microbiol. 39: 195–217

    Google Scholar 

  • Hammack RW & Edenborn HM (1992) The removal of nickel from mine waters using bacterial sulfate reduction. Appl. Microbiol. Biotechnol. 37: 674–678

    Google Scholar 

  • Hansen TA (1993) Carbon metabolism of sulfate-reducing bacteria. In: Odom JM & Singleton R (Eds) The sulfate-reducing bacteria: contemporary perspectives (pp 21–40). Springer-Verlag, New York

    Google Scholar 

  • Hardy JA & Hamilton WA (1981) The oxygen tolerance of sulfate-reducing bacteria isolated from North Sea waters. Curr. Microbiol. 6: 259–262

    Google Scholar 

  • Hatchikian EC (1970) Menadione reductase fromDesulfovibrio gigas. Biochim. Biophys. Acta 212: 353–355

    Google Scholar 

  • Hatchikian EC, LeGall J & Bell GR (1977) In: Michelson AM, McCard JM & Fridovich I (Eds) Superoxide and superoxide dismutase (pp 159–172). Academic Press, London

    Google Scholar 

  • Hatchikian EC & Zeikus JG (1983) Characterization of a new type of dissimilatory sulfite reductase present inThermodesulfobacterium commune. J. Bacteriol. 153: 1211–1220

    Google Scholar 

  • Hayward HR (1960) Anaerobic degradation of choline. III Acetaldehyde as an intermediate in the fermentation of choline by extracts ofVibrio cholinicus. J. Biol. Chem. 235: 3592–3596

    Google Scholar 

  • Heijthuijsen JHFG & Hansen TA (1989) Anaerobic degradation of betaine by marineDesulfobacterium strains. Arch. Microbiol. 152: 393–396

    Google Scholar 

  • Hensgens CMH, Vonck J, Van Beeumen J, van Bruggen EFJ & Hansen TA (1993) Purification and characterization of an oxygenlabile, NAD-dependent alcohol dehydrogenase fromDesulfovibrio gigas. J. Bacteriol. 175: 2859–2863

    Google Scholar 

  • Hensgens CMH, Nienhuis-Kuiper HE & Hansen TA (1994) Effect of tungstate on the growth ofDesulfovibrio gigas NCIMB 9332 and other sulfate-reducing bacteria with ethanol as a substrate. Arch. Microbiol. (in press)

  • Hochstein LI, Tomlinson GA (1988) The enzymes associated with denitrification. Ann. Rev. Microbiol. 40: 79–105

    Google Scholar 

  • Ingvorsen K & Jørgensen BB (1984) Kinetics of sulfate uptake by freshwater and marines species ofDesulfovibrio. Arch. Microbiol. 139: 61–66

    Google Scholar 

  • Jones HE & Chambers LA (1975) Localized intracellular polyphosphate formation byDesulfovibrio gigas. J. Gen. Microbiol. 89: 67–72

    Google Scholar 

  • Jørgensen BB & Bak F (1991) Pathways and microbiology of thiosulfate transformations and sulfate reduction in a marine sediment (Kattegat, Denmark). Appl. Environ. Microbiol. 57: 847–856

    Google Scholar 

  • Jørgensen BB, Isaksen MF & Jannasch HW (1992) Bacterial sulfate reduction above 100°C in deep-sea hydrothermal vent sediments. Science 258: 1756–1757

    Google Scholar 

  • Jüttner F & Henatsch JJ (1986) Anoxic hypolimnion is a significant source of biogenic toluene. Nature 323: 797–798

    Google Scholar 

  • Kiene RP, Oremland RS, Catena A, Miller LG & Capone DG (1986) Metabolism of reduced, methylated sulfur compounds in anaerobic sediments and a pure culture of an estuarine methanogen. Appl. Environ. Microbiol. 52: 1037–1045

    Google Scholar 

  • Kim JH & Akagi JM (1985) Characterization of a trithionate reductase system fromDesulfovibrio vulgaris. J. Bacteriol. 163: 472–475

    Google Scholar 

  • Klemps R, Cypionka H & Pfennig N (1985) Growth with hydrogen, and further physiological characteristics ofDesulfotomaculum species. Arch. Microbiol. 143: 203–208

    Google Scholar 

  • Krämer M & Cypionka H (1989) Sulfate formation via ATP sulfurylase in thiosulfate- and sulfite-disproportionating bacteria. Arch. Microbiol. 151: 232–237

    Google Scholar 

  • Kreke B & Cypionka H (1992) Protonmotive force in freshwater sulfate-reducing bacteria, and its role in sulfate accumulation inDesulfobulbus propionicus. Arch. Microbiol. 158: 183–187

    Google Scholar 

  • Kreke B & Cypionka H (1994) Role of sodium ions for sulfate transport and energy metabolism inDesulfovibrio salexigens. Arch. Microbiol. 161: 55–61

    Google Scholar 

  • Kremer DR & Hansen TA (1987) Glycerol and dihydroxyacetone dissimilation inDesulfovibrio strains. Arch. Microbiol. 147: 249–256

    Google Scholar 

  • Kremer DR & Hansen TA (1988) Pathway of propionate degradation inDesulfobulbus propionicus. FEMS Microbiol. Lett. 49: 273–277

    Google Scholar 

  • Kremer DR & Hansen TA (1989) Demonstration of HOQNO and antimycin A sensitive coupling of NADH oxidation and APS and sulfite reduction in a marineDesulfovibrio strain. FEMS Microbiol. Lett. 49: 273–277

    Google Scholar 

  • Kremer DR, Nienhuis-Kuiper HE & Hansen TA (1988a) Ethanol dissimilation inDesulfovibrio. Arch. Microbiol. 150: 552–557

    Google Scholar 

  • Kremer DR, Veenhuis M, Fauque G, Peck HD Jr, LeGall J, Lampreia J, Moura JJG & Hansen TA (1988b) Immunocytochemical localization of APS reductase and bisulfite reductase in threeDesulfovibrio species. Arch. Microbiol. 150: 296–301

    Google Scholar 

  • Kremer DR, Nienhuis-Kuiper HE, Timmer CJ & Hansen TA (1989) Catabolism of malate and related dicarboxylic acids in variousDesulfovibrio strains and the involvement of an oxygen-labile NADPH dehydrogenase. Arch. Microbiol. 151: 34–39

    Google Scholar 

  • Kuever J, Kulmer J, Janssen S, Fischer U & Blotevogel K-H (1993) Isolation and characterization of a new spore-forming sulfate-reducing bacterium growing by complete oxidation of catechol. Arch. Microbiol. 159: 282–288

    Google Scholar 

  • Kunow J, Schwörer B, Stetter KO & Thauer RK (1993) A F420-dependent NADP reductase in the extremely thermophilic sulfate-reducingArchaeoglobusfulgidus. Arch. Microbiol. 160: 199–205

    Google Scholar 

  • Lampreia J, Moura I, Teixeira M, Peck HD Jr, LeGall J, Huynh B & Moura JJG (1990) The active centers of adenylylsulfate reductase fromDesulfovibrio gigas. Characterization and spectroscopic studies. Eur. J. Biochem. 188: 653–664

    Google Scholar 

  • LeGall J, Prickril BC, Moura I, Xavier AV, Moura JJG & Hyunh BH (1988) Isolation and characterization of rubrerythrin, a non-heme iron protein fromDesulfovibrio vulgaris that contains rubredoxin centers and a hemerythrin-like binuclear iron cluster. Biochemistry 27: 1636–1642

    Google Scholar 

  • Lin ECC & Iuchi S (1991) Regulation of gene expression in fermentative and respiratory systems inEscherichia coli and related bacteria. Ann. Rev. Genet. 25: 361–387

    Google Scholar 

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

    Google Scholar 

  • Lovley DR & Lonergan DJ (1990) Anaerobic oxidation of toluene, phenol, andp-cresol by the dissimilatory iron-reducing organism GS-15. Appl. Environ. Microbiol. 56: 1858–1864

    Google Scholar 

  • Lovley DR, Widman PK, Woodward JC & Phillips EJP (1993) Reduction of uranium by cytochromec 3 ofDesulfovibrio vulgaris. Appl. Environ. Microbiol. 59: 3572–3576

    Google Scholar 

  • Marschall C, Frenzel P & Cypionka H (1993) Influence of oxygen on sulfate reduction and growth of sulfate-reducing bacteria. Arch. Microbiol. 159: 168–173

    Google Scholar 

  • Meinhardt SW, Wang D-C, Hon-nami K, Yagi T, Oshima T & Ohnishi T (1990) Studies on the NADH-menaquinone oxidoreductase segment of the respiratory chain inThermus thermophilus HB-8. J. Biol. Chem. 265: 1360–1368

    Google Scholar 

  • Möller D, Schauder R, Fuchs G & Thauer RK (1987) Acetate oxidation to CO2 via a citric acid cycle involving an ATP-citrate lyase: a mechanism for the synthesis of ATP via substrate level phosphorylation inDesulfobacter postgatei growing on acetate and sulfate. Arch. Microbiol. 148: 202–207

    Google Scholar 

  • Möller-Zinkhan D & Thauer RK (1988) Membrane-bound NADPH dehydrogenase-and ferredoxin: NADP oxidoreductase activity involved in electron transport during acetate oxidation to CO2 inDesulfobacter postgatei. Arch. Microbiol. 150: 145–154

    Google Scholar 

  • Möller-Zinkhan D & Thauer RK (1990) Anaerobic lactate oxidation to 3 CO2 byArchaeoglobus fulgidus via the carbon monoxide dehydrogenase pathway: demonstration of the acetyl-CoA carbon-carbon eleavage reaction in cell extracts. Arch. Microbiol. 153: 215–218

    Google Scholar 

  • Moura I, Tavares P, Moura JJG, Ravi N, Huynh BH, Liu MY & LeGall J (1990) Purification and characterization of desulfoferrodoxin. J. Biol. Chem. 265: 21596–21602

    Google Scholar 

  • Moura JJG, Costa C, Liu M-Y, Moura I & LeGall J (1991) Structural and functional approach toward a classification of the complex cytochromec system found in sulfate-reducing bacteria. Biochim. Biophys. Acta 1058: 61–66

    Google Scholar 

  • Nanninga HJ & Gottschal JC (1987) Properties ofDesulfovibrio carbinolicus sp. nov. and other sulfate-reducing bacteria isolated form an anaerobic-purification plant. Appl. Environ. Microbiol. 53: 802–809

    Google Scholar 

  • Nivière V, Bernadac A, Forget N, Fernandez VM & Hatchikian CE (1991) Localization of hydrogenase inDesulfovibrio gigas. Arch. Microbiol. 155: 579–586

    Google Scholar 

  • Odom JM & Peck HD Jr (1981) Hydrogen cycling as a general mechanism for energy coupling in the sulfate reducing bacteria,Desulfovibrio sp. FEMS Microbiol. Lett. 12: 47–50

    Google Scholar 

  • Ohnishi T (1993) NADH-quinone oxidoreductase, the most complex complex. J. Bioenerg. Biomembr. 25: 325–329

    Google Scholar 

  • Okabe S, Nielsen PH & Characklis WG (1992) Factors effecting microbial sulfate reduction byDesulfovibrio desulfuricans in continuous culture: limiting nutrients and sulfide concentration. Biotechnol. Bioeng. 40: 725–734

    Google Scholar 

  • Ollivier B, Hatchikian CE, Prensier G, Guezennec J & Garcia JL (1991)Desulfohalobium retbaense gen. nov., sp. nov., a halophilic sulfate-reducing bacterium from sediments of a hypersaline lake in Senegal. Int. J. Syst. Bacteriol. 41: 74–81

    Google Scholar 

  • Oppenberg B & Schink B (1990) Anaerobic degradation of 1,3-propanediol by sulfate-reducing and by fermenting bacteria. Ant. v. Leeuwenhoek 57: 205–213

    Google Scholar 

  • Oremland RS, Culbertson CW & Winfrey MR (1991) Methylmercury decomposition in sediments and bacterial cultures: involvement of methanogens and sulfate reducers in oxidative demethylation. Appl. Environ. Microbiol. 57: 130–137

    Google Scholar 

  • Ouatarra AS, Cuzin N, Traore AS & Garcia JL (1992) Anaerobic degradation of 1,2-propanediol by a newDesulfovibrio strain andD. alcoholovorans. Arch. Microbiol. 158: 218–225

    Google Scholar 

  • Pankhania IP, Spormann AM, Hamilton WA & Thauer RK (1988) Lactate conversion to acetate, CO2, and H2 in cell suspensions ofDesulfovibrio vulgaris (Marburg): indications for the involvement of an energy driven reaction. Arch. Microbiol. 150: 26–31

    Google Scholar 

  • Peck HD Jr (1993) Bioenergetic strategies of the sulfate-reducing bacteria. In: Odom JM & Singleton R (Eds) The sulfate-reducing bacteria: contemporary perspectives (pp 41–76). Springer-Verlag, New York

    Google Scholar 

  • Peck HD Jr, Le Gall J, Lespinat PA, Berlier Y & Fauque G (1987) A direct demonstration of hydrogen cycling employing membraneinlet mass spectrometry. FEMS Microbiol. Lett. 40: 295–299

    Google Scholar 

  • Pierik AJ, Duyvis MG, van Helvoort JMLM, Wolbert RBG & Hagen WR (1992) The third subunit of desulfoviridin-typedissimilatory sulfite reductases. Eur. J. Biochem. 205: 111–115

    Google Scholar 

  • Platen H, Temmes A & Schink B (1990) Anaerobic degradation of acetone byDesulfococcus biacutus spec. nov. Arch. Microbiol. 154: 355–361

    Google Scholar 

  • Pochart P, Doré J, Lémann F, Goderel I & Rambaud JC (1992) Interrelations between populations of methanogenic archaea and sulfate-reducing bacteria in the human colon. FEMS Microbiol. Lett. 98: 225–228

    Google Scholar 

  • Pollock WBR, Loutfi M, Bruschi M, Rapp-Giles BJ & Voordouw G (1991) Cloning, sequencing, and expression of the gene encoding the high-molecular-weight cytochromec fromDesulfovibrio vulgaris Hildenborough. J. Bacteriol. 173: 220–228

    Google Scholar 

  • Postgate JR (1979) The sulphate-reducing bacteria. Cambridge University Press, Cambridge

    Google Scholar 

  • Postgate JR, Kent HM, Robson RL & Cheshyre JA (1984) The genomes ofDesulfovibrio gigas andD. vulgaris. J. Gen. Microbiol. 130: 1597–1601

    Google Scholar 

  • Preuss A, Fimpel J & Diekert G (1993) Anaerobic transformation of 2,4,6-trinitrotoluene (TNT). Arch. Microbiol. 159: 345–353

    Google Scholar 

  • Prickril BC, Kurtz DM, LeGall J & Voordouw G (1991) Cloning and sequencing of the gene for rubrerythrin fromDesulfovibrio vulgaris (Hildenborough). Biochemistry 30: 11118–11123

    Google Scholar 

  • Qatibi AI, Cayol JL & Garcia JL (1991a) Glycerol and propanediols degradation byDesulfovibrio alcoholovorans in pure culture in the presence of sulfate, or in syntrophic association withMethanospirillum hungatei. FEMS Microbiol Ecol 85: 233–240

    Google Scholar 

  • Qatibi AI, Nivière V & Garcia JL (1991b)Desulfovibrio alcoholovorans sp. nov., a sulfate-reducing bacterium able to grow on glycerol, 1,2- and 1,3-propanediol. Arch. Microbiol. 155: 143–148

    Google Scholar 

  • Rabus R, Nordhaus R, Ludwig W & Widdel F (1993) Complete oxidation of toluene under strictly anoxic conditions by a new sulfate-reducing bacterium. Appl. Environ. Microbiol. 59: 1444–1451

    Google Scholar 

  • Reis MAM, Almeida JS, Lemos PC & Carrondo MJT (1992) Effect of hydrogen sulfide on growth of sulfate reducing bacteria. Biotechnol. Bioeng. 40: 593–600

    Google Scholar 

  • Rohde M, Fürstenau U, Mayer F, Przybyla AE, Peck HD, LeGall J, Choi ES & Menon NK (1990) Localization of membrane-associated (NiFe) and (NiFeSe) hydrogenases ofDesulfovibrio vulgaris using immunoelectron microscropic procedures. Eur. J. Biochem. 191: 389–396

    Google Scholar 

  • Romão MJ, Barata BAS, Archer M, Lobeck K, Moura I, Carrondo MA, LeGall J, Lottspeich F, Huber R & Moura JG (1993) Subunit composition, crystallization and preliminary crystallographic studies of theDesulfovibrio gigas aldehyde oxidoreductase containing molybdenum and [2Fe-2S] centers. Eur. J. Biochem. 215: 729–732

    Google Scholar 

  • Romero C & Jüttner F (1993) Isolation of a new toluene producingClostridium from anoxic sediments of a freshwater lake. Abstracts XI International Symposium on Environmental Biogeochemistry, Salamanca

  • Rossi M, Pollock BR, Reij MW, Keon RG, Fu R & Voordouw G (1993) Thehmc operon ofDesulfovibrio vulgaris subsp.vulgaris Hildenborough encodes a potential transmembrane redox protein complex. J. Bacteriol. 175: 4699–4711

    Google Scholar 

  • Rousset M, Dermoun Z, Chippaux M & Belaich JP (1991) Marker exhange mutagenesis of thehydN genes inDesulfovibrio fructosovorans. Mol. Microbiol. 5: 1735–1740

    Google Scholar 

  • Samain E, Patil DS, DerVartanian DV, Albagnac G & LeGall J (1985) Isolation of succinate dehydrogenase fromDesulfobulbus elongatus, a propionate oxidizing, sulfate reducing bacterium. FEBS Lett. 216: 140–144

    Google Scholar 

  • Santos H, Fareleira P, Pedregal C, LeGall J & Xavier AV (1991)In vivo 31P-NMR studies ofDesulfovibrio species. Detection of a novel phosphorus-containing compound. Eur. J. Biochem. 201: 283–287

    Google Scholar 

  • Sass H, Steuber J, Kroder M, Kroneck PMH & Cypionka H (1992) Formation of thionates by freshwater and marine strains of sulfate-reducing bacteria. Arch. Microbiol. 158: 418–421

    Google Scholar 

  • Schauder R, Eikmanns B, Thauer RK, Widdel F & Fuchs G (1986) Acetate oxidation to CO2 in anaerobic bacteria via a novel pathway not involving reactions of the citric acid cycle. Arch. Microbiol. 145: 162–172

    Google Scholar 

  • Schauder R, Preuss A, Jetten M & Fuchs G (1989) Oxidative and reductive acetyl CoA/carbon monoxide dehydrogenase pathway inDesulfobacterium autotrophicum. 2. Demonstration of the enzymes of the pathway and comparison of carbon monoxide dehydrogenase. Arch. Microbiol. 151: 84–89

    Google Scholar 

  • Schmitz RA, Linder D, Stetter KO & Thauer RK (1991)N 5,N 10-methylenetetrathydromethanopterin reductase (coenzyme F420-dependent) and formylmethanofuran dehydrogenase from the hyperthermophileArchaeoglobusfulgidus. Arch. Microbiol. 156: 427–434

    Google Scholar 

  • Schnell S, Bak F & Pfennig N (1989) Anaerobic degradation of aniline and dihydroxybenzenes by newly isolated sulfate-reducing bacteria and description ofDesulfobacterium anilini. Arch. Microbiol. 152: 556–563

    Google Scholar 

  • Schnell S & Schink B (1991) Anaerobic aniline degradation via reductive deamination of 4-aminobenzoyl-CoA inDesulfobacterium anilini. Arch. Microbiol. 155: 183–190

    Google Scholar 

  • Schnell S & Schink B (1992) Anaerobic degradation of 3-aminobenzoate by a newly isolated sulfate reducer and a methanogenic enrichment culture. Arch. Microbiol. 158: 328–334

    Google Scholar 

  • Schwörer B, Breitung J, Klein AR, Stetter KO & Thauer RK (1993) Formylmethanofuran: tetrahydromethanopterin formyltransferase andN 5,N 10-methylenetetrahydromethanopterin dehydrogenase from the sulfate-reducingArchaeglobusfulgidus: similarities with the enzymes from methanogenic Archaea. Arch. Microbiol. 159: 225–232

    Google Scholar 

  • Smith DW (193) Ecological actions of sulfate-reducing bacteria. In: Odom JM & Singleton R (Eds) The sulfate-reducing bacteria: contemporary perspectives (pp 161–188). Springer-Verlag, New York

  • Smith LT & Kaplan NO (1980) Purification, properties, and kinetic mechanism of coenzyme A-linked aldehyde dehydrogenase fromClostridium kluyveri. Arch. Biochem. Biophys. 203: 663–675

    Google Scholar 

  • Speich N & Trüper HG (1988) Adenylylsulphate reductase in a dissimilatory sulphate-reducing archaebacterium. J. Gen. Microbiol. 134: 1419–1425

    Google Scholar 

  • Spormann AM & Thauer RK (1988) Anaerobic acetate oxidation to CO2 byDesulfotomaculum acetoxidans. Demonstration of enzymes required for the operation of an oxidative acetyl-CoA/carbon monoxide dehydrogenase pathway. Arch. Microbiol. 150: 374–380

    Google Scholar 

  • Spormann AM & Thauer RK (1989) Anaerobic acetate oxidation byDesulfotomaculum acetoxidans. Isotopic exchange between CO2 and the carbonyl group of acetyl-CoA and topology of enzymes involved. Arch. Microbiol. 152: 189–195

    Google Scholar 

  • Stahlmann J, Warthmann R & Cypionka H (1991) Na+-dependent accumulation of sulfate and thiosulfate in marine sulfate-reducing bacteria. Arch. Microbiol. 155: 554–558

    Google Scholar 

  • Stams AJM & Hansen TA (1982) Oxygen-labile lactate dehydrogenase activity inDesulfovibrio desulfuricans. FEMS Microbiol. Lett. 13: 389–394

    Google Scholar 

  • Stams AJM & Hansen TA (1986) Metabolism of L-alanine inDesulfotomaculum ruminis and two marineDesulfovibrio strains. Arch. Microbiol. 145: 277–279

    Google Scholar 

  • Stams AJM, Hansen TA & Skyring GW (1985) Utilization of amino acids as energy substrates by two marineDesulfovibrio strains. FEMS Microbiol. Lett. 31: 11–15

    Google Scholar 

  • Stams AJM, Kremer DR, Nicolay K, Weenk GH & Hansen TA (1984) Pathway of propionate formation inDesulfobulbus propionicus. Arch. Microbiol. 139: 167–173

    Google Scholar 

  • Stams AJM, Veenhuis M, Weenk GH & Hansen TA (1983) Occurrence of polyglucose as a storage polymer inDesulfovibrio species andDesulfobulbus propionicus. Arch. Microbiol. 136: 54–59

    Google Scholar 

  • Stetter KO (1988)Archaeoglobus fulgidus gen. nov., sp. nov.: a new taxon of extremely thermophilic archaebacteria. Syst. Appl. Microbiol. 10: 172–173

    Google Scholar 

  • Stieb M & Schink B (1989) Anaerobic degradation of isobutyrate by methanogenic enrichment cultures and by aDesulfococcus multivorans strain. Arch. Microbiol. 151: 126–132

    Google Scholar 

  • Stille W & Trüper HG (1984) Adenylylsulfate reductase in some new sulfate-reducing bacteria. Arch. Microbiol. 137: 145–150

    Google Scholar 

  • Stouthamer AH (1979) The search for correlation between theoretical and experimental growth yields. In: Quayle JR (Ed) Microbial Biochemistry (pp 1–47) University Park Press, Baltimore

    Google Scholar 

  • Stouthamer AH (1988) Bioenergetics and yields with electron acceptors other than oxygen. In: Erickson LE & Chung DY (Eds) Handbook on anaerobic fermentations (pp 345–437). Marcel Dekker, New York

    Google Scholar 

  • Stouthamer AH (1991) Metabolic regulation including anaerobic metabolism inParacoccus denitrificans. J. Bioenerg. Biomembr. 23: 163–185

    Google Scholar 

  • Stouthamer AH (1992) Metabolic pathways inParacoccus denitrificans and closely related bacteria in relation to the phylogeny of prokaryotes. Antonie v. Leeuwenhoek 61: 1–33

    Google Scholar 

  • Sublette KL & Gwozdz KJ (1991) An economic analysis of microbial reduction of sulfur dioxide as a means of byproduct recovery from regenerable processes for flue gas desulfurization. Appl. Biochem. Biotechnol. 28/29: 635–646

    Google Scholar 

  • Szewzyk R & Pfennig N (1990) Competition for ethanol between sulfate-reducing and fermenting bacteria. Arch. Microbiol. 153: 470–477

    Google Scholar 

  • Tanaka K (1990) Several new substrates forDesulfovibrio vulgaris Marburg and a spontaneous mutant from it. Arch. Microbiol. 155: 18–21

    Google Scholar 

  • Tanaka K (1992) Anaerobic oxidation of 1,5-pentanediol,2-butanol, and 2-propanol by a newly isolated sulfate-reducer. J. Ferm. Bioeng. 73: 362–365

    Google Scholar 

  • Tasaki M, Kamagata Y, Nakamura K & Mikami E (1992) Utilization of methoxylated benzoates and formation of intermediates byDesulfotomaculum thermobenzoicum in the presence or absence of sulfate. Arch. Microbiol. 157: 209–212

    Google Scholar 

  • Thauer RK (1988) Citric-acid cycle, 50 years on. Modification and alternative pathway in anaerobic bacteria. Eur. J. Biochem. 176: 497–508

    Google Scholar 

  • Thauer RK, Jungermann K & Decker K (1977) Energy conservation in chemotrophic anaerobic bacteria. Bacteriol. Rev. 41: 100–180

    Google Scholar 

  • Thauer RK, Möller-Zinkhan D & Spormann AM (1989) Biochemistry of acetate catabolism in anaeobic chemotrophic bacteria. Ann. Rev. Microbiol. 43: 43–67

    Google Scholar 

  • Turner N, Barata B, Bray RC, Deistung J, Le Gall J & Moura JJG (1987) The molybdenumiron-sulphur protein fromDesulfovibrio gigas as a form of aldehyde oxidase. Biochem. J. 243: 755–761

    Google Scholar 

  • Turner DL, Santos H, Fareleira P, Pacheco I, LeGall J & Xavier AV (1992) Structure determination of a novel cyclic phospho-compound isolated fromDesulfovibrio desulfuricans. Biochem. J. 285: 387–390

    Google Scholar 

  • Tursman JF & Cork DJ (1989) Influence of sulfate and sulfate-reducing abcteria and anaerobic digestion technology. Biological Waste Treatment, pp 273–285

  • Underwood-Lemons T, Moura I & To Ye K (1993) Resonance Raman study of sirohydrochlorin and siroheme in sulfite reductases from sulfate reducing bacteria. Biochim. Biophys. Acta 1157: 275–284

    Google Scholar 

  • Unemoto T & Hayashi H (1993) Na+-translocating NADH-quinone reductase of marine and halophilic bacteria. J. Bioenerg. Biomembr. 25: 385–391

    Google Scholar 

  • van den Berg WAM, van Dongen WMAM & Veeger C (1991) Reduction of the amount of periplasmic hydrogenas inDesulfovibrio vulgaris (Hildenborough) with antisense RNA: direct evidence for an important role of this hydrogenase in lactate metabolism. J. Bacteriol. 173: 3688–3694

    Google Scholar 

  • van der Maarel MJEC, Quist P, Dijkhuizen L & Hansen TA (1993) Anaerobic degradation of dimethylsulfoniopropionate to 3-S-methylmercaptopropionate by a marineDesulfobacterium strain. Arch. Microbiol. 160: 411–412

    Google Scholar 

  • Vinogradov AD (1993) Kinetics, control, and mechanism of ubiquinone reduction by the mammalian respiratory chain-linked NADH-ubiquinone reductase. J. Bioenerg. Biomembr. 25: 367–375

    Google Scholar 

  • Visscher PT, Prins RA & van Gemerden H (1992) Rates of sulfate reduction and thiosulfate consumption in a marine microbial mat. FEMS Microbiol. Ecol. 86: 283–294

    Google Scholar 

  • Voordouw G (1993) Molecular biology of the sulfate-reducing bacteria. In: Odom JM & Singleton R (Eds) The sulfate-reducing bacteria: contemporary perspectives (pp 88–130). Springer-Verlag, New York

    Google Scholar 

  • Voordouw G, Nivière V, Ferris FG, Fedorak PM & Westlake DWS (1990) Distribution of hydrogenase genes inDesulfovibrio spp. and their use in identification of species from the oil field environment. Appl. Environ. Microbiol. 56: 3748–3754

    Google Scholar 

  • Vonck J, Arfman N, de Vries GE, Van Beeumen J, van Bruggen EFJ & Dijkhuizen L (1991) Electron microscopic analysis and biochemical characterization of a novel methanol dehydrogenase from the thermotolerantBacillus sp. C1. J. Biol. Chem. 266: 3949–3954

    Google Scholar 

  • Warthmann R & Cypionka H (1990) Sulfate transport inDesulfobulbus propionicus andDesulfococcus multivorans. Arch. Microbiol. 154: 144–149

    Google Scholar 

  • White H, Strobl G, Feicht R & Simon H (1989) Carboxylic acid reductase: a new tungsten enzyme catalyses the reduction of non-activated carboxylic acids to aldehydes. Eur. J. Biochem. 184: 89–96

    Google Scholar 

  • White H, Huber C, Feicht R & Simon H (1993) On a reversible molybdenum-containing aldehyde oxidoreductase fromClostridium formicoaceticum. Arch. Microbiol. 159: 244–249

    Google Scholar 

  • Widdel F (1992a) The genusDesulfotomaculum. In: Balows A, Trüper HG, Dworkin M, Harder W & Schleifer KH (Eds) The Prokaryotes, 2nd edition (pp 1792–1799). Springer, New York

    Google Scholar 

  • Widdel F (1992b) The genusThermodesulfobacterium. In: Balows A, Trüper HG, Dworkin M, Harder W & Schleifer KH (Eds) The Prokaryotes, 2nd edition (pp 3390–3392). Springer, New York

    Google Scholar 

  • Widdel F & Bak F (1992) Gram-negative mesophilic sulfate-reducing bacteria. In: Balows A, Trüper HG, Dworkin M, Harder W & Schleifer KH (Eds) The Prokaryotes, 2nd edition (pp 3352–3378), Springer, New York

    Google Scholar 

  • Widdel F & Hansen TA (1992) The dissimilatory sulfate-reducing and sulfur-reducing bacteria. In: Balows A, Trüper HG, Dworkin M, Harder W & Schleifer KH (Eds) The Prokaryotes, 2nd edition (pp 583–624), Springer, New York

    Google Scholar 

  • Yagi T (1993) The bacterial energy-transducing NADH-quinone oxidoreductases. Biochim. Biophys. Acta 1141: 1–17

    Google Scholar 

  • Zellner G, Kneifel H & Winter J (1990) Oxidation of benzaldehydes to benzoic acid derivatives by threeDesulfovibrio strains. Appl. Environ. Microbiol. 56: 2228–2233

    Google Scholar 

  • Zellner G, Stackebrandt E, Kneifel H, Messner P, Sleytr UB, Conway de Macario E, Zabel HP, Stetter KO & Winter J (1989) Isolation and characterization of a thermophilic, sulfate reducing archaebacterium,Archaeoglobus fulgidus, strain Z. Syst. Appl. Microbiol. 11: 151–160

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Microbiology, University of Groningen, Kerklaan 30, 9751 NN, Haren, The Netherlands

    Theo A. Hansen

Authors
  1. Theo A. Hansen
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hansen, T.A. Metabolism of sulfate-reducing prokaryotes. Antonie van Leeuwenhoek 66, 165–185 (1994). https://doi.org/10.1007/BF00871638

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00871638

Key words

Search

Navigation