Environmental Constraints that Limit Methanogenesis

  • Tori Hoehler
  • Nathaniel A. Losey
  • Robert P. Gunsalus
  • Michael J. McInerney
Living reference work entry
Part of the Handbook of Hydrocarbon and Lipid Microbiology book series (HHLM)


Methanogens are active in many different ecosystems, including habitats with biologically-derived organic matter as substrates such as aquatic sediments, wetlands, agricultural or natural soils subject to inundation, sewage digesters, and the anoxic portions of animal digestive tracts. Methanogens are also present in habitats with geochemically-supplied substrates such as hot springs, hydrothermal vents, volcanically-influenced habitats, and, potentially, the deep crustal subsurface. Methanogens as a group tolerate a broad range of physicochemical conditions, including temperatures from −2 °C to 122 °C, pH values of 3.0–10.2, salinities up to halite saturation, and pressures of at least 75 MPa. Globally, variations in methane emissions can be explained to a large degree by variations in temperature and water availability. The distribution and activity of methanogens are constrained by ecological interactions that can be stimulatory or competitive, and by physicochemical factors that act at the biochemical or bioenergetic levels. In addition to the constraints placed on methanogens by physicochemical extremes, methanogen distribution and activity are constrained by the availability of energy and nutrients, the presence of inhibitory molecules (most notably oxygen), and the seawater anion, sulfate, due to competitive ecological interactions. Although methanogen tolerances to individual extremes are documented in culture, and the corresponding biochemical adaptations are understood to varying degrees, the natural environment frequently presents combinations of extreme conditions and energy limitations that may limit methanogen distribution to less than the optimally tolerated range of a single parameter. Little is understood about the compound effects of such extremes, nor the commonalities among them that will ultimately form the basis for predictive models of environmental methanogen population distribution. Future work that targets these questions, through a combination of culture work, “omic” analyses, in situ studies, and conceptual and quantitative models, will be needed to better understand the physiological ecology of methanogens.



This project received support from the UCLA-DOE Institute (DE-FC03-02ER6342) to R.P.G. and National Science Foundation grant 1515843 to M.J.M. and R.P.G. TMH received support through NASA Cooperative Agreement NNA15BB02A (NAI ‘Rock Powered Life’ team).


  1. Abe F (2007) Exploration of the effects of high hydrostatic pressure on microbial growth, physiology and survival: perspectives from piezophysiology. Biosci Biotechnol Biochem 71:2347–2357PubMedCrossRefGoogle Scholar
  2. Achtnich C, Bak F, Conrad R (1995) Competition for electron donors among nitrate reducers, ferric iron reducers, sulfate reducers, and methanogens in anoxic paddy soil. Biol Fertil Soils 19:65–72CrossRefGoogle Scholar
  3. Bernhardt G, Jaenicke R, Ludeman H-D, Konnig H, Stetter KO (1988) High pressure enhances the growth rate of the thermophilic archaebacterium Methanococcus thermolithotrophicus without extending its temperature range. Appl Environ Microbiol 54:1258–1261PubMedPubMedCentralGoogle Scholar
  4. Bloom AA, Lee-Taylor J, Madronich S, Messenger DJ, Palmer PI, Reay DS, McLeod AR (2010a) Global methane emission estimates from ultraviolet irradiation of terrestrial plant foliage. New Phytol 187:417–425PubMedCrossRefGoogle Scholar
  5. Bloom AA, Palmer PI, Fraser A, Reay DS, Frankenburg C (2010b) Large-scale controls of methanogenesis inferred from methane and gravity spaceborne data. Science 327:322–325PubMedCrossRefGoogle Scholar
  6. Boone DR, Mathrani IM, Liu Y, Menaia FG, Mah RA, Boone JE (1993) Isolation and characterization of Methanohalophilus portucalensis sp. nov. and DNA-reassociation study of Methanohalophilus. Int J Syst Evol Microbiol 43:430–437Google Scholar
  7. Borrel G, O’Toole PW, Harris HMB, Peyret P, Brugère J-F, Gribaldo S (2013) Phylogenomic data support a seventh order of methylotrophic methanogens and provide insights into the evolution of methanogenesis. Genome Biol Evol 5:1769–1780PubMedPubMedCentralCrossRefGoogle Scholar
  8. Borrel G, Parisot N, Harris HMB, Peyretaillade E, Gaci N, Tottey W, Bardot O, Raymann K, Gribaldo S, Peyret P, O’Toole PW, Brugère J-F (2014) Comparative genomics highlights the unique biology of Methanomasssiliicoccales, a Thermoplasmatales-related seventh order of methanogenic archaea that encodes pyrrolysine. BMC Genomics 15:679PubMedPubMedCentralCrossRefGoogle Scholar
  9. Bräuer SL, Cadillo-Quiroz H, Yashiro E, Yavitt JB, Zinder SH (2006) Isolation of a novel acidiphilic methanogen from an acidic peat bog. Nature 442:192–194PubMedCrossRefGoogle Scholar
  10. Bräuer SL, Cadillo-Quiroz H, Ward RJ, Yavitt JB, Zinder SH (2011) Methanoregula boonei gen. nov., sp. nov., an acidiphilic methanogen isolated from an acidic peat bog. Int J Syst Evol Microbiol 61:45–52PubMedCrossRefGoogle Scholar
  11. Burggraf S, Fricke H, Neuner A, Kristjansson J, Rouvier P, Mandelco L, Woese CR, Stetter KO (1990) Methanococcus igneus sp. nov., a novel hyperthermophilic methanogen from a shallow submarine hydrothermal system. Syst Appl Microbiol 13:263–269PubMedCrossRefGoogle Scholar
  12. Cadillo-Quiroz H, Yashiro E, Yavitt JB, Zinder SH (2008) Characterization of the archaeal community in a minerotrophic fen and terminal restriction fragment length polymorphism-directed isolation of a novel hydrogenotrophic methanogen. Appl Environ Microbiol 74:2059–2068PubMedPubMedCentralCrossRefGoogle Scholar
  13. Cadillo-Quiroz H, Yavitt JB, Zinder SH (2009) Methanosphaerula palustris gen. nov., sp. nov., a hydrogenotrophic methanogen isolated from a minerotrophic fen peatland. Int J Syst Evol Microbiol 59:928–935PubMedCrossRefGoogle Scholar
  14. Caviccholi R (2006) Cold-adapted archaea. Nat Rev Microbiol 4:331–343CrossRefGoogle Scholar
  15. Chaban B, Ng SYM, Jarrell KF (2006) Archaeal habitats-from the extreme to ordinary. Can J Microbiol 52:73–116PubMedCrossRefGoogle Scholar
  16. Chong SC, Liu Y, Cummins M, Valentine DL, Boone DR (2002) Methanogenium marinum sp. nov., a H2-utilizing methanogen from Skan Bay, Alaska, and kinetics of H2 utilization. Antonie Van Leeuwenhoek 81:263–270PubMedCrossRefGoogle Scholar
  17. Conrad R (1999) Contribution of hydrogen to methane production and control of hydrogen concentrations in methanogenic soil and sediments. FEMS Microbiol Ecol 28:193–202CrossRefGoogle Scholar
  18. Cord-Ruwisch R, Seitz HJ, Conrad R (1988) The capacity of hydrogenotrophic anaerobic bacteria to compete for traces of hydrogen depends on the redox potential of the terminal electron acceptor. Arch Microbiol 149:350–357CrossRefGoogle Scholar
  19. Dlugokencky EJ, Nisbet EG, Fisher R, Lowry D (2011) Global atmospheric methane: budget, changes, and dangers. Phil Trans R Soc A 369:2058–2072PubMedCrossRefGoogle Scholar
  20. Dridi B, Fardeau M-L, Ollivier B, Raoult D, Drancourt M (2012) Methanomassiliicoccus luminyensis gen. nov., sp. Nov., a methanogenic archaeon isolated from human feces. Int J Syst Evol Microbiol 62:1902–1907PubMedCrossRefGoogle Scholar
  21. Evans PN, Parks DH, Chadwick GL, Robbins SJ, Orphan VJ, Golding SD, Tyson GW (2015) Methane metabolism in the archaeal phylum Bathyarchaeota revealed by genome-centric metagenomics. Science 350:434–438PubMedCrossRefGoogle Scholar
  22. Finke N, Hoehler TM, Jørgensen BB (2007) Hydrogen ‘leakage’ during methanogenesis from methanol and methylamine: implications for anaerobic carbon degradation pathways in aquatic sediments. Environ Microbiol 9:1060–1071PubMedCrossRefGoogle Scholar
  23. Fransmann RD, Springer N, Ludwig W, Conway de Marcio E, Rohde M (1992) A methanogenic archaeon from Ace Lake, Antarctica: Methanococcoides burtonii sp. nov. Syst Appl Microbiol 15:573–581CrossRefGoogle Scholar
  24. Fransmann RD, Liu Y, Balkwill DL, Aldrich HC, Conway de Marcio E, Boone DR (1997) Methanogenium frigidum sp. nov., a psychrophilic H2-using methanogen from Ace Lake, Antarctica. Int J Syst Bacteriol 47:1068–1072CrossRefGoogle Scholar
  25. Harder J (1997) Species-independent maintenance energy and natural population sizes. FEMS Microbiol Ecol 23:39–44CrossRefGoogle Scholar
  26. Hedderich R, Whitman W (2006) Physiology and biochemistry of the methane-producing Archaea. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (eds) The prokaryotes: an evolving electronic resource for the microbial community, 3rd edn, vol 2. Springer, New York, pp 1050–1079CrossRefGoogle Scholar
  27. Hoehler TM (2004) Biological energy requirements as quantitative boundary conditions for life in the subsurface. Geobiology 2:205–215CrossRefGoogle Scholar
  28. Hoehler TM (2005) Biogeochemistry of dihydrogen. In: Sigel A, Sigel H, Sigel RKO (eds) Metal ions in biological systems: biogeochemical cycles of elements. Marcel Dekker, New York, pp 9–48CrossRefGoogle Scholar
  29. Hoehler TM (2007) An energy balance concept of habitability. Astrobiology 7:824–838PubMedCrossRefGoogle Scholar
  30. Hoehler TM, Jørgensen B (2013) Microbial life under extreme energy limitation. Nat Rev 11:83–94Google Scholar
  31. Hoehler TM, Alperin MJ, Albert DB, Martens CS (1998) Thermodynamic control on hydrogen concentrations in anoxic sediments. Geochim Cosmochim Acta 62:1745–1756CrossRefGoogle Scholar
  32. Hoehler TM, Alperin MJ, Albert DB, Martens CS (2001) Apparent minimum free energy requirements for methanogenic Archaea and sulfate-reducing bacteria in an anoxic marine sediment. FEMS Microbiol Ecol 38:33–41CrossRefGoogle Scholar
  33. Huber R, Huber H, Stetter KO (2000) Towards the ecology of hyperthermophiles: biotopes, new isolation strategies and novel metabolic properties. FEMS Microbiol Rev 24:615–623PubMedCrossRefGoogle Scholar
  34. Imachi H, Sekiguchi Y, Kamagata Y, Hanada S, Ohashi A, Harada H (2002) Pelotomaculum thermopropionicum gen. nov., sp. nov., an anaerobic, thermophilic, syntrophic propionate-oxidizing bacterium. Int J Syst Evol Microbiol 52:1729–1735PubMedGoogle Scholar
  35. Jaenicke R, Sterner R (2002) Life at high temperatures. In: Dworkin M, Falkow S, Rosenberg E, Schleifer KH, Stackebrandt E (eds) The prokaryotes, 2nd edn, vol 2. Springer, New York, pp 167–209Google Scholar
  36. Jeanthon C, L’Haridon S, Reysenbach AL, Vernet M, Messner P, Sleytr UB, Prieur D (1998) Methanococcus infernus sp. nov., a novel hyperthermophilic lithotrophic methanogen isolated from a deep-sea hydrothermal vent. Int J Syst Bacteriol 48:913–919PubMedCrossRefGoogle Scholar
  37. Jeanthon C, L’Haridon S, Reysenbach AL, Corre E, Vernet M, Messner P, Sleytr UB, Prieur D (1999) Methanococcus vulcanius sp. nov., a novel hyperthermophilic methanogen isolated from East Pacific Rise and identification of Methanococcus spp. DSM 4213 as Methanococcus fervens sp. nov. Int J Syst Bacteriol 49:583–589PubMedCrossRefGoogle Scholar
  38. Karl DM, Beversdorf L, Björkman KM, Church MJ, Martinez A, DeLong EF (2008) Aerobic production of methane in the sea. Nature Geosci 1:473–478CrossRefGoogle Scholar
  39. Kelley DS et al (2005) A serpentinite-hosted ecosystem: the Lost City hydrothermal field. Science 307:1428–1434PubMedCrossRefGoogle Scholar
  40. Kendall MM, Liu Y, Boone DR (2006a) Butyrate- and propionate-degrading syntrophs from permanently cold marine sediments in Skan Bay, Alaska, and description of Algorimarina butyrica gen. nov., sp. nov. FEMS Microbiol Lett 262:107–114PubMedCrossRefGoogle Scholar
  41. Kendall MM, Liu Y, Sieprawska-Lupa M, Stetter KO, Whitman WB, Boone DR (2006b) Methanococcus aeolicus sp. nov., a mesophilic, methanogenic archaeon from shallow and deep marine sediments. Int J Syst Evol Microbiol 56:1525–1529PubMedCrossRefGoogle Scholar
  42. Kendall MM, Wardlaw GD, Tang CF, Bonin AS, Liu Y, Valentine DL (2007) Diversity of Archaea in marine sediments from Skan Bay, Alaska, including cultivated methanogens and description of Methanogenium boonei. Appl Environ Microbiol 73:407–414PubMedCrossRefGoogle Scholar
  43. Keppler F, Hamilton JTG, Brass M, Röckmann T (2006) Methane emissions from terrestrial plants under aerobic conditions. Nature 439:187–191PubMedCrossRefGoogle Scholar
  44. King GM (1983) Utilization of hydrogen, acetate, and “noncompetitive” substrates by methanogenic bacteria in marine sediments. Geomicrobiol J 3:275–306CrossRefGoogle Scholar
  45. Kotsyurbenko OR (2005) Trophic interactions in the methanogenic microbial community of low-temperature terrestrial ecosystems. FEMS Microbiol Ecol 53:3–13PubMedCrossRefGoogle Scholar
  46. Kotsyurbenko OR, Glagolev MV, Nozhevnikova AN, Conrad R (2001) Competition between homoacetogenic bacteria and methanogenic archaea for hydrogen at low temperature. FEMS Microbiol Ecol 38:153–159CrossRefGoogle Scholar
  47. Krulwich TA (1995) Alkaliphiles: ‘basic’ molecular problems of pH tolerance and bioenergetics. Mol Microbiol 15:403–410PubMedCrossRefGoogle Scholar
  48. Krulwich TA (2000) Alkaliphilic prokaryotes. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (eds) The prokaryotes: an evolving electronic resource for the microbial community, vol 2. Springer, New York, pp 309–336Google Scholar
  49. Krulwich TA, Ito M, Gilmour R, Sturr MG, Guffanti AA, Hicks DB (1996) Energetic problems of extremely alkaliphilic aerobes. Biochim Biophys Acta 1275:21–26PubMedCrossRefGoogle Scholar
  50. Kurr M, Huber R, König H, Jannasch HW, Fricke H, Trincone A, Kristjansson JK, Stetter KO (1991) Methanopyrus kandleri, gen. and sp. nov., represents a novel group of hyperthermophilic methanogens, growing at 110°C. Arch Microbiol 156:239–247CrossRefGoogle Scholar
  51. L’Haridon S, Reysenbach A-L, Banta A, Messner P, Schumann P, Stackebrandt E, Jeanthon C (2003) Methanocaldococcus indicus sp. nov., a novel hyperthermophilic methanogen isolated from the Central Indian Ridge. Int J Syst Evol Microbiol 53:1931–1935PubMedCrossRefGoogle Scholar
  52. Lai MC, Gunsalus RP (1992) Glycine betaine and potassium ion are the major compatible solutes in the extremely halotolerant methanogen Methanohalophilus strain Z7302. J Bacteriol 174:7474–7477PubMedPubMedCentralCrossRefGoogle Scholar
  53. Lai MC, Sowers KR, Robertson DE, Roberts MF, Gunsalus RP (1991) Distribution of compatible solutes in the halophilic methanogenic archaebacteria. J Bacteriol 173:5352–5358PubMedPubMedCentralCrossRefGoogle Scholar
  54. Lauerer G, Kristjansson JK, Langworthy TA, König H, Stetter KO (1986) Methanothermus sociabilis sp. nov., a second species within the Methanothermaceae growing at 97°C. Syst Appl Microbiol 8:100–105CrossRefGoogle Scholar
  55. Liu Y, Boone DR, Choy C (1990) Methanohalophilus oregonensis sp. nov., a methylotrophic methanogen from an alkaline, saline aquifer. Int J Syst Bacteriol 40:111–116CrossRefGoogle Scholar
  56. Liu Y, Whitman WB (2008) Metabolic, phylogenetic, and ecological diversity of the methanogenic Archaea. Ann N Y Acad Sci 1125:171–189PubMedCrossRefGoogle Scholar
  57. Lovley DR, Goodwin S (1988) Hydrogen concentrations as an indicator of the terminal electron-accepting reactions in aquatic sediments. Geochim Cosmochim Acta 52:2993–3003CrossRefGoogle Scholar
  58. Mathrani IM, Boone DR, Mah RA, Fox GE, Lau PP (1988) Methanohalophilus zhilinae, sp. nov. an alkaliphilic, halophilic, methylotrophic methanogen. Int J Syst Bacteriol 38:139–142PubMedCrossRefGoogle Scholar
  59. Mayumi D, Mochimaru H, Tamaki H, Yamamoto K, Yoshioka Y, Suzuki Y, Kamagata Y, Sakata S (2016) Methane production from coal by a single methanogen. Science 354:222–225PubMedCrossRefGoogle Scholar
  60. Mehta MP, Baross JA (2006) Nitrogen fixation at 92 degrees C by a hydrothermal vent archaeon. Science 314:1783–1786PubMedCrossRefGoogle Scholar
  61. Miller JF, Shah NN, Nelson CM, Lulow JM, Clark DS (1988) Pressure and temperature effects on growth and methane production of extreme thermophile Methanococcus jannashii. Appl Environ Microbiol 54:3039–3042PubMedPubMedCentralGoogle Scholar
  62. Mondav R, Woodcroft BJ, Kim E-H, McCalley CK, Hodgkins SB, Crill PM, Chanton J, Hurst GB, VerBerkmoes NC, Saleska SR, Hugenholtz P, Rich VI, Tyson GW (2014) Discovery of a novel methanogen prevalent in thawing permafrost. Nat Comm 5:3212CrossRefGoogle Scholar
  63. Morita RY (2000) Is H2 the universal energy source for long-term survival? Microbial Ecol 38:307–320CrossRefGoogle Scholar
  64. Nilsen RK, Torsvik T, Lien T (1996) Desulfotomaculum thermocisternum sp. nov., a sulfate reducer isolated from a hot North Sea oil reservoir. Int J Syst Bacteriol 46:397–402CrossRefGoogle Scholar
  65. Nisbet EG, Chappellaz J (2009) Shifting gear, quickly. Science 324:477–478PubMedCrossRefGoogle Scholar
  66. Nobu MK, Narihiro T, Kuroda K, Mei R, Liu W-T (2016) Chasing the elusive Eurarchaeota class WSA2: genomes reveal a uniquely fastidious methyl-reducing methanogen. ISME J 10:1–10CrossRefGoogle Scholar
  67. Nozhevnikova AN, Nekrasova V, Ammann A, Zehnder AJB, Wehrli B, Holliger C (2007) Influence of temperature and high acetate concentrations on methanogenensis in lake sediment slurries. FEMS Microbiol Ecol 62:336–344PubMedCrossRefGoogle Scholar
  68. Ollivier B, Caumette P, Garcia JL, Mah RH (1994) Anaerobic bacteria from hypersaline environments. Microbiol Mol Biol Rev. 58:27–38Google Scholar
  69. Oremland RS, Boone DR (1994) Methanolobus taylorii sp. nov., a new methylotrophic, estuarine methanogen. Int J Syst Bacteriol 44:573–575CrossRefGoogle Scholar
  70. Oremland RS, Miller LG, Colbertson CW, Robinson SW, Smith RL, Lovley D, Whiticar MJ, King GM, Kiene RP, Iversen N, Sargent M (1993) Aspects of the biogeochemistry of methane in Mono Lake and Mono Basin of California. In: Oremland RS (ed) Biogeochemistry of global change. Chapman & Hall, New York, pp 704–741CrossRefGoogle Scholar
  71. Oren A (1999) Bioenergetic aspects of halophilism. Microbiol Mol Biol Rev 63:334–348PubMedPubMedCentralGoogle Scholar
  72. Oren A (2001) The bioenergetic basis for the decrease in metabolic diversity at increasing salt concentrations: implications for the functioning of salt lake ecosystems. Hydrobiologia 466:61–72CrossRefGoogle Scholar
  73. Oren A (2002) Diversity of halophilic microorganisms: environments, phylogeny, physiology, and applications. J Ind Microbiol Biotechnol 28:56–63PubMedCrossRefGoogle Scholar
  74. Parshina SN, Ermakova AV, Bomberg M, Detkova EN (2014) Methanospirillum stamsii sp. nov., a psychrotolerant, hydrogenotrophic, methanogenic archaeon isolated from an anaerobic expanded granular sludge bed bioreactor operated at low temperature. Int J Syst Evol Microbiol 64:180–186PubMedCrossRefGoogle Scholar
  75. Patel GB, Sprott GD, Fein JE (1990) Isolation and characterization of Methanobacterium espanolae sp. nov., a mesophilic moderately acidophilic methanogen. Int J Syst Bacteriol 40:12–18CrossRefGoogle Scholar
  76. Paterek JR, Smith PH (1988) Methanohalophilus mahii gen. nov., sp. nov., a methylotrophic halophilic methanogen. Int J Syst Bacteriol 38:122–123CrossRefGoogle Scholar
  77. Price PB, Sowers T (2004) Temperature dependence of metabolic rates for microbial growth, maintenance and survival. Proc Natl Acad Sci USA 101:4631–4636PubMedPubMedCentralCrossRefGoogle Scholar
  78. Ramanathan V, Cicerone RJ, Singh HB, Kiehl JT (1985) Trace gas trends and their potential role in climate change. J Geophys Res 90:5547–5566CrossRefGoogle Scholar
  79. Reeburgh WS (2007) Oceanic methane biogeochemistry. Chem Rev 107:486–513PubMedCrossRefGoogle Scholar
  80. Schink B (1997) Energetics of syntrophic cooperation in methanogenic degradation. Microbiol Mol Biol Rev 61:262–280PubMedPubMedCentralGoogle Scholar
  81. Schink B, Stams AJM (2006) Syntrophism among prokaryotes. In: Dworkin M, Falkow S, Rosenberg E, Schleifer KH, Stackebrandt E (eds) The prokaryotes: an evolving electronic resource for the microbiological community, 3rd edn, vol 2. Springer, New York, pp 309–335CrossRefGoogle Scholar
  82. 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 50:771–779PubMedCrossRefGoogle Scholar
  83. Shock EL, Holland ME (2007) Quantitative habitability. Astrobiology 7:839–851PubMedCrossRefGoogle Scholar
  84. Simankova MV, Parshina SN, Tourova TP, Kolganova TV, Zehnder AB, Nozhevnikova AN (2001) Methanosarcina lacustris sp. nov., a new psychrotolerant methanogenic archaeon from anoxic lake sediments. Syst Appl Microbiol 24:362–367PubMedCrossRefGoogle Scholar
  85. Simankova MV, Kotsyurbenko OR, Lueders T, Nozhevnikova AN, Wagner B, Conrad R, Friedrich MW (2003) Isolation and characterization of new strains of methanogens from cold terrestrial habitats. Syst Appl Microbiol 26:312–318PubMedCrossRefGoogle Scholar
  86. Singh N, Kendall MM, Liu Y, Boone DR (2005) Isolation and characterization of methylotrophic methanogens from anoxic marine sediments in Skan Bay, Alaska: description of Methanococcoides alaskense sp. nov., and emended description of Methanosarcina baltica. Int J Syst Evol Microbiol 55:2531–2538PubMedCrossRefGoogle Scholar
  87. Sorokin DY, Chernyh NA (2016) “Candidatus Desulfonatronobulbus propionicus”: a first haloalkaliphilic member of the order Syntrophobacteriales from soda lakes. Extremophiles 20:895–901PubMedCrossRefGoogle Scholar
  88. Sorokin DY, Abbas BA, Merkel AY, Rijpstra WIC, Sinninghe Damst JS, Sukhacheva MV, van Loosdrecht, MC (2015) Methanocalculus alkaliphilus sp. nov., and Methanosalsum natronophilus sp. nov., novel haloalkaliphilic methanogens from hypersaline soda lakes. Int J Syst Evol Microbiol 65:3739–3745PubMedCrossRefGoogle Scholar
  89. Sorokin DY, Abbas B, Geleijnse M, Kolganova TV, Kleerebezem R, Loosdrecht MCM (2016) Syntrophic associations from hypersaline soda lakes converting organic acids and alcohols to methane at extremely haloalkaline conditions. Environ Microbiol 18:3189–3202PubMedCrossRefGoogle Scholar
  90. Stetter KO, Thomm M, Winter J, Wildgruber G, Huber H, Zillig W, Janécovic D, König H, Palm P, Wunderl S (1981) Methanothermus fervidus, sp. nov., a novel extremely thermophilic methanogen isolated from an Icelandic hot spring. Zentralbl Bakteriol Parasitenkd Infektionskr Hyg Abt 1 Orig Reihe C 2:166–178Google Scholar
  91. 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 46:1131–1137PubMedCrossRefGoogle Scholar
  92. Takai, K, Nealson KN, Horikoshi K (2004) Methanotorris formicicus sp. nov., a novel extremely thermophilic methane-producing archaeon isolated from a black smoker in Central Indian Ridge. Int J Syst Bacteriol 54:1095–1100CrossRefGoogle Scholar
  93. Takai K, Nakamura K, Toki T, Tsunogai U, Miyazaki M, Miyazaki J, Hirayama H, Nakagawa S, Nunoura T, Horikoshi K (2008) Cell proliferation at 122°C and isotopically heavy CH4 production by a hyperthermophilic methanogen under high-pressure cultivation. Proc Natl Acad Sci USA 105:10949–10954PubMedPubMedCentralCrossRefGoogle Scholar
  94. Thamdrup, B (2000) Bacterial manganese and iron reduction in aquatic sediments. Adv Micro Ecol 16:41–84Google Scholar
  95. Thauer RK, Jungermann K, Decker K (1977) Energy conservation in chemotrophic anaerobic bacteria. Bacteriol Rev 41:100–180PubMedPubMedCentralGoogle Scholar
  96. Thauer RK, Kaster A-K, Seedorf H, Buckel W, Heddrich R (2008) Methanogenic archaea: ecologically relevant differences in energy conservation. Nat Rev 6:579–591Google Scholar
  97. Tijhuis L, van Loosdrecht MCM, Heijnen JJ (1993) A thermodynamically based correlation for maintenance Gibbs energy requirements in aerobic and anaerobic chemotrophic growth. Biotechnol Bioeng 42:509–519PubMedCrossRefGoogle Scholar
  98. Turetsky MR, Kotowska A, Bubier J, Dise NB, Crill PM, Hornibrook ERC, Minkkinen K, Moore TR et al (2014) A synthesis of methane emissions from 71 northern, temperate, and subtropical wetlands. Global Change Biol 20:2183–2197CrossRefGoogle Scholar
  99. Ueno Y, Yamada K, Yoshida N, Maruyama S, Isozaki Y (2006) Evidence from fluid inclusions for microbial methanogenesis in the early Archaean era. Nature 440:516–519PubMedCrossRefGoogle Scholar
  100. Vanwonterghem I, Evans PN, Parks DH, Jensen PD, Woodcroft BJ, Hugenholtz P, Tyson GW (2016) Methylotrophic methanogenesis discovered in the archaeal phylum Verstraetearchaeota. Nat Microbiol 1:16170. PubMedCrossRefGoogle Scholar
  101. Ver Eecke HC, Butterfield DA, Huber JA, Lilley MD, Olson EJ, Roe KK, Evans LJ, Merkel AY, Cantin HV, Holden JF (2012) Hydrogen-limited growth of hyperthermophilic methanogens at deep sea hydrothermal vents. Proc Natl Acad Sci USA 109:13674–13679CrossRefGoogle Scholar
  102. von Klein D, Arab H, Völker H, Thomm M (2002) Methanosarcina baltica, sp. nov., a novel methanogen isolated from the Gotland deep of the Baltic Sea. Extremophiles 6:103–110CrossRefGoogle Scholar
  103. Wagman DD, Evans WH, Parker VB, Halo I, Bailey SM, Schumm RH (1968) Selected values of chemical thermodynamic properties, Technical note, vol 270–3. National Bureau of Standards, Washington, DCGoogle Scholar
  104. Wagner D, Schirmack J, Ganzert L, Morozova D, Mangelsdorf K (2013) Methanosarcina soligelidi sp. nov., a desiccation- and freeze-thaw-resistant methanogenic archaeon from a Siberian permafrost-affected soil. Int J Syst Evol Microbiol 63:2986–2991PubMedCrossRefGoogle Scholar
  105. Williams RT, Crawford RL (1984) Methane production in Minnesota peatlands. Appl Environ Microbiol 47:1266–1271PubMedPubMedCentralGoogle Scholar
  106. Yu IK, Kawamura F (1987) Halomethanococcus doii gen. nov., sp. nov.: an obligately halophilic methanogenic bacterium from solar salt ponds. J Gen Appl Microbiol 33:303–310CrossRefGoogle Scholar
  107. Yvon-Durocher G, Allen AP, Bastviken D, Conrad R, Gudasz C, St-Pierre A, Thanh-Duc N, del Giorgio PA (2014) Methane fluxes show consistent temperature dependence across microbial to ecosystem scales. Nature 507:488–491PubMedCrossRefGoogle Scholar
  108. Zehnder AJB, Stumm W (1988) Geochemistry and biogeochemistry of anaerobic habitats. In: Zehnder AJB (ed) Biology of anaerobic microorganisms. Wiley, New York, pp 1–38Google Scholar
  109. Zhang G, Jiang N, Liu X, Dong X (2008) Methanogenesis from methanol at low temperatures by a novel psychrophilic methanogen, “Methanolobus psychrophilus” sp. nov., prevalent in Zoige wetland of the Tibetan plateau. Appl Environ Microbiol 74:6114–6120PubMedPubMedCentralCrossRefGoogle Scholar
  110. Zhilina TH (1983) A new obligate halophilic methane-producing bacterium. Mikrobiologiya 52:375–382Google Scholar
  111. Zhilina TN, Zavarzin GA (1987) Methanohalobium evestigatus, gen. nov., sp. nov., the extremely halophilic methanogenic archaebacterium. Dokl Akad Nauk SSSR 293:464–468Google Scholar
  112. Zhilina TN, Zavarzina DG, Kevbrin VV, Kolganova TV (2013) Methanocalculus natronophilus sp. nov., a new alkaliphilic hydrogenotrophic methanogenic archaeon from a soda lake, and proposal of the new family Methanocalculaceae. Microbiology 82:698–706CrossRefGoogle Scholar
  113. Zhou L, Liu X, Dong X (2014) Methanospirillum psychrodurum sp. nov., isolated from wetland soil. Int J Syst Evol Microbiol 64:638–641PubMedCrossRefGoogle Scholar
  114. Zinder S (1993) Physiological ecology of methanogens. In: Ferry JG Methanogenesis: ecology, physiology, biochemistry and genetics. Chapman & Hall, New York, pp 128–206CrossRefGoogle Scholar

Copyright information

© This is a U.S. Government work and not under copyright protection in the US; foreign copyright protection may apply 2018

Authors and Affiliations

  • Tori Hoehler
    • 1
  • Nathaniel A. Losey
    • 2
  • Robert P. Gunsalus
    • 3
  • Michael J. McInerney
    • 2
  1. 1.Exobiology BranchNASA Ames Research CenterMoffett FieldUSA
  2. 2.Department of Microbiology and Plant BiologyUniversity of OklahomaNormanUSA
  3. 3.Department of Microbiology, Immunology, and Molecular GeneticsUCLALos AngelesUSA

Personalised recommendations