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Metabolic interactions between anaerobic bacteria in methanogenic environments

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Abstract

In methanogenic environments organic matter is degraded by associations of fermenting, acetogenic and methanogenic bacteria. Hydrogen and formate consumption, and to some extent also acetate consumption, by methanogens affects the metabolism of the other bacteria. Product formation of fermenting bacteria is shifted to more oxidized products, while acetogenic bacteria are only able to metabolize compounds when methanogens consume hydrogen and formate efficiently. These types of metabolic interaction between anaerobic bacteria is due to the fact that the oxidation of NADH and FADH2 coupled to proton or bicarbonate reduction is thermodynamically only feasible at low hydrogen and formate concentrations. Syntrophic relationships which depend on interspecies hydrogen or formate transfer were described for the degradation of e.g. fatty acids, amino acids and aromatic compounds.

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References

  • Ahring BK & Westermann P (1987a) Thermophilic anaerobic degradation of butyrate by a butyrate-utilizing bacterium in coculture and triculture with methanogenic bacteria. Appl. Environ. Microbiol. 53: 429–433

    Google Scholar 

  • —— (1987b) Kinetics of butyrate, acetate, and hydrogen metabolism in a thermophilic, anaerobic, butyrate-degrading triculture. Appl. Environ. Microbiol. 53: 434–439

    Google Scholar 

  • —— (1988) Product inhibition of butyrate metabolism by acetate and hydrogen in a thermophilic coculture. Appl. Environ. Microbiol. 54: 2393–2397

    Google Scholar 

  • Amos DA & McInerney MJ (1990) Growth ofSyntrophomonas wolfei on short-chain unsaturated fatty acids. Arch. Microbiol. 154: 31–36

    Google Scholar 

  • Barik S, Brulla WJ & Bryant MP (1985) PA-1, a versatile anaerobe obtained in pure culture, catabolizes benzenoids and other compounds in syntrophy with hydrogenotrophs, and P-2 plusWolinella sp. degrades benzenoids. Appl. Environ. Microbiol. 50: 304–310

    Google Scholar 

  • Barker HA (1981) Amino acid degradation by anaerobic bacteria. Ann. Rev. Biochem. 50: 23–40

    Google Scholar 

  • Beaty PS & McInerney MJ (1987) Growth ofSyntrophomonas wolfei in pure culture on crotonate. Arch. Microbiol. 147: 389–393

    Google Scholar 

  • Belaich JP, Heitz P, Rousset M & Garcia JL (1990) Energetics of the growth of a new syntrophic benzoate degrading bacterium. In: Belaich JP, Bruschi M & Garcia JL (eds) Microbiology and biochemistry of strict anaerobes involved in interspecies hydrogen transfer (pp 269–280) Plenum Publishing Corporation, New York

    Google Scholar 

  • Ben-Bassat A, Lamed R & Zeikus JG (1981) Ethanol production by thermophilic bacteria: metabolic control of end product formation inThermoanaerobium brockii. J. Bacteriol. 146: 192–199

    Google Scholar 

  • Biesterveld S & Stams AJM (1990) Growth ofBacteroides xylanolyticus X5-1 in the presence and absence of a methanogen. In: Belaich JP, Bruschi M & Garcia JL (eds) Microbiology and biochemistry of strict anaerobes involved in interspecies hydrogen transfer (pp 365–368) Plenum Publishing Corporation, New York

    Google Scholar 

  • Biesterveld S, Kok MD, Dijkema C, Zehnder AJB and Stams AJM (1994a) Xylose catabolism inBacteroides xylanolyticus X5-1. Arch. Mirobiol. (In Press)

  • Biesterveld S, Zehnder AJB and Stams AJM (1994) Regulation of product formation inBacteroides xylanolyticus X5-1 by interspecies electron transfer. Appl Environ Microbiol 60: 1347–1352

    Google Scholar 

  • Blomgren A, Hansen A & Svensson B (1990) Enrichment of a mesophilic, syntrophic bacterial consortium converting acetate to methane at high ammonium concentrations. In: Belaich JP, Bruschi M & Garcia JL (eds) Microbiology and biochemistry of strict anaerobes involved in interspecies hydrogen transfer (pp 225–234) Plenum Publishing Corporation, New York

    Google Scholar 

  • Boone DR (1991) Ecology of methanogenesis. In: Rogers JE & Whitman WB (eds) Microbial production and consumption of greenhouse gases: methane, nitrogen oxides, and halomethanes (pp 57–70) American Society for Microbiology, Washington

    Google Scholar 

  • Boone DR & Bryant MP (1980) Propionate-degrading bacterium,Syntrophobacter wolinii sp. nov. gen. nov., from methanogenic ecosystems. Appl. Environ. Microbiol. 40: 626–632

    Google Scholar 

  • Boone DR, Johnson RL & Liu Y (1989) Diffusion of the interspecies electron carriers H2 and formate in methanogenic ecosystems, and applications in the measurement of K M for H2 and formate uptake. Appl. Environ. Microbiol. 55: 1735–1741

    Google Scholar 

  • Boone DR & Xun L (1987) Effects of pH, temperature and nutrients on propionate degradation by a methanogenic enrichment culture, Appl. Environ. Microbiol. 53: 1589–1592

    Google Scholar 

  • Bornstein BT & Barker HA (1948) The energy metabolism ofClostridium kluyveri and the synthesis of fatty acids. J. Biol. Chem. 172: 659–669

    Google Scholar 

  • Bryant MP & Boone DR (1987) Isolation and characterization ofMethanobacterium formicicum MF. Int. J. Syst. Bacteriol. 37: 171

    Google Scholar 

  • Bryant MP, Campbell LL, Reddy CA & Crabill MR (1967) Growth ofDesulfovibrio in lactate or ethanol media low in sulfate in association with H2-utilizing methanogenic bacteria. Appl. Environ. Microbiol. 33: 1162–1169

    Google Scholar 

  • Bryant MP, Wolin EA, Wolin MJ & Wolfe RS (1967)Methanobacillus omelianskii, a symbiotic association of two species of bacteria. Arch. Mikrobiol. 59: 20–31

    Google Scholar 

  • Buckel W & Barker HA (1974) Two pathways of glutamate fermentation by anaerobic bacteria. J. Bacteriol. 117: 1248–1260

    Google Scholar 

  • Bull AT & Slater JH (1982) Microbial interactions and community structure. In: Bull AT & Slater JH (eds) Microbial interactions and communities (pp 13–44) Academic Press, London

    Google Scholar 

  • Chang R (1977) Physical chemistry with applications to biological systems. Macmillan Publishing Co., New York

    Google Scholar 

  • Chen M & Wolin MJ (1977) Influence of CH4 production byMethanobacterium ruminantium on the fermentation of glucose and lactate bySelenomonas ruminantium. Appl. Environ. Microbiol. 34: 756–759

    Google Scholar 

  • Cheng G, Plugge CM, Roelofsen W, Houwen FP & Stams AJM (1992)Selenomonas acidaminovorans sp. nov., a versatile thermophilic proton-reducing anaerobe able to grow by decarboxylation of succinate to propionate. Arch. Microbiol. 157: 169–175

    Google Scholar 

  • Chung KT (1976) Inhibitory effects of H2 on growth ofClostridium cellobioparum. Appl. Environ. Microbiol. 31: 342–348

    Google Scholar 

  • Conrad R, Schink B and Phelps TJ (1986) Thermodynamics of H2-consuming and H2-producing metabolic reactions in diverse methanogenic environments under in situ conditions. FEMS Microbiol. Ecol. 38: 353–360

    Google Scholar 

  • Cord-Ruwisch R, Seitz HJ & Conrad R (1988) The capacity of hydrogenotrophic anaerobic bacteria to complete traces of hydrogen depends on the redox potential of the terminal electron acceptors. Arch. Microbiol. 149: 350–357

    Google Scholar 

  • Crill PM, Harriss RC & Bartlett KB (1991) Methane fluxes from terrestrial wetland environments. In: Rogers JE & Whitman WB (eds) Microbial production and consumption of greenhouse gases: methane, nitrogen oxides, and halomethanes (pp 175–187) American Society for Microbiology, Washington

    Google Scholar 

  • Dietrich G, Weiss N, Winter J (1988)Acetothermus paucivorans, gen.nov., sp.nov., a strictly anaerobic, thermophilic bacterium from sewage sludge, fermenting hexoses to acetate, CO2 and H2. Syst. Appl. Microbiol. 10: 174–179

    Google Scholar 

  • Dolfing J (1988) Acetogenesis. In: Zehnder AJB (ed) Biology of anaerobic microorganisms (pp 417–468) John Wiley & Sons, New York

    Google Scholar 

  • Dolfing J, Griffioen A, van Neerven ARW & Zevenhuizen (1985) Chemical and bacteriological composition of granular methanogenic sludge. Can. J. Microbiol. 31: 744–750

    Google Scholar 

  • Dubourguier HC, Prensier G & Albagnac G (1988) Structure and microbial activities of granular anaerobic sludge. In: Lettinga, G., A.J.B. Zehnder, J.T.C. Grotenhuis, L.W. Hulshoff Pol (eds) Granular anaerobic sludge; microbiology and technology (pp 18–33) Pudoc, Wageningen

    Google Scholar 

  • Dubourguier HC, Samain E, Prensier G & Albagnac G (1986) Characterization of two strains ofPelobacter carbinolicus isolated from anaerobic digesters. Arch. Microbiol. 145: 248–253

    Google Scholar 

  • Dörner C (1992) Biochemie und Energetik der Wasserstoff-Freisetzung in der syntrophen Vergärung von Fettsäuren und Benzoat. Dissertation, University of Tübingen

  • Dwyer DF, Weeg-Aerssens E, Shelton DR & Tiedje JM (1988) Bioenergetic conditions of butyrate metabolism by a syntrophic, anaerobic bacterium in coculture with hydrogen-oxidizing methanogenic and sulfidogenic bacteria. Appl. Environ. Microbiol. 54: 1354–1359

    Google Scholar 

  • Evans WC & Fuchs G (1988) Anaerobic degradation of aromatic compounds. Ann. Rev. Microbiol. 42: 289–317

    Google Scholar 

  • Ferry JG & Wolfe RS (1976) Anaerobic degradation of benzoate to methane by a consortium. Arch. Microbiol. 107: 33–40

    Google Scholar 

  • Friedrich M, Laderer U & Schink B. (1991) Fermentative degradation of glycolic acid by defined syntrophic cocultures. Arch. Microbiol. 156: 398–404

    Google Scholar 

  • Friedrich M & Schink B (1993) Hydrogen formation from glycolate driven by reversed electron transport in membrane vesicles of a syntrophic glycolate-oxidizing bacterium. Eur. J. Biochem. 217: 233–240

    Google Scholar 

  • Gottschalk G (1985) Bacterial Metabolism. Second Edition. Springer Verlag, New York

    Google Scholar 

  • Gottschalk G & Blaut M (1990) Generation of proton and sodium motive forces in methanogenic bacteria. Biochim. Biophys. Acta 1018: 263–266

    Google Scholar 

  • Grotenhuis JTC, Smit M, Plugge CM, Xu Y, Van Lammeren AAM, Stams AJM, & Zehnder AJB (1991) Bacteriological composition and structure of granular sludge adapted to different substrates. Appl Environ Microbiol 57: 1942–1949

    Google Scholar 

  • Gujer W & Zehnder AJB (1982) Conversion processes in anaerobic digestion. Wat. Sci. Technol. 15: 127–167

    Google Scholar 

  • Guyot JP & Brauman A (1986) Methane production from formate by syntrophic association ofMethanobacterium bryantii andDesulfovibrio vulgaris JJ. Appl. Environ. Microbiol. 52: 1436–1437

    Google Scholar 

  • Harmsen HJM, Wullings B, Akkermans ADL, Ludwig W & Stams AJM (1993) Phylogenetic analysis ofSyntrophobacter wolinii reveals a relationship with sulfate-reducing bacteria. Arch. Microbiol. 160: 238–240

    Google Scholar 

  • Henson JM & Smith PH (1985) Isolation of a butyrate-utilizing bacterium in coculture withMethanobacterium thermoautotrophicum from a thermophilic digestor. Appl. Environ. Microbiol. 49: 1461–1466

    Google Scholar 

  • Holliger C, Stams AJM & Zehnder AJB (1988) Anaerobic degradation of recalcitrant compounds. In: Hall ER & Hobson PN (eds) Anaerobic digestion 1988, Fifth International Symposium on Anaerobic Digestion, Bologna (pp 211–225) Pergamon Press, Oxford

    Google Scholar 

  • Houwen FP, Dijkema C, Schoenmakers CHH, Stams AJM & Zehnder AJB (1987)13C-NMR study of propionate degradation by a methanogenic coculture. FEMS Microbiol. Lett. 41: 269–274

    Google Scholar 

  • Houwen FP, Dijkema C, Stams AJM & Zehnder AJB (1991) Propionate metabolism in anaerobic bacteria; determination of carboxylation reactions with13C-NMR spectroscopy. Biochim. Biophys. Acta 1056: 126–132

    Google Scholar 

  • Houwen FP, Plokker J, Dijkema C & Stams AJM (1990) Enzymatic evidence for involvement of the methylmalonyl-CoA pathway in propionate oxidation bySyntrophobacter wolinii. Arch. Microbiol. 155: 52–55

    Google Scholar 

  • Huser BA, Wuhrmann K & Zehnder AJB (1982)Methanothrix soehngenii gen. nov. sp. nov., a new acetotrophic non-hydrogen-oxidizing methane bacterium. Arch. Microbiol. 132: 1–9

    Google Scholar 

  • Ianotti EL, Kafkewitz D, Wolin MJ, & Bryant MP (1973) Glucose fermentation products byRuminococcus albus grown in continuous culture withVibrio succinogenes: changes caused by interspecies transfer of H2. J. Bacteriol. 114: 1231–1240

    Google Scholar 

  • Iza J (1991) Fluidized bed reactors for anaerobic wastewater treatment. Water. Sci. Technol. 24: 109–132

    Google Scholar 

  • Jetten MSM, Stams AJM & Zehnder AJB (1990) Acetate threshold values and acetate activating enzymes in methanogenic bacteria. FEMS Microbiol. Ecol. 73: 339–344

    Google Scholar 

  • Jetten MSM, Stams AJM & Zehnder AJB (1992) Methanogenesis from acetate: a comparison of the acetate metabolism inMethanothrix soehngenii andMethanosarcina spp. FEMS Microbiol. Rev. 88: 181–198

    Google Scholar 

  • Jones WJ (1991) Diversity and physiology of methanogens. In: Rogers JE & Whitman WB (eds) Microbial production and consumption of greenhouse gases: methane, nitrogen oxides, and halomethanes (pp 39–55) American Society for Microbiology, Washington

    Google Scholar 

  • Kaesler B & Schönheit P (1989) The sodium cycle in methanogenesis. CO2 reduction to the formaldehyde level in methanogenic bacteria is driven by a primary electrochemical potential of Na+ generated by formaldehyde reduction to CH4. Eur. J. Biochem. 186: 309–316

    Google Scholar 

  • Kamagata Y, Kitagawa N, Tasaki M, Nakamura K & Mikami E (1992) Degradation of benzoate by an anaerobic consortium and some properties of a hydrogenotrophic methanogen and sulfate-reducing bacterium in the consortium. J. Ferment. Bioeng. 73: 213–218

    Google Scholar 

  • Kasper HF, Holland AJ & Mountfort DO (1987) Simultaneous butyrate oxidation bySyntrophomonas wolfei and catalytic olefin reduction in the absence of interspecies hydrogen transfer. Arch. Microbiol. 147: 334–339

    Google Scholar 

  • Knoll G & Winter J (1987) Anaerobic degradation of phenol in sewage sludge. Appl. Microbiol. Biotechnol. 25: 384–391

    Google Scholar 

  • Koch ME, Dolfing J, Wuhrmann K & Zehnder AJB (1983) Pathways of propionate degradation by enriched methanogenic cultures. Appl. Environ. Microbiol. 45: 1411–1414

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Kröger A, Geisler V, Lemma E, Theis F & Lenger R (1993) Bacterial fumarate respiration. Arch. Microbiol. 158: 311–314

    Google Scholar 

  • Krumholz LR, Bryant MP (1986)Syntrophococcus sucromutans sp.nov.gen.nov. uses carbohydrates as electron donors and formate, methoxymonobenzoids orMethanobrevibacter as electron acceptor systems. Arch. Microbiol. 143: 313–318

    Google Scholar 

  • Laanbroek HJ, Abee T & Voogd IL (1982) Alcohol conversions byDesulfobulbus propionicus Lindhorst in the presence and absence of sulphate and hydrogen. Arch. Microbiol. 133: 178–184

    Google Scholar 

  • Lamed R & Zeikus JG (1980.). Ethanol production by thermophilic bacteria: relationship between fermentation product yields of and catabolic enzyme activities inClostridium thermocellum andThermoanaerobium brockii. J. Bacteriol. 144: 569–578

    Google Scholar 

  • Latham MJ, & Wolin MJ (1977) Fermentation of cellulose byRuminococcus flavefaciens in the presence and absence ofMethanobacterium ruminantium. Appl. Environ. Microbiol. 34: 297–301

    Google Scholar 

  • Lee MJ & Zinder SH (1988a) 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: 124–129

    Google Scholar 

  • —— (1988b) Hydrogen partial pressures in a thermophilic acetateoxidizing methanogenic coculture. Appl. Environ. Microbiol. 54: 1457–1461

    Google Scholar 

  • —— (1988c) Carbon monoxide pathway enzyme activities in a thermophilic anaerobic bacterium grown acetogenically and in a syntrophic acetate-oxidizing coculture. Arch. Microbiol. 150: 513–518

    Google Scholar 

  • Lettinga G & Hulshoff-Pol LW (1991) UASB process design for various types of waste waters. Wat. Sci. Tech. 24:88–107

    Google Scholar 

  • Londry KL & Fedorak PM (1992) Benzoic intermediates in the anaerobic biodegradation of phenol. Can J. Microbiol. 38: 1–11

    Google Scholar 

  • Mah RA, Xun LY, Boone DR, Ahring B, Smith PH, Wilkie A (1990) Methanogenesis from propionate in sludge and enrichment systems. In: Belaich JP, Bruschi M & Garcia JL (eds) Microbiology and biochemistry of strict anaerobes involved in interspecies hydrogen transfer (pp 99–119) Plenum Press, New York

    Google Scholar 

  • Marvin-Sikkema FD, Rees E, Kraak MN, Gottschal JC & Prins RA (1993) Influence of metronidazole, CO, CO2, and methanogens on the fermentative metabolism of the anaerobic fungusNeocallimastix sp. strain L2. Appl. Environ. Microbiol. 59: 2678–2683

    Google Scholar 

  • Marvin-Sikkema FD, Richardson AJ, Stewart CS, Gottschal JC & Prins RA (1990) Influence of hydrogen-consuming bacteria on cellulose degradation by anaerobic fungi. Appl. Environ. Microbiol. 56: 3793–3797

    Google Scholar 

  • Matthies C & Schink B (1993) Anaerobic degradation of long-chain dicarboxylic acids by methanogenic enrichment cultures. FEMS Microbiol. Lett. 111: 177–182

    Google Scholar 

  • McInerney MJ (1988) Anaerobic hydrolysis and fermentation of fats and proteins. In: Zehnder AJB (ed) Biology of anaerobic microorganisms (pp 373–415) John Wiley & sons, New York

    Google Scholar 

  • McInerney MJ, Bryant MP, Hespell RB & Costerton JW (1981)Syntrophomonas wolfei gen.nov.sp.nov, an anaerobic syntrophic, fatty acid-oxidizing bacterium. Appl. Environ. Microbiol. 41: 1029–1039

    Google Scholar 

  • McInerney MJ, Bryant MP & Pfennig N (1979) Anaerobic bacterium that degrades fatty acids in syntrophic association with methanogens. Arch. Microbiol. 122: 129–135

    Google Scholar 

  • Miller TL (1991) Biogenic sources of methane. In: Rogers JE & Whitman WB (eds) Microbial production and consumption of greenhouse gases: methane, nitrogen oxides, and halomethanes (pp 175–187) American Society for Microbiology, Washington

    Google Scholar 

  • Mohn WM & Tiedje JM (1992) Microbial reductive dechlorination. Microbiol. Rev. 56: 482–507

    Google Scholar 

  • Mountfort DO, Brulla JW, Krumholz LR & Bryant MP (1984)Syntrophus buswellii gen. nov., sp. nov.: a benzoate cataboliser from methanogenic ecosystems. Int. J. Syst. Bacteriol. 34: 216–217

    Google Scholar 

  • Mountfort DO & Bryant MP (1982) Isolation and characterization of an anaerobic benzoate-degrading bacterium from sewage sludge. Arch. Microbiol. 133: 249–256

    Google Scholar 

  • Mucha H, Lingens F & Trösch W (1988) Conversion of propionate to acetate and methane by syntrophic consortia. Appl. Microbiol. Biotechnol. 27: 581–586

    Google Scholar 

  • Nagase M & Matsuo T (1982) Interaction between amino-acid degrading bacteria and methanogenic bacteria in anaerobic digestion. Biotechnol. Bioeng. 24: 2227–2239

    Google Scholar 

  • —— (1987) Properties ofDesulfovibrio carbinolicus sp. nov. and other sulfate reducing bacteria isolated from an anaerobic purification plant. Appl. Environ. Microbiol. 53: 802–809

    Google Scholar 

  • Nanninga HJ & Gottschal JC (1985) Amino acid fermentation and hydrogen transfer in mixed cultures. FEMS Microbiol. Ecol. 31: 261–269

    Google Scholar 

  • Örlygsson J, Houwen FP & Svensson BH (1993) Anaerobic degradation of protein and the role of methane formation in steady state thermophilic enrichment cultures. Swedish J. Agric. Res. 23: 45–54

    Google Scholar 

  • Oremland RS (1988) Biogeochemistry of methanogenic bacteria. In: Zehnder AJB (ed) Biology of anaerobic microorganisms (pp 641–706) John Wiley & Sons, New York

    Google Scholar 

  • Oude Elferink SJWH, Visser A, Hulshoff Pol LW & Stams AJM (1994) Sulfate reduction in methanogenic bioreactors. FEMS Microbiol. Rev. (In Press)

  • Patel GB (1984) Characterization and nutritional properties of methanotrix concillii sp. nov., a mesophilic aceticlastic methanogen. Can. J. Microbiol. 30: 1383–1396

    Google Scholar 

  • Patel GB & Sprott GD (1990)Methanosaeta concilii gen. nov., sp. nov., (‘Methanothrix concilii’) andMethanosaeta thermoacetophila nom. rev., comb. nov. Int. J. Syst. Bacteriol. 40: 79–82

    Google Scholar 

  • Platen H & Schink B (1987) Methanogenic degradation of acetone by an enrichment culture. Arch. Microbiol. 149: 136–141

    Google Scholar 

  • Plugge CM, Dijkema C & Stams AJM (1993) Acetyl-CoA cleavage pathway in a syntrophic propionate oxidizing bacterium growing on fumarate in the absence of methanogens. FEMS Microbiol. Lett. 110: 71–76

    Google Scholar 

  • Plugge CM, Grotenhuis JTC & Stams AJM (1990) Isolation and characterization of an ethanol-degrading bacterium from methanogenic granular sludge. In: Belaich JP, Bruschi M & Garcia JL (eds) Microbiology and biochemistry of strict anaerobes involved in interspecies hydrogen transfer (pp 439–442) Plenum Press, New York

    Google Scholar 

  • Robbins JE (1988) A proposed pathway for catabolism of propionate in methanogenic cocultures. Appl. Environ. Microbiol. 54: 1300–1301

    Google Scholar 

  • Robinson JA & Tiedje JM (1984) Competition between sulphate-reducing and methanogenic bacteria for H2 under resting and growing conditions. Arch. Microbiol. 137: 26–32

    Google Scholar 

  • Roy F, Samain E, Dubourguier HC & Albagnac G (1986)Syntrophomonas sapovorans sp.nov. a new obligately proton-reducing anaerobe oxidizing saturated and unsaturated long chain fatty acids. Arch. Microbiol. 145: 142–147

    Google Scholar 

  • Samain E, Albagnac G, Dubourguier HC & Touzel JP (1982) Characterization of a new propionic acid bacterium that ferments ethanol and displays a growth factor dependent associations with a Gramnegative homoacetogen. FEMS Microbiol. Lett. 15: 69–74

    Google Scholar 

  • Samain E, Dubourguier HC & Albagnac G (1984) Isolation and characterization ofDesulfobulbus elongatus sp.nov., from a mesophilic industrial digestor. Syst. Appl. Microbiol. 5: 391–401

    Google Scholar 

  • Samain E, Dubourguier HC, LeGall J & Albagnac G (1986) Regulation of hydrogenase activity in the propionate-oxidizing sulfate reducing bacteriumDesulfobulbus elongatus. In: Dubourguier HC, Albagnac G, Montreuil J, Romond C, Sautiere & Guillaume J (eds) Biology of anaerobic bacteria (pp 23–27) Elsevier, Amsterdam

    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 pathway inDesulfobacterium autotrophicum. 2. Demonstration of the enzymes of the pathway and comparison of CO dehydrogenase. Arch. Microbiol. 151: 84–89

    Google Scholar 

  • Schauer NL, Brown DP & Ferry JG (1982) Kinetics of formate metabolism inMethanobacterium formicicum andMethanospirillum hungatei. Appl. Environ. Microbiol. 44: 540–554

    Google Scholar 

  • Scheifinger CC, Linehan B, & Wolin MJ (1975) H2 production bySelenomonas ruminantium in the absence and presence of methanogenic bacteria. Appl. Microbiol. 29: 480–483

    Google Scholar 

  • Schink B (1984) Fermentation of 2,3-butanediol byPelobacter carbinolicus sp.nov. andPelobacter propionicus sp.nov., and evidence for propionate formation from C2 compounds. Arch. Microbiol. 137: 33–41

    Google Scholar 

  • —— (1985) Fermentation of acetylene by an obligate anaerobe,Pelobacter acetylenicus sp. nov. Arch. Microbiol. 142: 295–301

    Google Scholar 

  • —— (1992) Syntrophism among prokaryotes. In: Balows A, Trüper HG, Dworkin M, Harder W & Schleifer KH (eds) The Prokaryotes (pp 276–299) Springer Verlag, New York

    Google Scholar 

  • Schink B, Brune A & Schnell S (1992) Anaerobic degradation of aromatic compounds. In: Winkelmann G (ed) Microbial degradation of natural products (pp 219–242) VCH Verlagsgesellschaft, Weinheim

    Google Scholar 

  • Schink B & Stieb M (1983) Fermentative degradation of polyethylene glycol by a new strictly anaerobic Gram-negative nonsporeforming bacterium,Pelobacter venetianus sp. nov. Appl. Environ. Microbiol. 45: 1905–1923

    Google Scholar 

  • Schink B & Thauer RK (1988) Energetics of syntrophic methane formation and the influence of aggregation. In: Lettinga G, Zehnder AJB, Grotenhuis JTC & Hulshoff Pol LW (eds), Granular anaerobic sludge; microbiology and technology (pp 5–17) Pudoc, Wageningen

    Google Scholar 

  • Schmidt JE & Ahring BK (1993) Effects of hydrogen and formate on the degradation of propionate and butyrate in thermophilic granules from an upflow anaerobic sludge blanket reactor. Appl. Environ. Microbiol. 59: 2546–2551

    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 

  • Scholten-Koerselman I, Houwaard F, Janssen P & Zehnder AJB (1986)Bacteroides xylanolyticus sp. nov., a xylanolytic bacterium from methane producing cattle manure. Antonie van Leeuwenhoek 52: 543–554

    Google Scholar 

  • Seitz HJ, Schink B & Conrad R (1988) Thermodynamics of hydrogen metabolism in methanogenic cocultures degrading ethanol or lactate. FEMS Microbiol. Lett 55: 119–124

    Google Scholar 

  • Seitz HJ, Schink B, Pfennig N & Conrad R (1990) Energetics of syntrophic ethanol oxidation in defined chemostat cocultures. 2. Energy sharing in biomass production. Arch. Microbiol. 155: 89–93

    Google Scholar 

  • Shelton DR & Tiedje JM (1984) Isolation and partial characterization of bacteria in an anaerobic consortium that mineralizes 3-chlorobenzoic acid. Appl. Environ. Microbiol. 48: 840–848

    Google Scholar 

  • Soutschek E, Winter J, Schindler F & Kandler O (1984)Acetomicrobium flavidum, gen.nov. sp.nov., a thermophilic, anaerobic bacterium from sewage sludge, forming acetate, CO2 and H2 from glucose. Syst. Appl. Microbiol. 5: 377–390

    Google Scholar 

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

    Google Scholar 

  • Stams AJM, Grolle KCF, Frijters CTMJ & Van Lier JB (1992) Enrichment of thermophilic propionate-oxidizing bacteria in syntrophy withMethanobacterium thermoautotrophicum orMethanobacterium thermoformicicum. Appl. Environ. Microbiol. 58: 346–352

    Google Scholar 

  • Stams AJM, Grotenhuis JTC & Zehnder AJB (1989) Structure function relationship in granular sludge. In: Hattori T, Ishida Y, Maruyama, Morita RY & Uchida A (eds) Recent advances in microbial Ecology (pp 440–445) Japan Scientific Societies Press, Tokyo

    Google Scholar 

  • Stams AJM & Hansen TA (1984) Fermentation of glutamate and other compounds byAcidaminobacter hydrogenoformans gen.nov. sp.nov, an obligate anaerobe isolated from black mud. Studies with pure cultures and mixed cultures with sulfate-reducing and methanogenic bacteria. Arch. Microbiol. 137: 329–337

    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 & Plugge CM (1990) Isolation of syntrophic bacteria on metabolic intermediates. In: Belaich JP, Bruschi M & Garcia JL (eds) Microbiology and biochemistry of strict anaerobes involved in interspecies hydrogen transfer (pp 473–476) Plenum Publishing Corporation, New York

    Google Scholar 

  • Stams AJM, Van Dijk J, Dijkema C & Plugge CM (1993) Growth of syntrophic propionate-oxidizing bacteria with fumarate in the absence of methanogenic bacteria. Appl. Environ. Microbiol. 59: 1114–1119

    Google Scholar 

  • Stams AJM & Zehnder AJB (1990) Ecological impact of syntrophic alcohol and fatty acid utilization. In: Belaich JP, Bruschi M & Garcia JL (eds) Microbiology and biochemistry of strict anaerobes involved in interspecies hydrogen transfer (pp 87–98) Plenum Publishing Corporation, New York

    Google Scholar 

  • Stieb M & Schink B (1985) Anaerobic degradation of fatty acids byClostridium bryantii sp. nov., a sporeforming obigately syntrophic bacterium. Arch. Microbiol. 140: 387–390

    Google Scholar 

  • Szewzyk U & Schink B (1989) Degradation of hydroquinone, gentisate, and benzoate by a fermenting bacterium in pure or defined mixed cultures. Arch. Microbiol. 151: 541–545

    Google Scholar 

  • Tschech A & Schink B (1986) Fermentative degradation of monohydroxybenzoates by defined syntrophic cocultures. Arch. Microbiol. 145: 396–402

    Google Scholar 

  • Thauer RK (1990) Energy metabolism of methanogenic bacteria. Biochim. Biophys. acta 1018: 256–259

    Google Scholar 

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

    Google Scholar 

  • Thauer RK & Morris JG (1984) Metabolism of chemotrophic anaerobes: old views and new aspects. In: Kelly DP & Carr NG (eds) The microbe 1984: part 2. Prokaryotes and eukaryotes (pp 123–168) Cambridge University Press, Cambridge

    Google Scholar 

  • Thiele JH & Zeikus JG (1987) Interactions between hydrogen- and formate-producing bacteria and methanogens during anaerobic digestion, In: Erickson LE & Fung D (eds) Handbook on anaerobic fermentations (pp 537–595) Marcel Dekker, New York

    Google Scholar 

  • —— (1988) Control of interspecies electron flow during anaerobic digestion: significance of formate transfer versus hydrogen transfer during syntrophic methanogenesis in flocs. Appl. Environ. Microbiol. 54: 20–29

    Google Scholar 

  • Thiele JH, Chartrain M & Zeikus JG (1988) Control of interspecies electron flow during anaerobic digestion: role of the floc formation. Appl. Environ. Microbiol. 54: 10–19

    Google Scholar 

  • Tholozan JL, Samain E, Grivet JP, Moletta R, Dubourguier HC & Albagnac G (1988) Reductive carboxylation of propionate into butyrate in methanogenic ecosystems. Appl. Environ. Microbiol. 54: 441–445

    Google Scholar 

  • Van Lier JB, Grolle KCF, Frijters CTMJ, Stams AJM & Lettinga G (1993) Effect of acetate, propionate and butyrate on the thermophilic anaerobic degradation of propionate by methanogenic sludge and defined cultures. Appl. Environ. Microbiol. 59: 1003–1011

    Google Scholar 

  • Visser A, Beeksma I, van der Zee A, Stams AJM & Lettinga G (1994) Anaerobic degradation of volatile fatty acids at different sulfate concentrations. Appl. Microbiol. Biotechnol. 40: 549–556

    Google Scholar 

  • Vogels GD, Keltjens JT & van der Drift C (1988) Biochemistry of methane formation. In: Zehnder AJB (ed) Biology of anaerobic microorganisms (pp 707–770) John Wiley & Sons, New York

    Google Scholar 

  • Weimer PJ & Zeikus JG (1977) Fermentation of cellulose and cellobiose byClostridium thermocellum in the presence and absence ofMethanobacterium thermoautotrophicum. Appl. Environ. Microbiol. 33: 289–297

    Google Scholar 

  • Whitman WB, Bowen TL & Boone DR (1992) The methanogenic bacteria. In: Balows A, Trüper HG, Dworkin M, Harder W & Schleifer KH (eds) The Prokaryotes (pp 719–768) Springer Verlag, New York

    Google Scholar 

  • Widdel F (1988) Microbiology and ecology of sulfate- and sulfur-reducing bacteria. In: Zehnder AJB (ed) Biology of anaerobic microorganisms (pp 469–586) John Wiley & Sons, New York

    Google Scholar 

  • Widdel F & Pfennig N (1982) Studies on dissimilatory sulfatereducing bacteria that decompose fatty acids. II. Incomplete oxidation of propionate byDesulfobulbus propionicus gen. nov. sp. nov. Arch. Microbiol. 131: 360–365

    Google Scholar 

  • Wildenauer FX & Winter J (1986) Fermentation of isoleucine and arginine by pure and syntrophic cultures ofClostridium sporogenes. FEMS Microbiol. Ecol. 38: 373–379

    Google Scholar 

  • Winter J, Schindler F & Wildenauer FX (1987) Fermentation of alanine and glycine by pure and syntrophic cultures ofClostridium sporogenes. FEMS Microbiol. Ecol. 45: 153–161

    Google Scholar 

  • Winter J & Wolfe RS (1980) Methane formation from fructose by syntrophic associations ofAcetobacterium woodii and different strains of methanogens. Arch. Microbiol. 124: 73–79

    Google Scholar 

  • Wofford NQ, Beaty PS & McInerney MJ (1986) Preparation of cellfree extracts and the enzymes involved in fatty acid metabolism inSyntrophomonas wolfei. J. Bacteriol. 167: 179–185

    Google Scholar 

  • Wolin MJ (1976) Interactions between H2-producing and methane-producing species. In: Schlegel HG, Gottschalk G & Pfennig N (eds) Microbial formation and utilization of gases (H2, CH4, CO) (pp 14–15) Goltze, Göttingen

    Google Scholar 

  • Wolin MJ (1982) Hydrogen transfer in microbial communities. In: Bull AT & Slater JH (eds) Microbial interactions and communities (pp 323–356) Academic Press, London

    Google Scholar 

  • Wu WM, Rickley RF, Jain MK & Zeikus JG (1993) Energetics and regulations of formate and hydrogen metabolism byMethanobacterium formicicum. Arch. Microbiol. 159: 57–65

    Google Scholar 

  • Young JC (1991) Factors affecting the design and performance of upflow anaerobic filters. Wat. Sci. Tech. 24: 133–155

    Google Scholar 

  • Zehnder AJB & Wuhrmann K (1977) Physiology of aMethanobacterium Strain AZ. Arch. Microbiol. 111: 199–205

    Google Scholar 

  • Zeikus JG & Henning DL (1975)Methanobacterium arbophilicum sp.nov. An obligate anaerobe isolated from wetwood of living trees. Antonie van Leeuwenhoek 41: 543–552

    Google Scholar 

  • Zhao H, Yang D, Woese CR & Bryant MP (1989) Assignment of the syntrophic, fatty acid-degrading anaerobeClostridium bryantii toSyntrophospora bryantii gen. nov., comb. nov. Int. J. Syst. Bacterial. 40: 40–44

    Google Scholar 

  • —— (1993) Assignment of fatty acid-β-oxidizing syntrophic bacteria to Syntrophomonadaceae fam. nov. on the basis of 16S rRNA sequences. Int. J. Syst. Bacterial. 43: 278–286

    Google Scholar 

  • Zindel U, Freudenberg W, Reith M, Andreesen JR, Schnell J & Widdel F (1988)Eubacterium acidaminophilum sp.nov., a versatile amino acid degrading anaerobe producing or utilizing H2 or formate. Description and enzymatic studies. Arch. Microbiol. 150: 254–266

    Google Scholar 

  • Zinder SH (1994) Syntrophic acetate oxidation and ‘reversible acetogenesis’ In: Drake HL (ed) Acetogenesis. Chapman and Hall, New York (In Press)

    Google Scholar 

  • Zinder SH, Caldwell SC, Anguish T, Lee M & Koch M (1984) Methanogenesis in a thermophilic (58 °C) anaerobic digestor:Methanothrix sp. as an important aceticlastic methanogen. Appl. Environ. Microbiol. 47: 796–807

    Google Scholar 

  • Zinder SH & Koch M (1984) Non-acetoclastic methanogenesis from acetate: acetate oxidation by a thermophilic syntrophic coculture. Arch. Microbiol. 138: 263–272

    Google Scholar 

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Stams, A.J.M. Metabolic interactions between anaerobic bacteria in methanogenic environments. Antonie van Leeuwenhoek 66, 271–294 (1994). https://doi.org/10.1007/BF00871644

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