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.
Similar content being viewed by others
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
—— (1987b) Kinetics of butyrate, acetate, and hydrogen metabolism in a thermophilic, anaerobic, butyrate-degrading triculture. Appl. Environ. Microbiol. 53: 434–439
—— (1988) Product inhibition of butyrate metabolism by acetate and hydrogen in a thermophilic coculture. Appl. Environ. Microbiol. 54: 2393–2397
Amos DA & McInerney MJ (1990) Growth ofSyntrophomonas wolfei on short-chain unsaturated fatty acids. Arch. Microbiol. 154: 31–36
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
Barker HA (1981) Amino acid degradation by anaerobic bacteria. Ann. Rev. Biochem. 50: 23–40
Beaty PS & McInerney MJ (1987) Growth ofSyntrophomonas wolfei in pure culture on crotonate. Arch. Microbiol. 147: 389–393
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
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
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
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
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
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
Boone DR & Bryant MP (1980) Propionate-degrading bacterium,Syntrophobacter wolinii sp. nov. gen. nov., from methanogenic ecosystems. Appl. Environ. Microbiol. 40: 626–632
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
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
Bornstein BT & Barker HA (1948) The energy metabolism ofClostridium kluyveri and the synthesis of fatty acids. J. Biol. Chem. 172: 659–669
Bryant MP & Boone DR (1987) Isolation and characterization ofMethanobacterium formicicum MF. Int. J. Syst. Bacteriol. 37: 171
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
Bryant MP, Wolin EA, Wolin MJ & Wolfe RS (1967)Methanobacillus omelianskii, a symbiotic association of two species of bacteria. Arch. Mikrobiol. 59: 20–31
Buckel W & Barker HA (1974) Two pathways of glutamate fermentation by anaerobic bacteria. J. Bacteriol. 117: 1248–1260
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
Chang R (1977) Physical chemistry with applications to biological systems. Macmillan Publishing Co., New York
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
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
Chung KT (1976) Inhibitory effects of H2 on growth ofClostridium cellobioparum. Appl. Environ. Microbiol. 31: 342–348
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
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
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
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
Dolfing J (1988) Acetogenesis. In: Zehnder AJB (ed) Biology of anaerobic microorganisms (pp 417–468) John Wiley & Sons, New York
Dolfing J, Griffioen A, van Neerven ARW & Zevenhuizen (1985) Chemical and bacteriological composition of granular methanogenic sludge. Can. J. Microbiol. 31: 744–750
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
Dubourguier HC, Samain E, Prensier G & Albagnac G (1986) Characterization of two strains ofPelobacter carbinolicus isolated from anaerobic digesters. Arch. Microbiol. 145: 248–253
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
Evans WC & Fuchs G (1988) Anaerobic degradation of aromatic compounds. Ann. Rev. Microbiol. 42: 289–317
Ferry JG & Wolfe RS (1976) Anaerobic degradation of benzoate to methane by a consortium. Arch. Microbiol. 107: 33–40
Friedrich M, Laderer U & Schink B. (1991) Fermentative degradation of glycolic acid by defined syntrophic cocultures. Arch. Microbiol. 156: 398–404
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
Gottschalk G (1985) Bacterial Metabolism. Second Edition. Springer Verlag, New York
Gottschalk G & Blaut M (1990) Generation of proton and sodium motive forces in methanogenic bacteria. Biochim. Biophys. Acta 1018: 263–266
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
Gujer W & Zehnder AJB (1982) Conversion processes in anaerobic digestion. Wat. Sci. Technol. 15: 127–167
Guyot JP & Brauman A (1986) Methane production from formate by syntrophic association ofMethanobacterium bryantii andDesulfovibrio vulgaris JJ. Appl. Environ. Microbiol. 52: 1436–1437
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
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
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
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
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
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
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
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
Iza J (1991) Fluidized bed reactors for anaerobic wastewater treatment. Water. Sci. Technol. 24: 109–132
Jetten MSM, Stams AJM & Zehnder AJB (1990) Acetate threshold values and acetate activating enzymes in methanogenic bacteria. FEMS Microbiol. Ecol. 73: 339–344
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
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
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
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
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
Knoll G & Winter J (1987) Anaerobic degradation of phenol in sewage sludge. Appl. Microbiol. Biotechnol. 25: 384–391
Koch ME, Dolfing J, Wuhrmann K & Zehnder AJB (1983) Pathways of propionate degradation by enriched methanogenic cultures. Appl. Environ. Microbiol. 45: 1411–1414
Kremer DR & Hansen TA (1988) Pathway of propionate degradation inDesulfobulbus propionicus. FEMS Microbiol. Lett. 49: 273–277
Kremer DR, Nienhuis-Kuiper HE & Hansen TA (1988) Ethanol dissimilation inDesulfovibrio. Arch. Microbiol. 150: 552–557
Kröger A, Geisler V, Lemma E, Theis F & Lenger R (1993) Bacterial fumarate respiration. Arch. Microbiol. 158: 311–314
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
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
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
Latham MJ, & Wolin MJ (1977) Fermentation of cellulose byRuminococcus flavefaciens in the presence and absence ofMethanobacterium ruminantium. Appl. Environ. Microbiol. 34: 297–301
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
—— (1988b) Hydrogen partial pressures in a thermophilic acetateoxidizing methanogenic coculture. Appl. Environ. Microbiol. 54: 1457–1461
—— (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
Lettinga G & Hulshoff-Pol LW (1991) UASB process design for various types of waste waters. Wat. Sci. Tech. 24:88–107
Londry KL & Fedorak PM (1992) Benzoic intermediates in the anaerobic biodegradation of phenol. Can J. Microbiol. 38: 1–11
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
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
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
Matthies C & Schink B (1993) Anaerobic degradation of long-chain dicarboxylic acids by methanogenic enrichment cultures. FEMS Microbiol. Lett. 111: 177–182
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
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
McInerney MJ, Bryant MP & Pfennig N (1979) Anaerobic bacterium that degrades fatty acids in syntrophic association with methanogens. Arch. Microbiol. 122: 129–135
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
Mohn WM & Tiedje JM (1992) Microbial reductive dechlorination. Microbiol. Rev. 56: 482–507
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
Mountfort DO & Bryant MP (1982) Isolation and characterization of an anaerobic benzoate-degrading bacterium from sewage sludge. Arch. Microbiol. 133: 249–256
Mucha H, Lingens F & Trösch W (1988) Conversion of propionate to acetate and methane by syntrophic consortia. Appl. Microbiol. Biotechnol. 27: 581–586
Nagase M & Matsuo T (1982) Interaction between amino-acid degrading bacteria and methanogenic bacteria in anaerobic digestion. Biotechnol. Bioeng. 24: 2227–2239
—— (1987) Properties ofDesulfovibrio carbinolicus sp. nov. and other sulfate reducing bacteria isolated from an anaerobic purification plant. Appl. Environ. Microbiol. 53: 802–809
Nanninga HJ & Gottschal JC (1985) Amino acid fermentation and hydrogen transfer in mixed cultures. FEMS Microbiol. Ecol. 31: 261–269
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
Oremland RS (1988) Biogeochemistry of methanogenic bacteria. In: Zehnder AJB (ed) Biology of anaerobic microorganisms (pp 641–706) John Wiley & Sons, New York
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
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
Platen H & Schink B (1987) Methanogenic degradation of acetone by an enrichment culture. Arch. Microbiol. 149: 136–141
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
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
Robbins JE (1988) A proposed pathway for catabolism of propionate in methanogenic cocultures. Appl. Environ. Microbiol. 54: 1300–1301
Robinson JA & Tiedje JM (1984) Competition between sulphate-reducing and methanogenic bacteria for H2 under resting and growing conditions. Arch. Microbiol. 137: 26–32
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
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
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
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
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
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
Schauer NL, Brown DP & Ferry JG (1982) Kinetics of formate metabolism inMethanobacterium formicicum andMethanospirillum hungatei. Appl. Environ. Microbiol. 44: 540–554
Scheifinger CC, Linehan B, & Wolin MJ (1975) H2 production bySelenomonas ruminantium in the absence and presence of methanogenic bacteria. Appl. Microbiol. 29: 480–483
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
—— (1985) Fermentation of acetylene by an obligate anaerobe,Pelobacter acetylenicus sp. nov. Arch. Microbiol. 142: 295–301
—— (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
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
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
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
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
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
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
Seitz HJ, Schink B & Conrad R (1988) Thermodynamics of hydrogen metabolism in methanogenic cocultures degrading ethanol or lactate. FEMS Microbiol. Lett 55: 119–124
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
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
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
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
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
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
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
Stams AJM, Kremer DR, Nicolay K, Weenk GH & Hansen TA (1984) Pathway of propionate formation inDesulfobulbus propionicus. Arch. Microbiol. 139: 167–173
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
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
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
Stieb M & Schink B (1985) Anaerobic degradation of fatty acids byClostridium bryantii sp. nov., a sporeforming obigately syntrophic bacterium. Arch. Microbiol. 140: 387–390
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
Tschech A & Schink B (1986) Fermentative degradation of monohydroxybenzoates by defined syntrophic cocultures. Arch. Microbiol. 145: 396–402
Thauer RK (1990) Energy metabolism of methanogenic bacteria. Biochim. Biophys. acta 1018: 256–259
Thauer RK, Jungermann K & Decker K (1977) Energy conservation in chemotrophic anaerobic bacteria. Bacteriol. Rev. 41: 100–180
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
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
—— (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
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
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
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
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
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
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
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
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
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
Wildenauer FX & Winter J (1986) Fermentation of isoleucine and arginine by pure and syntrophic cultures ofClostridium sporogenes. FEMS Microbiol. Ecol. 38: 373–379
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
Winter J & Wolfe RS (1980) Methane formation from fructose by syntrophic associations ofAcetobacterium woodii and different strains of methanogens. Arch. Microbiol. 124: 73–79
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
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
Wolin MJ (1982) Hydrogen transfer in microbial communities. In: Bull AT & Slater JH (eds) Microbial interactions and communities (pp 323–356) Academic Press, London
Wu WM, Rickley RF, Jain MK & Zeikus JG (1993) Energetics and regulations of formate and hydrogen metabolism byMethanobacterium formicicum. Arch. Microbiol. 159: 57–65
Young JC (1991) Factors affecting the design and performance of upflow anaerobic filters. Wat. Sci. Tech. 24: 133–155
Zehnder AJB & Wuhrmann K (1977) Physiology of aMethanobacterium Strain AZ. Arch. Microbiol. 111: 199–205
Zeikus JG & Henning DL (1975)Methanobacterium arbophilicum sp.nov. An obligate anaerobe isolated from wetwood of living trees. Antonie van Leeuwenhoek 41: 543–552
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
—— (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
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
Zinder SH (1994) Syntrophic acetate oxidation and ‘reversible acetogenesis’ In: Drake HL (ed) Acetogenesis. Chapman and Hall, New York (In Press)
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
Zinder SH & Koch M (1984) Non-acetoclastic methanogenesis from acetate: acetate oxidation by a thermophilic syntrophic coculture. Arch. Microbiol. 138: 263–272
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
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
Issue Date:
DOI: https://doi.org/10.1007/BF00871644