Abstract
This chapter deals with microbial communities of bacteria and archaea which closely cooperate in methanogenic degradation and perform metabolic functions in this community that neither one of them could carry out alone. The methanogenic degradation of fatty acids, alcohols, most aromatic compounds, amino acids, and others is performed in partnership between fermenting bacteria and methanogenic Archaea. The energy available in these processes is very small, attributing only fractions of an ATP unit per reaction run to every partner. The biochemical strategies taken include in most cases reactions of substrate-level phosphorylation combined with various kinds of reversed electron transport systems in which part of the gained ATP is reinvested into thermodynamically unfavorable electron transport processes. Altogether, these systems represent fascinating examples of energy efficiency at the lowermost energy level that allows microbial life.
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References
Aklujkar M, Haveman SA, DiDonato R, Chertkov O, Han CS, Land ML, Brown P, Lovley DR (2012) The genome of Pelobacter carbinolicus reveals surprising metabolic capabilities and physiological features. BMC Genomics 13:690
Allison MJ (1970) Nitrogen metabolism in rumen microorganisms. In: Phillipson AT (ed) Physiology and digestion and metabolism in the ruminant. Oriel Press, Stockfield, pp 456–473
Allison MJ, Bryant MP (1963) Biosynthesis of branched-chain amino acids from branched-chain fatty acids by rumen bacteria. Arch Biochem Biophys 101:269–277
Alperin MJ, Hoehler TM (2009) Anaerobic methane oxidation by archaea/sulfate-reducing bacteria aggregates: 1. thermodynamic and physical constraints. Am J Sci 309:869–957
Amos DA, McInerney MJ (1990) Growth of Syntrophomonas wolfei on unsaturated short chain fatty acids. Arch Microbiol 154:31–36
Andreesen JR (1994) Glycine metabolism in anaerobes. Antonie Van Leeuwenhoek 66:223–237
Andreesen JR (2004) Glycine reductase mechanism. Curr Opin Chem Biol 8:454–461
Andreesen JR, Bahl H, Gottschalk G (1989) Introduction to the physiology and biochemistry of the genus Clostridium. In: Minton NP, Clarke DC (eds) Clostridia. Plenum Press, New York, pp 27–62
Baena S, Fardeau M-L, Labat M, Ollivier B, Garcia J-L, Patel BKC (1998) Aminobacterium colombiense, gen. nov., sp. nov., an amino-acid degrading anaerobe isolated from anaerobic sludge. Anaerobe 4:241–250
Baena S, Fardeau M-L, Ollivier B, Labat M, Thomas P, Garcia J-L, Patel BKC (1999a) Aminomonas paucivorans gen. nov., sp. nov., a mesophilic, anaerobic, amino-acid-utilizing bacterium. Int J Syst Bacteriol 49:975–982
Baena S, Fardeau M-L, Woo THS, Ollivier B, Labat M, Patel BKC (1999b) Phylogenetic relationships of three amino-acid-utilizing anaerobes, Selenomonas acidaminovorans, “Selenomonas acidaminophila” and Eubacterium acidaminophilum, as inferred from partial 16S rDNA nucleotide sequences and proposal of Thermanaerovibrio acidaminovorans gen. nov., comb. nov. and Anaeromusa acidaminophila, gen. nov., sp. nov., comb. nov. Int J Syst Bacteriol 49:969–974
Barker HA (1981) Amino acid degradation by anaerobic bacteria. Annu Rev Biochem 50:23–40
Beaty PS, Wofford NQ, McInerney MJ (1987) Separation of Syntrophomonas wolfei from Methanospirillum hungatei in syntrophic cocultures by using percoll gradients. Appl Environ Microbiol 53:1183–1185
Biebl H, Pfennig N (1978) Growth yields of green sulfur bacteria in mixed cultures with sulfur and sulfate reducing bacteria. Arch Microbiol 117:9–16
Boetius A, Ravenschlag K, Schubert CJ, Rickert D, Widdel F, Giesecke A, Amann R, Jorgensen BB, Witte U, Pfannkuche O (2000) A marine microbial consortium apparently mediating anaerobic oxidation of methane. Nature 407:623–626
Boiangiu CD, Jayamani E, Brügel D, Herrmann G, Kim J, Forzi L, Hedderich R, Vgenopolou I, Pierik AJ, Steuber J, Buckel W (2005) Sodium ion pumps and hydrogen production in glutamate fermenting anaerobic bacteria. J Mol Microbiol Biotechnol 10:105–119
Boll M, Kung JW, Ermler U, Martins BM, Buckel W (2016) Fermentative cyclohexane carboxylate formation in Syntrophus aciditrophicus. J Mol Microbiol Biotechnol 26:165–179
Boone DR, Bryant MP (1980) Propionate-degrading bacterium, Syntrophobacter wolinii sp. nov. gen. nov., from methanogenic ecosystems. Appl Environ Microbiol 40:626–632
Borrel G, Harris HMB, Tottey W, Mihajlovski A, Parisot N, Peyretaillade E, Peyret P, Gribaldo S, O’Toole PW, Brugère JF (2012) Genome sequence of “Candidatus Methanomethylophilus alvus” Mx1201, a methanogenic archaeon from the human gut belonging to a seventh order of methanogens. J Bacteriol 194:6944–6945. https://doi.org/10.1128/JB.01867-12
Borrel G, O’Toole PW, Harris HMB, Peyret P, Brugère JF, Gribaldo S (2013) Phylogenomic data support a seventh order of methylotrophic methanogens and provide insights into the evolution of methanogenesis. Genome Biol Evol 5(10):1769–1780. https://doi.org/10.1093/gbe/evt128
Breznak JA, Kane MD (1990) Microbial H2/CO2 acetogenesis in animal guts: nature and nutritional significance. FEMS Microbiol Rev 7(3–4):309–313
Brune A (2007) Microbiology: woodworker’s digest. Nature 450:487–488
Bryant MP (1977) Microbiology of the rumen. In: Stevenson MJ (ed) Duke’s physiology of domestic animals, 9th edn. Cornell University Press, Itaca, pp 287–304
Bryant MP (1979) Microbial methane production – theoretical aspects. J Anim Sci 48:193–201
Bryant MP, Wolin EA, Wolin MJ, Wolfe RS (1967) Methanobacillus omelianskii, a symbiotic association of two species of bacteria. Arch Mikrobiol 59:20–31
Bryant MP, Campbell LL, Reddy CA, Crabill MR (1977) Growth of Desulfovibrio in lactate or ethanol media low in sulfate in association with H2-utilizing methanogenic bacteria. Appl Environ Microbiol 33:1162–1169
Buckel W (2001a) Unusual enzymes involved in five ways of glutamate fermentation. Appl Microbiol Biotechnol 57:263–273
Buckel W (2001b) Sodium ion-translocating decarboxylases. Biochem Biophys Acta 1505:15–27
Buckel W, Barker HA (1974) Two pathways of glutamate fermentation by anaerobic bacteria. J Bacteriol 117:1248–1260
Chen S, Liu X, Dong X (2005) Syntrophobacter sulfatireducens sp. nov., a novel syntrophic, propionate-oxidizing bacterium isolated from UASB reactors. Int J Syst Evol Microbiol 55:1319–1324
Chen S, Rotaru AE, Shrestha PM (2014) Promoting Interspecies Electron Transfer with Biochar. Sci Rep 4:5019
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 the decarboxylation of succinate to propionate. Arch Microbiol 157:169–175
Cherepanov DA, Mulkidjanian AY, Junge W (1999) Transient accumulation of elastic energy in proton translocating ATP synthase. FEBS Lett 449:1–6
Conklin A, Stensel HD, Ferguson J (2006) Growth kinetics and competition between Methanosarcina and Methanosaeta in mesophilic anaerobic digestion. Water Environ Res 78:486–496
Conway de Macario E, Macario AJL (2018) Methanogenic archaea in humans and other vertebrates. In: Hackstein JHP (ed) (Endo)symbiotic methanogens. Springer, Berlin, pp 103–119
Costa E, Perez J, Kreft JU (2006) Why is metabolic labour divided in nitrification? Trends Microbiol 14:213–219
Crable BR, Sieber JR, Mao X, Alvarez-Cohen L, Gunsalus RP, Ogorzalek Loo RR, Nguyen H, McInerney MJ (2016) Membrane complexes of Syntrophomonas wolfei involved in syntrophic butyrate degradation and hydrogen formation. Front Microbiol 7:1795. https://doi.org/10.3389/fmicb.2016.01795
De Bok FAM, Stams AJM, Dijkema C, Boone DR (2001) Pathway of propionate oxidation by a syntrophic culture of Smithella propionica and Methanospirillum hungatei. Appl Environ Microbiol 67:1800–1804
De Bok FAM, Luijten MLGC, Stams AJM (2002) Biochemical evidence for formate transfer in syntrophic propionate oxidizing cocultures of Syntrophobacter fumaroxidans and Methanospirillum hungatei. Appl Environ Microbiol 68:4247–4252
De Bok FAM, Harmsen JM, Plugge CM, de Vries MC, Akkermans ADL, de Vos WM, Stams AJM (2005) The first true obligately syntrophic propionate-oxidizing bacterium, Pelotomaculum schinkii sp. nov., cocultured with Methanospirillum hungatei, and emended description of the genus Pelotomaculum. Int J Syst Evol Microbiol 55:1697–1703
Dong X, Stams AJM (1995) Evidence for H2 and formate formation during syntrophic butyrate and propionate degradation. Anaerobe 1:35–39
Dong X, Plugge CM, Stams AJM (1994a) Anaerobic degradation of propionate by a mesophilic acetogenic bacterium in co- and triculture with different methanogens. Appl Environ Microbiol 60:2834–2838
Dong X, Cheng G, Stams AJM (1994b) Butyrate oxidation by Syntrophospora bryantii in coculture with different methanogens and in pure culture with pentenoate as electron acceptor. Appl Microbiol Biotechnol 42:647–652
Eichler B, Schink B (1986) Fermentation of primary alcohols and diols, and pure culture of syntrophically alcohol-oxidizing anaerobes. Arch Microbiol 143:60–66
Engelbrecht S, Junge W (1997) ATP synthase: a tentative structural model. FEBS Lett 414:485–491
Ettwig KF, Shima S, van de Pas-Schoonen KT, Kahnt J, Medema MH, op den Camp HJM, MSM J, Strous M (2008) Denitrifying bacteria anaerobically oxidize methane in the absence of Archaea. Environ Microbiol 10:3164–3173
Ettwig KF, Zhu B, Speth D, Keltjens JT, Jetten MS, Kartal B (2016) Archaea catalyze iron-dependent anaerobic oxidation of methane. Proc Natl Acad Sci U S A 113:12792–12796
Fang HHP, Chui HK, Li YY (1995) Microstructural analysis of UASB granules treating brewery wastewater. Water Sci Technol 31:129–135
Felchner-Zwirello M, Winter J, Gallert C (2013) Interspecies distances between propionic acid degraders and methanogens in syntrophic consortia for optimal hydrogen transfer. Appl Microbiol Biotechnol 97:9193–9205
Fenchel T, Finlay BJ (2018) Free-living protozoa with endosymbiotic methanogens. In: Hackstein JHP (ed) (Endo)symbiotic methanogens. Springer, Berlin, pp 1–11
Ferry JG (1992) Methanogenesis: ecology, physiology, biochemistry & genetics. Chapman & Hall, New York
Fuchs G (2008) Anaerobic metabolism of aromatic compounds. Ann N Y Acad Sci 1125:82–99
Fuchs G, Boll M, Heider J (2011) Microbial degradation of aromatic compounds – from one strategy to four. Nat Rev Microbiol 9:803–816
Gorby YA, Yanina S, McLean JS, Rosso KM, Moyles D, Dohnalkova A, Beveridge TJ, Chang IS, Kim BH, Kim KS, Culley DE, Reed SB, Romine MF, Saffarini DA, Hill EA, Shi L, Elias DA, Kennedy DW, Pinchuk G, Watanabe K, Ishii S, Logan B, Nealson KH, Fredrickson JK (2006) Electrically conductive nanowires produced by Shewanella oneidensis strain MR-1 and other microorganisms. Proc Natl Acad Sci 103:11358–11363
Gottschalk G (1986) Bacterial metabolism, 2nd edn. Springer, New York
Graentzdoerffer A, Rauh D, Pich A, Andreesen JR (2003) Molecular and biochemical characterization of two tungsten- and selenium-containing formate dehydrogenases from Eubacterium acidaminophilum that are associated with components of an iron-only hydrogenase. Arch Microbiol 179:116–130
Grotenhuis JTC, Smit M, Plugge CM, Xu YS, 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
Harmsen HJM, Akkermans ADL, Stams AJM, de Vos WM (1996) Population dynamics of propionate-oxidizing bacteria under methanogenic and sulfidogenic conditions in anaerobic granular sludge. Appl Environ Microbiol 62:2163–2168
Harmsen HJM, Van Kuijk BLM, Plugge CM, Akkermans ADL, de Vos WM, Stams AJM (1998) Description of Syntrophobacter fumaroxidans sp.nov., a syntrophic propionate-degrading sulfate-reducing bacterium. Int J Syst Bacteriol 48:1383–1387
Haroon MF, Hu SH, Shi Y, Imelfort M, Keller J, Hugenholtz P, Yuan ZG, Tyson GW (2013) Anaerobic oxidation of methane coupled to nitrate reduction in a novel archaeal lineage. Nature 500:567–570
Hattori S, Kamagata Y, Hanada S, Shoun H (2000) Thermacetogenium phaeum gen. nov., sp. nov., a strictly anaerobic, thermophilic, syntrophic acetate-oxidizing bacterium. Int J Syst Evol Microbiol 50:1601–1609
Hattori S, Galushko AS, Kamagata Y, Schink B (2005) Operation of the CO dehydrogenase/acetyl-CoA pathway in both acetate oxidation and acetate formation by the syntrophically acetate-oxidizing bacterium Thermacetogenium phaeum. J Bacteriol 187:3471–3476
Hazlewood GP, Nugent JHA (1978) Leaf fraction 1 protein as a nitrogen source for the growth of a proteolytic rumen bacterium. J Gen Microbiol 106:369–371
He Z, Zhang Q, Feng Y, Luo H, Pan X, Gadd GM (2018) Microbiological and environmental significance of metal-dependent anaerobic oxidation of methane. Sci Total Environ 610–611:759–768
Healy JB, Young LY (1978) Catechol and phenol degradation by a methanogenic population of bacteria. Appl Environ Microbiol 35(1):216–218
Herrmann G, Jayamani E, Mai G, Buckel W (2008) Energy conservation via electron-transferring flavoprotein in anaerobic bacteria. J Bacteriol 190:784–791
Hinrichs KU, Hayes JM, Sylva SP, Brewer PG, DeLong EF (1999) Methane-consuming archaebacteria in marine sediments. Nature 398:802–805
Hobson PN, Wallace RJ (1982) Microbial ecology and activities in the rumen. Crit Rev Microbiol 9:253–320
Iannotti EL, Kafkewitz D, Wolin MJ, Bryant MP (1973) Glucose fermentation products of Ruminococcus albus grown in continuous culture with Vibrio succinogenes: changes caused by interspecies transfer of H2. J Bacteriol 114:1231–1240
Imachi H, Sekiguchi Y, Kamagata Y, Hanada S, Ohashi A, Harada H (2002) Pelotomaculum thermopropionicum gen. nov., an anaerobic, thermophilic, syntrophic propionate-oxidizing bacterium. Int J Syst Evol Microbiol 52:1729–1735
Imachi H, Sakai S, Ohashi A, Harada H, Hanada S, Kamagata Y, Sekiguchi Y (2007) Pelotomaculum propionicicum sp nov., an anaerobic, mesophilic, obligately syntrophic propionate-oxidizing bacterium. Int J Syst Evol Microbiol 57:1487–1492
Ingham CJ, Sprenkels A, Bomer JG, Molenaar D, van den Berg A, van Hycklama Vlieg JET, de Vos WM (2007) A highly subdivided microbial growth chip constructed on a porous ceramic support. Proc Natl Acad Sci U S A 46:18217–18222
Jackson BE, Bhupathiraju VK, Tanner RS, Woese CR, McInerney MJ (1999) Syntrophus aciditrophicus sp. nov., a new anaerobic bacterium that degrades fatty acids and benzoate in syntrophic association with hydrogen-using microorganisms. Arch Microbiol 171:107–114
Jetten MSM, Stams AJM, Zehnder AJB (1992) Methanogenesis from acetate: a comparison of the acetate methabolism of Methanothrix soehngenii and Methanosarcina spp. FEMS Microbiol Rev 88:181–198
Kaden J, Galushko AS, Schink B (2002) Cysteine-mediated electron transfer in syntrophic acetate oxidation by cocultures of Geobacter sulfurreducens and Wolinella succinogenes. Arch Microbiol 178:53–58
Kato S, Hashimoto K, Watanabe K (2012) Methanogenesis facilitated by electric syntrophy via (semi)conductive iron-oxide minerals. Environ Microbiol 14:1646–1654
Kletzin A, Heimerl T, Flechsler J, van Niftrik L, Rachel R, Klingl A (2015) Cytochromes c in archaea: distribution, maturation, cell architecture, and the special case of Ignicoccus hospitalis. Front Microbiol 6:439
Knittel K, Boetius A (2009) Anaerobic oxidation of methane: progress with an unknown process. Annu Rev Microbiol 63:311–334
Kosaka T, Kato S, Shimoyama T, Ishii S, Abe T, Watanabe K (2008) The genome of Pelotomaculum thermopropionicum reveals niche-associated evolution in anaerobic microbiota. Genome Res 18:442–448
Kremer DR, Nienhuis-Kuiper HE, Hansen TA (1988) Ethanol dissimilation in Desulfovibrio. Arch Microbiol 150:552–557
Kröger A, Biel S, Simon J, Gross R, Unden G, Lancaster CRD (2002) Fumarate respiration of Wolinella succinogenes: enzymology, energetics and coupling mechanism. Biochim Biophys Acta 1553:23–38
Laso-Perez R, Wegener G, Knittel K, Widdel F, Harding KJ, Krukenberg V, Meier DV, Richter M, Tegetmeyer HE, Riedel D, Richnow HH, Adrian L, Reemtsma T, Lechtenfeld OJ, Musat F (2016) Thermophilic archaea activate butane via alkyl-coenzyme M formation. Nature 539:396–401
Leng L, Yang P, Singh S, Zhuang H, Xu L, Chen WH, Dolfing J, Li D, Zhang Y, Zeng H, Chu W, Lee PH (2018) A review on the bioenergetics of anaerobic microbial metabolism close to the thermodynamic limits and its implications for digestion applications. Bioresour Technol 247:1095–1106
Lever MA, Rogers K, Karyn L, Lloyd KG, Overmann J, Schink B, Thauer RK, Hoehler TM, Jørgensen BB (2015) Life under extreme energy limitation: a synthesis of laboratory- and field-based investigations. FEMS Microbiol Ecol 39:688–728
Li F, Hinderberger J, Seedorf H, Zhang J, Buckel W, Thauer RK (2008) Coupled ferredoxin and crotonyl coenzyme a (CoA) reduction with NADH catalyzed by the butyryl-CoA dehydrogenase/Etf complex from Clostridium kluyveri. J Bacteriol 190:843–850
Li H, Chang J, Liu P, Fu L, Ding D, Lu Y (2015) Direct interspecies electron transfer accelerates syntrophic oxidation of butyrate in paddy soil enrichments. Environ Microbiol 17:1533–1547
Limam RD, Chouari R, Mazéas L, Wu TD, Li T, Grossin-Debattista J, Guerquin-Kern J-L, Saidi M, Landoulsi A, Sghir A, Bouchez T (2014) Members of the uncultured bacterial candidate division WWE1 are implicated in anaerobic digestion of cellulose. Microbiol Open 3:157–167. https://doi.org/10.1002/mbo3.144
Liu Y, Whitman WB (2008) Metabolic, phylogenetic and ecological diversity of methanogenic archaea. In: Wiegel J, Maier MJ, Adams MW (eds) Incredible anaerobes: from physiology to genomics to fuels, vol 1125. Annals of the New York Academy of Sciences, New York, pp 171–189
Liu Y, Balkwill DL, Aldrich HC, Drake GR, Boone DR (1999) Characterisation of the anaerobic propionate-degrading syntrophs Smithella propionica gen. nov, sp. nov. and Syntrophobacter wolinii. Int J Syst Bacteriol 49:545–556
Liu FH, Rotaru AE, Shrestha PM, Malvankar NS, Nevin KP, Lovley DR (2012) Promoting direct interspecies electron transfer with activated carbon. Energy Environ Sci 5:8982–8989
Losey NA, Mus F, Peters JW, Le HM, McInerney MJ (2017) Syntrophomonas wolfei uses an NADH-dependent, ferredoxin-independent [FeFe]-hydrogenase to reoxidize NADH. Appl Environ Microbiol 83:e01335-17
Lovley DR (2017) Syntrophy goes electric: direct interspecies electron transfer. Annu Rev Microbiol 71:643–664
Lovley DR, Fraga JL, Blunt-Harris EL, Hayes LA, Phillips EJP, Coates JD (1998) Humic substances as a mediator for microbially catalyzed metal reduction. Acta Hydrochim Hydrobiol 26(3):152–157
Manzoor S, Muller B, Niazi A, Schnurer A, Bongcam-Rudloff E (2015) Working draft genome sequence of the mesophilic acetate oxidizing bacterium Syntrophaceticus schinkii strain Sp3. Stand Genomic Sci 10:99. https://doi.org/10.1186/s40793-015-0092-z
Manzoor S, Bongcam-Rudloff E, Schnurer A, Muller B (2016) Genome-guided analysis and whole transcriptome profiling of the mesophilic syntrophic acetate oxidising bacterium Syntrophaceticus schinkii. PLoS One 11:e0166520. https://doi.org/10.1371/journal.pone.0166520
McGlynn SE, Chadwick GL, Kempes CP, Orphan VJ (2015) Single cell activity reveals direct electron transfer in methanotrophic consortia. Nature 526:531–U146
McInerney MJ (1988) Anaerobic hydrolysis and fermentation of fats and proteins. In: Zehnder AJB (ed) Biology of anaerobic microorganisms. Wiley, New York, pp 373–415
McInerney MJ, Bryant MP, Pfennig N (1979) Anaerobic bacterium that degrades fatty acids in syntrophic association with methanogens. Arch Microbiol 122:129–135
McInerney MJ, Bryant MP, Pfennig N (1981) Syntrophomonas wolfei gen. nov. sp. nov., an anaerobic, syntrophic, fatty acid-oxidizing bacterium. Appl Environ Microbiol 41:1029–1039
McInerney MJ, Stams AJM, Boone DR (2005) Genus Syntrophobacter. In: Staley JT, Boone DR, Brenner DJ, de Vos P, Garrity GM, Goodfellow M, Krieg NR, Rainey FA, Schleifer KH (eds) Bergey’s manual of systematic bacteriology, vol 2, 2nd edn. Springer, New York, pp 1021–1027
McInerney MJ, Struchtemeyer CG, Sieber J, Mouttaki H, Stams AJM, Schink B, Rohlin L, Gunsalus RP (2008) Physiology, ecology, phylogeny and genomics of microorganisms capable of syntrophic metabolism. In: Wiegel J, Maier MJ, Adams MW (eds) Incredible anaerobes: from physiology to genomics to fuels, vol 1125. Annals of the New York Academy of Sciences, New York, pp 58–72
Meijer WG, Nienhuis-Kuiper ME, Hansen TA (1999) Fermentative bacteria from estuarine mud: phylogenetic position of Acidaminobacter hydrogenoformans and description of a new type of Gram-negative, propionigenic bacterium as Propionibacter pelophilus gen. nov., sp. nov. Int J Syst Bacteriol 49:1039–1044
Metje M, Frenzel P (2007) Methanogenesis and methanogenic pathways in a peat from subarctic permafrost. Environ Microbiol 9:954–964
Meulepas RJ, Jagersma CG, Khadem AF, Stams AJ, Lens PN (2010) Effect of methanogenic substrates on anaerobic oxidation of methane and sulfate reduction by an anaerobic methanotrophic enrichment. Appl Microbiol Biotechnol 87:1499–1506
Montag D, Schink B (2016) Biogas process parameters--energetics and kinetics of secondary fermentations in methanogenic biomass degradation. Appl Microbiol Biotechnol 100:1019–1026
Mountfort DO, Bryant MP (1982) Isolation and characterization of an anaerobic syntrophic benzoate-degrading bacterium from sewage sludge. Arch Microbiol 133:249–256
Müller N, Stingl U, Griffin BM, Schink B (2008) Dominant sugar utilizers in sediment of Lake Constance depend on syntrophic cooperation with methanogenic partner organisms. Environ Microbiol 10:1501–1511
Müller N, Schleheck D, Schink B (2009) Involvement of NADH:acceptor oxidoreducase and butyryl-CoA dehydrogenase in reversed electron transport during syntrophic butyrate oxidation by Syntrophomonas wolfei. J Bacteriol 191:6167–6177
Müller N, Worm P, Schink B, Stams AJM, Plugge CM (2010) Syntrophic butyrate and propionate oxidation processes: from genomes to reaction mechanisms. Environ Microbiol Rep 2:489–499
Müller N, Scherag FD, Pester M, Schink B (2015) Bacillus stamsii sp. nov., a facultatively anaerobic sugar degrader that is numerically dominant in freshwater lake sediment. Syst Appl Microbiol 38:379–389
Nagase M, Matsuo T (1982) Interaction between amino-acid degrading bacteria and methanogenic bacteria in anaerobic digestion. Biotechnol Bioeng 24:2227–2239
Nakano MM, Dailly YP, Zuber P, Clark DP (1997) Characterization of anaerobic fermentative growth of Bacillus subtilis: identification of fermentation end products and genes required for growth. J Bacteriol 179:6749–6755
Nanninga HJ, Gottschal JC (1985) Amino acid fermentation and hydrogen transfer in mixed cultures. FEMS Microbiol Ecol 31:261–269
Nanninga HJ, Drenth WJ, Gottschal JC (1987) Fermentation of glutamate by Selenomonas acidaminophila, sp. nov. Arch Microbiol 147:152–157
Nauhaus K, Boetius A, Krüger M, Widdel F (2002) In vitro demonstration of anaerobic oxidation of methane coupled to sulphate reduction in sediment from a marine gas hydrate area. Environ Microbiol 4:296–305
Oehler D, Poehlein A, Leimbach A, Müller N, Daniel R, Gottschalk G, Schink B (2012) Genome-guided analysis of physiological and morphological traits of the fermentative acetate oxidizer Thermacetogenium phaeum. BMC Genomics 13:723. https://doi.org/10.1186/1471-2164-13-723 URL http://www.biomedcentral.com/1471-2164/13/723
Orcutt B, Meile C (2008) Constraints on mechanisms and rates of anaerobic oxidation of methane by microbial consortia: process-based modeling of ANME-2 archaea and sulfate reducing bacteria interactions. Biogeosciences 5:1587–1599
Orphan VJ, House CH, Hinrichs KU, McKeegan KD, DeLong EF (2001) Methane-consuming archaea revealed by directly coupled isotopic and phylogenetic analysis. Science 293:484–487
Pelletier E, Kreymeyer A, Bocs S, Rouy Z, Gyapay G, Chouari R, Riviere D, Ganesan A, Daegelen P, Sghir A, Cohen GN, Medigue C, Weissenbach J, Paslier DL (2008) “Candidatus Cloacamonas acidaminovorans”: genome sequence reconstruction provides a first glimpse of a new bacterial division. J Bacteriol 190:2572–2579. https://doi.org/10.1128/JB.01248-07
Pfennig N, Biebl H (1976) Desulfuromonas acetoxidans gen. nov. sp. nov., a new anaerobic, sulfur-reducing acetate-oxidizing bacterium. Arch Microbiol 110:3–12
Philipp B, Schink B (2012) Different strategies in anaerobic biodegradation of aromatic compounds: nitrate reducers versus strict anaerobes. Environ Microbiol Rep 4:469–478. https://doi.org/10.1111/j.1758-2229.2011.00304
Platen H, Schink B (1987) Methanogenic degradation of acetone by an enrichment culture. Arch Microbiol 149:136–141
Platen H, Janssen PH, Schink B (1994) Fermentative degradation of acetone by an enrichment culture in membrane-separated culture devices and in cell suspensions. FEMS Microbiol Lett 122:27–32
Plugge CM, Stams AJM (2005) Syntrophism among Clostridiales. In: Duerre P (ed) Handbook on Clostridia. CRC Press, Boca Raton, pp 769–784
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, Zoetendal EG, Stams AJM (2000) Caloramator coolhaasii, sp. nov. a glutamate-degrading, moderately thermophilic anaerobe. Int J Syst Bacteriol 50:1155–1161
Plugge CM, van Leeuwen JM, Hummelen T, Balk M, Stams AJM (2001) Elucidation of the pathways of catabolic glutamate conversion in three thermophilic anaerobic bacteria. Arch Microbiol 176:29–36
Plugge CM, Balk M, Zoetendal EG, Stams AJM (2002a) Gelria glutamica, gen. nov., sp. nov., a thermophilic obligate syntrophic glutamate-degrading anaerobe. Int J Syst Evol Microbiol 52:401–406
Plugge CM, Balk M, Stams AJM (2002b) Desulfotomaculum thermobenzoicum subsp. thermosyntrophicum subsp. nov., a thermophilic syntrophic propionate-oxidizing spore-forming bacterium. Int J Syst Evol Microbiol 52:391–399
Plugge CM, Henstra AM, Worm P, Swarts DC, Paulitsch-Fuchs AH, Scholten JCM, Lykidis A, Lapidus AL, Goltsman E, Kim E, McDonald E, Rohlin L, Crable BR, Gunsalus RP, Stams AJM, McInerney MJ (2012) Complete genome sequence of Syntrophobacter fumaroxidans strain MPOBT. Stand Genomic Sci 10:91–106
Qiu YL, Hanada S, Ohashi A, Harada H, Kamagata Y, Sekiguchi Y (2008) Syntrophorhabdus aromaticivorans gen. nov., sp. nov., the first cultured anaerobe capable of degrading phenol to acetate in obligate syntrophic associations with a hydrogenotrophic methanogen. Appl Environ Microbiol 74:2051–2058
Raghoebarsing AA, Pol A, van de Pas-Schoonen KT, Smolders AJP, Ettwig KF, Rijpstra WIC, Schouten S, Damste JSS, Op den Camp HJM, Jetten MSM, Strous M (2006) A microbial consortium couples anaerobic methane oxidation to denitrification. Nature 440:918–921
Reda T, Plugge CM, Abram NJ, Hirst J (2008) Reversible interconversion of carbon dioxide and formate by an electroactive enzyme. PNAS 105:10654–10658
Reddy CA, Bryant MP, Wolin MJ (1972a) Characteristics of S organism isolated from Methanobacillus omelianskii. J Bacteriol 109:539–545
Reddy CA, Bryant M, Wolin MJ (1972b) Ferredoxin- and nicotinamide adenine dinucleotide-dependent H2 production from ethanol and formate in extracts of S organism isolated from Methanobacillus omelianskii. J Bacteriol 110:126–132
Reddy CA, Bryant MP, Wolin MJ (1972c) Ferredoxin-dependent conversion of acetaldehyde to acetate and H2 in extracts of S organism. J Bacteriol 110:133–138
Reguera G, McCarthy KD, Mehta T, Nicoll JS, Tuominen MT, Lovley DR (2005) Extracellular electron transfer via microbial nanowires. Nature 435:1098–1101
Rinke C, Schwientek P, Sczyrba A, Ivanova NN, Anderson IJ, Cheng J-F, Darling A, Malfatti S, Swan BK, Gies EA, Dodsworth JA, Hedlund BP, Tsiamis G, Sievert SM, Liu W-T, Eisen JA, Hallam SJ, Kyrpides NC, Stepanauskas R, Rubin EM, Hugenholtz P, Woyke T (2013) Insights into the phylogeny and coding potential of microbial dark matter. Nature 499:431–437. https://doi.org/10.1038/nature12352
Rotaru AE, Shrestha PM, Liu FH, Shrestha M, Shrestha D, Embree M, Zengler K, Wardman C, Nevin KP, Lovley DR (2014a) A new model for electron flow during anaerobic digestion: direct interspecies electron transfer to Methanosaeta for the reduction of carbon dioxide to methane. Energy Environ Sci 7(1):408–415
Rotaru AE, Shrestha PM, Liu F, Markovaite B, Chen S, Nevin KP, Lovley DR (2014b) Direct interspecies electron transfer between Geobacter metallireducens and Methanosarcina barkeri. Appl Environ Microbiol 80(15):4599–4605
Roy F, Samain E, Dubourgier 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
Scheller S, Yu H, Chadwick GL, McGlynn SE, Orphan VJ (2016) Artificial electron acceptors decouple archaeal methane oxidation from sulfate reduction. Science 351:703–707
Schink B (1985) Fermentation of acetylene by an obligate anaerobe, Pelobacter acetylenicus sp. nov. Arch Microbiol 142:295–301
Schink B (1989) Mikrobielle Lebensgemeinschaften in Gewässersedimenten. Naturwissenschaften 76:364–372
Schink B (1997) Energetics of syntrophic cooperation in methanogenic degradation. Microbiol Mol Biol Rev 61:262–280
Schink B, Stams AJM (2002) Syntrophism among prokaryotes. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (eds) The prokaryotes: an evolving electronic resource for the microbiological community, 3rd edn. Springer, New York, p 25
Schink B, Thauer RK (1988) Energetics of syntrophic methane formation and the influence of aggregation. In: Lettinga G et al (eds) Granular anaerobic sludge; microbiology and technology. Pudoc, Wageningen, pp 5–17
Schink B, Zeikus JG (1982) Microbial ecology of pectin decomposition in anoxic lake sediments. J Gen Microbiol 128:393–404
Schink B, Montag D, Keller A, Müller N (2017) Hydrogen or formate – alternative key players in methanogenic degradation. Environ Microbiol Rep 9:189–202
Schmidt A, Müller N, Schink B, Schleheck D (2013) A proteomic view at the biochemistry of syntrophic butyrate oxidation in Syntrophomonas wolfei. Plos One. http://www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone.0056905
Schmidt A, Frensch M, Schleheck D, Schink B, Müller N (2014) Degradation of acetaldehyde and its precursors by Pelobacter carbinolicus and P. acetylenicus. PLoS One 9(12):e115902. https://doi.org/10.1371/journal.pone.0115902
Schnürer A, Schink B, Svensson BH (1996) Clostridium ultunense sp. nov., a mesophilic bacterium oxidizing acetate in syntrophic association with a hydrogenotrophic methanogenic bacterium. Int J Syst Bacteriol 46:1145–1152
Schnürer A, Svensson BH, Schink B (1997) Enzyme activities in and energetics of acetate metabolism by the mesophilic syntrophically acetate-oxidizing anaerobe Clostridium ultunense. FEMS Microbiol Lett 154:331–336
Schöcke L, Schink B (1997) Energetics of methanogenic benzoate degradation by Syntrophus gentianae in syntrophic coculture. Microbiology 143:2345–2351
Schöcke L, Schink B (1999) Energetics and biochemistry of fermentative benzoate degradation by Syntrophus gentianae. Arch Microbiol 171:331–337
Scholten JCM, Culley DE, Brockman FJ, Wu G, Zhang W (2007) Evolution of the syntrophic interaction between Desulfovibrio vulgaris and Methanosarcina barkeri: involvement of an ancient horizontal gene transfer. Biochem Biophys Res Commun 5:48–54
Schut GJ, Adams MW (2009) The iron-hydrogenase of Thermotoga maritima utilizes ferredoxin and NADH synergistically: a new perspective on anaerobic hydrogen production. J Bacteriol 191:4451–4457
Sekiguchi Y, Kamagata Y, Nakamura K, Ohashi A, Harada H (2000) Syntrophothermus lipocalidus gen. nov., sp. nov., a novel thermophilic, syntrophic, fatty-acid-oxidizing anaerobe which utilizes isobutyrate. Int J Syst Evol Microbiol 50:771–779
Shresta PM, Rotaru AE (2014) Plugging in or going wireless: strategies for interspecies electron transfer. Front Microbiol. https://doi.org/103389/fmicb.2014.00237
Shrestha PM, Rotaru AE, Aklujkar M, Liu F, Shrestha M, Summers ZM, Malvankar N, Flores DC, Lovley DR (2013) Syntrophic growth with direct interspecies electron transfer as the primary mechanism for energy exchange. Environ Microbiol Rep 5(6):904–910
Sieber JR, Sims DR, Han C, Kim E, Lykidis A, Lapidus AL, McDonnald E, Rohlin L, Culley DE, Gunsalus RP, McInerney MJ (2010) The genome of Syntrophomonas wolfei: new insights into syntrophic metabolism and biohydrogen production. Environ Microbiol 12:2289–2301
Sieber JR, Le H, McInerney MJ (2014) The importance of hydrogen and formate transfer for syntrophic fatty, aromatic and alicyclic metabolism. Environ Microbiol 16:177–188
Sieber JR, Crable BR, Sheik CS, Hurst GB, Rohlin L, Gunsalus RP, McInerney MJ (2015) Proteomic analysis reveals metabolic and regulatory systems involved the syntrophic and axenic lifestyle of Syntrophomonas wolfei. Front Microbiol 6:115. https://doi.org/10.3389/fmicb.2015.00115
Sousa DZ, Smidt H, Alves MM, Stams AJM (2007) Syntrophomonas zehnderi sp. nov., an anaerobe that degrades long-chain fatty acids in co-culture with Methanobacterium formicicum. Int J Syst Evol Microbiol 57:609–615
Stams AJM (1994) Metabolic interactions between anaerobic bacteria in methanogenic environments. Antonie Van Leeuwenhoek 66:271–294
Stams AJM, Hansen TA (1984) Fermentation of glutamate and other compounds by Acidaminobacter 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, Plugge CM (2009) Electron transfer in syntrophic communities of anaerobic bacteria and archaea. Nat Rev Microbiol 7:568–577
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
Stickland LH (1934) The chemical reaction by which Cl. sporogenes obtains its energy. Biochem J 28:1746–1759
Stieb M, Schink B (1985) Anaerobic oxidation of fatty acids by Clostridium bryantii sp. nov., a sporeforming, obligately syntrophic bacterium. Arch Microbiol 140:387–390
Stieb M, Schink B (1986) Anaerobic degradation of isovalerate by a defined methanogenic coculture. Arch Microbiol 144:291–295
Stieb M, Schink B (1989) Anaerobic degradation of isobutyrate by methanogenic enrichment cultures and by a Desulfococcus multivorans strain. Arch Microbiol 151:126–132
Svetlitshnyi V, Rainey F, Wiegel J (1996) Thermosyntropha lipolytica gen. nov., sp. nov., a lipolytic, anaerobic, alkalitolerant, thermophilic bacterium utilizing short- and long-chain fatty acids in syntrophic coculture with a methanogenic archaeum. Int J Syst Bacteriol 46:1131–1137
Szewzyk U, Schink B (1989) Degradation of hydroquinone, gentisate, and benzoate by a fermenting bacterium in pure or defined mixed culture. Arch Microbiol 151:541–545
Tarlera S, Muxi L, Soubes M, Stams AJM (1997) Caloramator proteoclasticus sp. nov., a moderately thermophilic anaerobic proteolytic bacterium. Int J Syst Bacteriol 47:651–656
Tewes FJ, Thauer RK (1980) Regulation of ATP synthesis in glucose fermenting bacteria involved in interspecies hydrogen transfer. In: Gottschalk G, Pfennig N, Werner H (eds) Anaerobes and anaerobic infections. G Fischer, Stuttgart, pp 97–104
Thauer RK (2011) Anaerobic oxidation of methane with sulfate: on the reversibility of the reactions that are catalyzed by enzymes also involved in methanogenesis from CO2. Curr Opin Microbiol 14:292–299
Thauer RK, Morris JG (1984) Metabolism of chemotrophic anaerobes: old views and new aspects. In: Kelly DP, Carr NG (eds) The microbe 1984: prokaryotes and eukaryotes part II. Cambridge University Press, Cambridge, pp 123–168
Thauer RK, Jungermann K, Decker K (1977) Energy conservation in chemotrophic anaerobic bacteria. Bacteriol Rev 41:100–180
Timmers PHA, Welte CU, Koehorst JJ, Plugge CM, Jetten MS, Stams AJ (2017) Reverse methanogenesis and respiration in methanotrophic archaea. Archaea 2017:1654237. https://doi.org/10.1155/2017/1654237
Treude T, Orphan V, Knittel K, Gieseke A, House CH, Boetius A (2007) Consumption of methane and CO2 by methanotrophic microbial mats from gas seeps of the anoxic Black Sea. Appl Environ Microbiol 73:2271–2283
Valentine DL, Reeburgh VS, Blanton DC (2000) A culture apparatus for maintaining H2 at sub-nanomolar concentrations. J Microbiol Methods 39:243–251
Van Kuijk BLM, Stams AJM (1996) Purification and characterization of malate dehydrogenase from the syntrophic propionate-oxidizing bacterium strain MPOB. FEMS Microbiol Lett 144:141–144
Van Kuijk BLM, Schlösser E, Stams AJM (1998) Investigation of the fumarate metabolism of the syntrophic propionate-oxidizing bacterium strain MPOB. Arch Microbiol 169:346–352
van Lingen HJ, Plugge CM, Fadel JG, Kebreab E, Bannink A, Dijkstra J (2016) Thermodynamic driving force of hydrogen on rumen microbial metabolism: a theoretical investigation. PLoS One 11:10. https://doi.org/10.1371/journal.pone.0161362
Van Lingen HJ, Edwards JE, Vaidya JD, van Gastelen S, van den Bogert B, Saccenti E, Bannink A, Smidt H, Plugge CM, Dijkstra J (2017) Diurnal dynamics of gaseous and dissolved metabolites and microbiota composition in the bovine rumen. Front Microbiol 8:425
Vervoort Y, Gutiérrez Linares A, Roncoroni M, Liu C, Steensels J, Verstrepen KJ (2017) High-throughput system-wide engineering and screening for microbial biotechnology. Curr Opin Biotechnol 46:120–125
Viggi CC, Rosetti S, Fazi S, Paiano P, Majone M, Aulenta F (2014) Magnetite particles triggering a faster and more robust syntrophic pathway of methanogenic propionate degradation. Environ Sci Technol 48(13):7536–7543
Walker CB, He Z, Yang ZK, Ringbauer JA Jr, Zhou J, Voordouw G, Wall JD, Hazen TC, Arkin AP, Stahl DA (2009) The electron transfer system of syntrophically grown Desulfovibrio vulgaris. J Bacteriol 191:5793–5801
Wallrabenstein C, Schink B (1994) Evidence of reversed electron transport involved in syntrophic butyrate and benzoate oxidation by Syntrophomonas wolfei and Syntrophus buswellii. Arch Microbiol 162:136–142
Wallrabenstein C, Hauschild E, Schink B (1995) Syntrophobacter pfennigii sp. nov., new syntrophically propionate-oxidizing anaerobe growing in pure culture with propionate and sulfate. Arch Microbiol 164:346–352
Wegener G, Krukenberg V, Riedel D, Tegetmeyer HE, Boetius A (2015) Intercellular wiring enables electron transfer between methanotrophic archaea and bacteria. Nature 526:587–U315
Welte CU, Rasigraf O, Vaksmaa A, Versantvoort W, Arshad A, Op den Camp HJ, Jetten MS, Luke C, Reimann J (2016) Nitrate- and nitrite-dependent anaerobic oxidation of methane. Environ Microbiol Rep 8:941–955
Widdel F, Rouviere PE, Wolfe RS (1988) Classification of secondary alcohol-utilizing methanogens including a new thermophilic isolate. Arch Microbiol 150:477–481
Wofford NQ, Beaty PS, McInerney MJ (1986) Preparation of cell-free extracts and the enzymes involved in fatty acid metabolism in Syntrophomonas wolfei. J Bacteriol 167:179–185
Worm P, Stams AJM, Cheng X, Plugge CM (2011) Growth- and substrate-dependent transcription of formate dehydrogenase and hydrogenase coding genes in Syntrophobacter fumaroxidans and Methanospirillum hungatei. Microbiology 157:280–289
Worm P, Koehorst JJ, Visser M, Sedano-Núñez VT, Schaap PJ, Plugge CM, Sousa DZ, Stams AJM (2014) A genomic view on syntrophic versus non-syntrophic lifestyle in anaerobic fatty acid degrading communities. Biochim Biophys Acta 1837:2004–2016
Wu C, Liu X, Dong X (2006) Syntrophomonas cellicola sp. nov., a spore-forming syntrophic bacterium isolated from a distilled-spirit-fermenting cellar, and assignment of Syntrophospora bryantii to Syntrophomonas bryantii comb. nov. Int J Syst Evol Microbiol 56:2331–2335
Zehnder AJB (1978) Ecology of methane formation. In: Mitchell R (ed) Water pollution microbiology, vol 2. Wiley, London, pp 349–376
Zhang C, Liu X, Dong X (2004) Syntrophomonas curvata sp. nov., an anaerobe that degrades fatty acids in co-culture with methanogens. Int J Syst Evol Microbiol 54:969–973
Zhang C, Liu X, Dong X (2005) Syntrophomonas erecta sp. nov., a novel anaerobe that syntrophically degrades short-chain fatty acids. Int J Syst Evol Microbiol 55:799–803
Zhou S, Xu J, Yang G, Zhuang L (2014) Methanogenesis affected by the co-occurrence of iron(III)oxides and humic substances. FEMS Microbial Ecol 88:107–120
Zinder SH, Koch M (1984) Non-aceticlastic methanogenesis from acetate: acetate oxidation by a thermophilic syntrophic coculture. Arch Microbiol 138:263–272
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Müller, N., Timmers, P., Plugge, C.M., Stams, A.J.M., Schink, B. (2018). Syntrophy in Methanogenic Degradation. In: Hackstein, J. (eds) (Endo)symbiotic Methanogenic Archaea. Microbiology Monographs, vol 19. Springer, Cham. https://doi.org/10.1007/978-3-319-98836-8_9
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