Methanogens and Methanogenesis in Hypersaline Environments

Living reference work entry
Part of the Handbook of Hydrocarbon and Lipid Microbiology book series (HHLM)

Abstract

Methanogenesis is controlled by redox potential and permanency of anaerobic conditions; and in hypersaline environments, the high concentration of terminal electron acceptors, particularly sulfate, is an important controlling factor. This is because sulfate-reducing microbes, compared with methanogens, have a greater affinity for, and energy yield from, competitive substrates like hydrogen and acetate. However, hypersalinity is not an obstacle to methylotrophic methanogenesis; in many cases hypersaline environments have high concentrations of noncompetitive substrates like methylamines, which derive from compatible solutes such as glycine betaine that is synthesized by many microbes inhabiting hypersaline environments. Also, depletion of sulfate, as may occur in deeper sediments, allows increased methanogenesis. On the other hand, increasing salinity requires methanogens to synthesize or take up more compatible solutes at a significant energetic cost. Acetoclastic and hydrogenotrophic methanogens, with their lower energetic yields, are therefore more susceptible than methylotrophic methanogens, which further explains the predominance of methylotrophic methanogens like Methanohalophilus and Methanohalobium spp. in hypersaline environments. There are often deviations from the picture outlined above, which are sometimes difficult to explain. Identifying the role of uncultivated Euryarchaeota in hypersaline environments, elucidating the effects of different ions (which have differential stress effects and potential as electron acceptors), and understanding the effects of salinity on all microbes involved in methane cycling will help us to understand and predict methane production in hypersaline environments. A good demonstration of this is a recent discovery of extremely haloalkaliphilic methanogens living in hypersaline lakes, which utilize the methyl-reducing pathway and form a novel class “Methanonatronarchaeia” in the Euryarchaeota.

References

  1. Antunes A, Ngugi DK, Stingl U (2011) Microbiology of the Red Sea (and other) deep-sea anoxic brine lakes. Environ Microbiol Rep 3:416–433PubMedGoogle Scholar
  2. Boone DR, Mathrani IM, Liu Y, Menaia JAGF, Mah RA, Boone JE (1993) Isolation and characterization of Methanohalophilus portucalensis sp. nov. and DNA reassociation study of the genus Methanohalophilus. Int J Syst Bacteriol 43:430–437Google Scholar
  3. Boone DR (2001) Genus IV Methanohalophilus. In: Garrity GM (ed) Bergey’s manual of systematic bacteriology, The archaea and the deeply branching and phototrophic bacteria, vol 1, 2nd edn. Springer, New York, pp 281–283Google Scholar
  4. Borin S, Brusetti L, Mapelli F, D’Auria G, Brusa T, Marzorati M et al (2009) Sulfur cycling and methanogenesis primarily drive microbial colonization of the highly sulfidic Urania deep hypersaline basin. Proc Natl Acad Sci USA 106:9151–9156PubMedPubMedCentralGoogle Scholar
  5. 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 Methanomassiliicoccales, a Thermoplasmatales-related seventh order of methanogenic archaea that encodes pyrrolysine. BMC Genomics 15:679PubMedPubMedCentralGoogle Scholar
  6. Bräuer SL, Cadillo-Quiroz H, Yashiro E, Yavitt JB, Zinder SH (2006) Isolation of a novel acidophilic methanogen from a peat bog. Nature 442:192–194PubMedGoogle Scholar
  7. Bräuer SL, Cadillo-Quiroz H, Ward RJ, Yavitt JB, Zinder SH (2011) Methanoregula boonei gen. nov., sp. nov., an acidophilic methanogen isolated from an acidic peat bog. Int J Syst Evol Microbiol 61:45–52PubMedGoogle Scholar
  8. Buckley DH, Baumgartner LK, Visscher PT (2008) Vertical distribution of methane metabolism in microbial mats of the Great Sippewissett salt marsh. Environ Microbiol 10:967–977PubMedGoogle Scholar
  9. Carini S, Bano N, LeCleir G, Joye SB (2005) Aerobic methane oxidation and methanotroph community composition during seasonal stratification in Mono Lake, California (USA). Environ Microbiol 7:1127–1138PubMedGoogle Scholar
  10. Charlou JL, Donval JP, Zitter T, Roy N, Jean-Baptiste P, Foucher JP, Woodside J (2003) Evidence of methane venting and geochemistry of brines on mud volcanoes of the eastern Mediterranean Sea. Deep Sea Res I 50:941–958Google Scholar
  11. Conrad R, Frenzel P, Cohen Y (1995) Methane emission from hypersaline microbial mats – lack of aerobic methane oxidation activity. FEMS Microbiol Ecol 16:297–305Google Scholar
  12. Cui M, Ma A, Qi H, Zhuang X, Zhuang G (2015) Anaerobic oxidation of methane: an “active” microbial process. MicrobiologyOpen 4:1–11PubMedGoogle Scholar
  13. Curson ARJ, Todd JD, Sullivan MJ, Johnston AWB (2011) Catabolism of dimethylsulphoniopropionate: microorganisms, enzymes and genes. Nat Rev Microbiol 9:849–859PubMedGoogle Scholar
  14. Cytryn E, Minz D, Oremland RS, Cohen Y (2000) Distribution and diversity of archaea corresponding to the limnological cycle of a hypersaline stratified lake (Solar Lake, Sinai, Egypt). Appl Environ Microbiol 66:3269–3276PubMedPubMedCentralGoogle Scholar
  15. Daffonchio D, Borin S, Brusa T, Brusetti L, van der Wielen PWJJ, Bolhuis H, D’Auria G, Yakimov M, Giuliano L, Tamburini C, Marty D, McGenity TJ, Hallsworth JE, Sass AM, Timmis KN, Tselepides A, de Lange GJ, Huebner A, Thomson J, Varnavas SP, Gasparoni F, Gerber HW, Malinverno E, Corselli C (2006) Stratified prokaryote network in the oxic- anoxic transition of a deep-sea halocline. Nature 440:203–207PubMedGoogle Scholar
  16. Daly RA, Borton MA, Wilkins MJ, Hoyt DW, Kountz DJ, Wolfe RA et al (2016) Microbial metabolisms in a 2.5-km-deep ecosystem created by hydraulic fracturing in shales. Nat Microbiol 1:16146Google Scholar
  17. Davidova IA, Harmsen HJM, Stams AJM, Belyaev SS, Zehnder AJB (1997) Taxonomic description of Methanococcoides euhalobius and its transfer to the Methanohalophilus genus. Antonie Van Leeuwenhoek 71:313–318PubMedGoogle Scholar
  18. Dong HL, Zhang GX, Jiang HC, Yu BS, Chapman LR, Lucas CR, Fields MW (2006) Microbial diversity in sediments of saline Qinghai Lake, China: linking geochemical controls to microbial ecology. Microb Ecol 51:65–82PubMedGoogle Scholar
  19. Eder W, Schmidt M, Koch M, Garbe-Schonberg D, Huber R (2002) Prokaryotic phylogenetic diversity and corresponding geochemical data of the brine- seawater interface of the Shaban Deep, Red Sea. Environ Microbiol 4:758–763PubMedGoogle Scholar
  20. 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 350:434–438PubMedGoogle Scholar
  21. García-Maldonado JQ, Bebout BM, Everroad RC, Lopez-Cortes A (2015) Evidence of novel phylogenetic lineages of methanogenic archaea from hypersaline microbial mats. Microb Ecol 69:106–117PubMedGoogle Scholar
  22. Giani D, Jannsen D, Schostak V, Krumbein WE (1989) Methanogenesis in a saltern in the Bretagne (France). FEMS Microbiol Ecol 62:143–150Google Scholar
  23. Gramain A, Chong Díaz G, Demergasso C, Lowenstein TK, McGenity TJ (2011) Archaeal diversity along a subterranean salt core from the Salar Grande (Chile). Environ Microbiol 13:2105–2121PubMedGoogle Scholar
  24. Grant WD, Tindall BJ (1986) The alkaline saline environ- ment. In: Herbert RA, Codd GA (eds) Microbes in extreme environments. Academic, London, pp 25–54Google Scholar
  25. Gray N, Sherry A, Larter S, Erdmann M, Leyris J, Liengen T, Beeder J, Head IM (2009) Biogenic methane production in formation waters from a large gas field in the North Sea. Extremophiles 13:511–519PubMedGoogle Scholar
  26. Guan Y, Hikmawan T, Antunes A, Ngugi DK, Stingl U (2015) Diversity of methanogens and sulfate-reducing bacteria in the interfaces of five deep-sea anoxic brines of the Red Sea. Res Microbiol 166:688–699PubMedGoogle Scholar
  27. Hallsworth JE, Yakimov MM, Golyshin PN, Gillion JLM, D’Auria G, de Lima Alves F, La Cono V, Genovese M, McKew BA, Hayes SL, Harris G, Giuliano L, Timmis KN, McGenity TJ (2007) Limits of life in MgCl2-containing environments: chaotropicity defines the window. Environ Microbiol 9:801–813PubMedGoogle Scholar
  28. Harris JK, Caporaso JG, Walker JJ, Spear JR, Gold NJ, Robertson CE et al (2013) Phylogenetic stratigraphy in the Guerrero Negro hypersaline microbial mat. ISME J 7:50–60PubMedGoogle Scholar
  29. Heyer J, Berger U, Hardt M, Dunfield PF (2005) Methylohalobius crimeensis gen. nov., sp. nov., a moderately halophilic, methanotrophic bacterium isolated from hypersaline lakes of Crimea. Int J Syst Evol Microbiol 55:1817–1826PubMedGoogle Scholar
  30. Hoehler TM, Bebout BM, Des Marais DJ (2001) The role of microbial mats in the production of reduced gases on the early Earth. Nature 412:324–327PubMedGoogle Scholar
  31. Hovorka S (1987) Depositional environments of marine-dominated bedded halite, Permian San Andres formation, Texas. Sedimentology 34:1029–1054Google Scholar
  32. Iversen N, Oremland RS, Klug MJ (1987) Big Soda Lake (Nevada). 3. Pelagic methanogenesis and anaerobic methane oxidation. Limnol Oceanogr 32:804–814Google Scholar
  33. Jahnke LL, Orphan VJ, Embaye T, Turk KA, Kubo M, Summons RE, Des Marais DJ (2008) Lipid biomarker and phylogenetic analyses to reveal archaeal biodiversity and distribution in a hypersaline microbial mat and underlying sediment. Geobiology 6:394–410PubMedGoogle Scholar
  34. Jiang H, Dong H, Yu B, Liu X, Li Y, Ji S, Zhang CL (2007) Microbial response to salinity change in Lake Chaka, a hypersaline lake on Tibetan plateau. Environ Microbiol 9:2603–2621PubMedGoogle Scholar
  35. Joye SB, Connell TL, Miller LG, Oremland RS, Jellison RS (1999) Oxidation of ammonia and methane in an alkaline, saline lake. Limnol Oceanogr 44:178–188Google Scholar
  36. Joye SB, MacDonald IR, Montoya JP, Peccini M (2005) Geophysical and geochemical signatures of Gulf of Mexico seafloor brines. Biogeosciences 2:295–309Google Scholar
  37. Joye SB, Samarkin VA, MacDonald IR, Hinrichs K-U, Elvert M, Teske AP, Lloyd KG, Lever MA, Montoya JP, Meile CD (2009) Metabolic variability in seafloor brines revealed by carbon and sulphur dynamics. Nat Geosci 2:349–354Google Scholar
  38. Kelley CA, Poole JA, Tazaz AM, Chanton JP, Bebout BM (2012) Substrate limitation for methanogenesis in hypersaline environments. Astrobiology 12:89–97PubMedGoogle Scholar
  39. Kelley CA, Nicholson BE, Beaudoin CS, Detweiler AM, Bebout BM (2014) Trimethylamine and organic matter additions reverse substrate limitation effects on the δ13C values of methane produced in hypersaline microbial mats. Appl Environ Microbol 80:7316–7323Google Scholar
  40. Kiene RP, Visscher PT (1987) Production and fate of methylated sulfur compounds from methionine and dimethylsulfoniopropionate in anoxic salt marsh sediments. Appl Environ Microbiol 53:2426–2434PubMedPubMedCentralGoogle Scholar
  41. Kiene RP, Oremland RS, Catena A, Miller LG, Capone DG (1986) Metabolism of reduced methylated sulfur compounds in anaerobic sediments and by a pure culture of an estuarine methanogen. Appl Environ Microbiol 52:1037–1045PubMedPubMedCentralGoogle Scholar
  42. King GM (1988) Methanogenesis from methylated amines in a hypersaline algal mat. Appl Environ Microbiol 54:130–136PubMedPubMedCentralGoogle Scholar
  43. Kirk MF, Wilson BH, Marquart KA, Zeglin LH, Vinson DS, Flynn TM (2015) Solute concentrations influence microbial methanogenesis in coal-bearing strata of the Cherokee basin, USA. Front Microbiol 6:1287PubMedPubMedCentralGoogle Scholar
  44. Krumgalz BS, Millero FJ (1982) Physico-chemical study of the Dead Sea waters. I. Activity coefficients of major ions in Dead Sea water. Mar Chem 11:209–222Google Scholar
  45. Kulp TR, Han S, Saltikov CW, Lanoil BD, Zargar K, Oremland RS (2007) Effects of imposed salinity gradients on dissimilatory arsenate reduction, sulfate reduction, and other microbial processes in sediments from two California soda lakes. Appl Environ Microbiol 73:5130–5137PubMedPubMedCentralGoogle Scholar
  46. La Cono V, Smedile F, Bortoluzzi G, Arcadi E, Maimone G, Messina E et al (2011) Unveiling microbial life in new deep-sea hypersaline Lake Thetis. Part I: prokaryotes and environmental settings. Environ Microbiol 13:2250–2268PubMedGoogle Scholar
  47. La Cono V, Arcadi E, La Spada G (2015) A three-component microbial consortium from deep-sea salt-saturated anoxic Lake Thetis links anaerobic glycine betaine degradation with methanogenesis. Microorganisms 3:500–517PubMedPubMedCentralGoogle Scholar
  48. Lai M-C, Sowers KR, Robertson DE, Roberts MF, Gunsalus RP (1991) Distribution of compatible solutes in the halophilic methanogenic archaebacteria. J Bacteriol 173:5352–5358PubMedPubMedCentralGoogle Scholar
  49. Lazar CS, Parkes RJ, Cragg BA, L’Haridon S, Toffin L (2011) Methanogenic diversity and activity in hypersaline sediments of the centre of the Napoli mud volcano, Eastern Mediterranean Sea. Environ Microbiol 13:2078–2091PubMedGoogle Scholar
  50. Ley RE, Harris JK, Wilcox J, Spear JR, Miller SR, Bebout BM, Maresca JA, Bryant DA, Sogin ML, Pace NR (2006) Unexpected diversity and complexity of the Guerrero Negro hypersaline microbial mat. Appl Environ Microbiol 72:3685–3695PubMedPubMedCentralGoogle Scholar
  51. L’Haridon S, Chalopin M, Colombo D, Toffin L (2014) Methanococcoides vulcani sp. nov., a marine methylotrophic methanogen that uses betaine, choline and N,N-dimethylethanolamine for methanogenesis, isolated from a mud volcano, and emended description of the genus Methanococcoides. Int J Syst Evol Microbiol 64:1978–1983PubMedGoogle Scholar
  52. Lin JL, Joye SB, Scholten JCM, Schafer H, McDonald IR, Murrell JC (2005) Analysis of methane monooxygenase genes in Mono Lake suggests that increased methane oxidation activity may correlate with a change in methanotroph community structure. Appl Environ Microbiol 71:6458–6462PubMedPubMedCentralGoogle Scholar
  53. Liu Y, Boone DR, Chay C (1990) Methanohalophilus oregonense sp. nov., a methylotrophic methanogen from an alkaline, saline aquifer. Int J Syst Bacteriol 40:111–116Google Scholar
  54. Lloyd KG, Lapham L, Teske A (2006) An anaerobic methane-oxidizing community of ANME-1b Archaea in hypersaline Gulf of Mexico sediments. Appl Environ Microbiol 72:7218–7230PubMedPubMedCentralGoogle Scholar
  55. Lovley DR, Dwyer DF, Klug MJ (1982) Kinetic analysis of competition between sulfate reducers and methanogens for hydrogen in sediments. Appl Environ Microbiol 45:187–192Google Scholar
  56. Lozupone CA, Knight R (2007) Global patterns in bacterial diversity. Proc Natl Acad Sci U S A 104:11436–11440PubMedPubMedCentralGoogle Scholar
  57. MacDonald IR, Reilly JF, Guinasso NL, Brooks JM, Carney RS, Bryant WA, Bright TJ (1990) Chemosynthetic mussels at a brine-filled pockmark in the northern Gulf of Mexico. Science 248:1096–1099PubMedGoogle Scholar
  58. McGenity TJ (2010) Methanogens and methanogenesis in hypersaline environments. In: Timmis KN (ed) Handbook of hydrocarbon and lipid microbiology. Springer, Berlin, pp 666–680Google Scholar
  59. McGenity TJ, Oren A (2012) Hypersaline environments. In: Bell EM (ed) Life at extremes: environments, organisms and strategies for survival. CAB International, Wallingford, pp 402–437Google Scholar
  60. McGenity TJ, Gemmell RT, Grant WD, Stan-Lotter H (2000) Origins of halophilic microorganisms in ancient salt deposits. Environ Microbiol 2:243–250PubMedGoogle Scholar
  61. McKay CP, Rask JC, Detweiler AM, Bebout BM, Everroad RC, Lee JZ et al (2016) An unusual inverted saline microbial mat community in an interdune sabkha in the Rub’ al Khali (the Empty Quarter), United Arab Emirates. PLoS One 11:e0150342PubMedPubMedCentralGoogle Scholar
  62. Maignien L, Parkes RJ, Cragg B, Niemann H, Knittel K, Coulon S, Akhmetzhanov A, Boon N (2013) Anaerobic oxidation of methane in hypersaline cold seep sediments. FEMS Microbiol Ecol 83:214–231PubMedGoogle Scholar
  63. Martens CS, Chanton JP, Paull CK (1991) Biogenic methane from abyssal brine seeps at the base of the Florida escarpment. Geology 19:851–854Google Scholar
  64. Marvin diPasquale M, Oren A, Cohen Y, Oremland RS (1999) Radiotracer studies of bacterial methanogen- esis in sediments from the Dead Sea and Solar Lake (Sinai). In: Oren A (ed) Microbiology and biogeochemistry of hypersaline environments. CRC Press, Boca Raton, pp 149–160Google Scholar
  65. Mathrani IM, Boone DR, Mah RA, Fox GE, Lau PP (1988) Methanohalophilus zhilinae sp. nov., an alkaliphilic, halophilic, methylotrophic methanogen. Int J Syst Bacteriol 38:139–142PubMedGoogle Scholar
  66. Mwirichia R, Alam I, Rashid M, Vinu M, Ba-Alawi W, Kamau AA, Ngugi DK, Göker M, Klenk H-P, Bajic V, Stingl U (2016) Metabolic traits of an uncultured archaeal lineage – MSBL1- from brine pools of the Red Sea. Sci Rep 6:19181PubMedPubMedCentralGoogle Scholar
  67. Michaelis WA, Jenisch A, Richnow HH (1990) Hydrothermal petroleum generation in Red Sea sediments from the Kebrit and Shaban Deeps. Appl Geochem 5:103–114Google Scholar
  68. Mouné S, Caumette P, Matheron R, Willison JC (2003) Molecular sequence analysis of prokaryotic diversity in the anoxic sediments underlying cyanobacterial mats of two hypersaline ponds in Mediterranean salterns. FEMS Microbiol Ecol 44:117–130PubMedGoogle Scholar
  69. Naehr TH, Eichhubl P, Orphan VJ, Hovland M, Paull CK, Ussler P III, Lorenson TD, Greene HG (2007) Authigenic carbonate formation at hydrocarbon seeps in continental margin sediments: a comparative study. Deep Sea Res II 54:1268–1291Google Scholar
  70. Nakatsugawa N (1991) Novel methanogenic archaebacteria which grow in extreme environments. In: Horikoshi K, Grant WD (eds) Superbugs: microorganisms in extreme environments. Japan Scientific Societies Press, Berlin/Tokyo, pp 212–220Google Scholar
  71. Namsaraev BB, Zhilina TN, Kulyrova AV, Gorlenko VM (1999) Bacterial methanogenesis in soda lakes of the southeastern Transbaikal region. Microbiology (Russia) 68:586–591Google Scholar
  72. Nolla-Ardèvol V, Strous M, Sorokin DY, Merkel AY, Tegetmeyer HE (2012) Activity and diversity of haloalkaliphilic methanogens in Central Asian soda lakes. J Biotechnol 161:167–173PubMedGoogle Scholar
  73. Nobu MK, Narihiro T, Kuroda K, Mei R, Liu W-T (2016) Chasing the elusive Euryarchaeota class WSA2: genomes reveal a uniquely fastidious methyl-reducing methanogen. ISME J 10:2478–2487PubMedPubMedCentralGoogle Scholar
  74. Obraztsova AJ, Shipin OV, Bezrukova LV, Beliaev SS (1988) Properties of the coccoid methylotrophic methanogen, Methanococcoides euhalobius sp. nov. Microbiology 56:523–527Google Scholar
  75. Ollivier B, Caumette P, Garcia JL, Mah RA (1994) Anaerobic bacteria from hypersaline environments. Microbiol Rev 58:27–38PubMedPubMedCentralGoogle Scholar
  76. Ollivier B, Cayol JL, Patel BKC, Magot M, Fardeau ML, Garcia JL (1997) Methanoplanus petrolearius sp. nov., a novel methanogenic bacterium from an oil- producing well. FEMS Microbiol Lett 147:51–56PubMedGoogle Scholar
  77. Ollivier B, Fardeau ML, Cayol JL, Magot M, Patel BKC, Prensier G, Garcia JL (1998) Methanocalculus halotolerans gen. nov., sp. nov., isolated from an oil-producing well. Int J Syst Bacteriol 48:821–828PubMedGoogle Scholar
  78. Oremland RS, Marsh LM, Polcin S (1982a) Methane production and simultaneous sulphate reduction in anoxic, salt marsh sediments. Nature 296:143–145Google Scholar
  79. Oremland RS, Marsh L, Desmarais DJ (1982b) Methanogenesis in Big Soda Lake, Nevada: an alkaline, moderately hypersaline desert lake. Appl Environ Microbiol 43:462–468PubMedPubMedCentralGoogle Scholar
  80. Oremland RS, Des Marais DJ (1983) Distribution, abundance and carbon isotopic composition of gaseous hydrocarbons in Big Soda Lake, Nevada: an alkaline, meromictic lake. Geochim Cosmochim Acta 47:2107–2114Google Scholar
  81. Oremland RS, King GM (1989) Methanogenesis in hypersaline environments. In: Cohen Y, Rosenberg E (eds) Microbial Mats: physiological ecology of benthic microbial communities. American Society for Microbiology, Washington, DC, pp 180–190Google Scholar
  82. Oremland RS, Miller LG (1993) Biogeochemistry of natural gases in three alkaline, permanently stratified (meromictic) lakes. USGS Professional Paper, 1570:439–452Google Scholar
  83. Oremland RS, Miller LG, Whiticar MJ (1987) Sources and flux of natural gases from Mono Lake, California. Geochim Cosmochim Acta 51:2915–2929Google Scholar
  84. Oremland RS, Miller LG, Culbertson 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 the Mono Basin of California. In: Oremland RS (ed) Biogeochemistry of global change: radiatively active trace gases. Chapman and Hall, New York, pp 704–741Google Scholar
  85. Oren A (1990) Formation and breakdown of glycine betaine and trimethylamine in hypersaline environments. Antonie Van Leeuwenhoek 58:291–298PubMedGoogle Scholar
  86. Oren A (1999) Bioenergetic aspects of halophilism. Microbiol Mol Biol Rev 63:334–348PubMedPubMedCentralGoogle Scholar
  87. Oren A (2002) Halophilic organisms and their environments. Kluwer Academic Publishers, DordrechtGoogle Scholar
  88. Oren A (2008) Microbial life at high salt concentrations: phylogenetic and metabolic diversity. Saline Systems 4:2PubMedPubMedCentralGoogle Scholar
  89. Oren A (2011) Thermodynamic limits to microbial life at high salt concentrations. Environ Microbiol 13:1908–1923PubMedGoogle Scholar
  90. Orphan VJ, Jahnke LL, Embaye T, Turk KA, Pernthaler A, Summons RE, Des Marais DJ (2008) Characterization and spatial distribution of methanogens and methanogenic biosignatures in hypersaline microbial mats of Baja California. Geobiology 6:376–393PubMedGoogle Scholar
  91. Paterek JR, Smith PH (1988) Methanohalophilus mahii gen. nov., sp. nov., a methylotrophic halophilic methanogen. Int J Syst Bacteriol 38:122–123Google Scholar
  92. Paull CK, Jull AJT, Toolin LJ, Linick T (1985) Stable isotope evidence for chemosynthesis in an abyssal seep community. Nature 317:709–711Google Scholar
  93. Perreault NN, Andersen DT, Pollard WH, Greer CW, Whyte LG (2007) Characterization of the prokaryotic diversity in cold saline perennial springs of the Canadian High Arctic. Appl Environ Microbiol 73:1532–1543PubMedPubMedCentralGoogle Scholar
  94. Pironon J, Pagel M, Lėvêque MH, Mogė M (1995a) Organic inclusions in salt. Part 1. Solid and liquid organic matter, carbon dioxide and nitrogen species in fluid inclusions from the Bresse Basin (France). Org Geochem 23:391–402Google Scholar
  95. Pironon J, Pagel M, Walgenwitz F, Barrės O (1995b) Organic inclusions in salt. Part 2. Oil, gas and ammonium in inclusions from the Gabon margin. Org Geochem 23:739–750Google Scholar
  96. Roberts MF (2005) Organic compatible solutes of halotolerant and halophilic microorganisms. Saline Systems 1:5PubMedPubMedCentralGoogle Scholar
  97. Roedder E (1984) The fluids in salt. Am Mineral 69:413–439Google Scholar
  98. Roveri M, Flecker R, Krijgsman W, Lofi J, Lugli S, Manzi V, Sierro FJ, Bertini A, Camerlenghi A, De Lange G, Govers R, Hilgen FJ, Hübscher C, Meijer PT, Stoica M (2014) The Messinian salinity crisis: past and future of a great challenge for marine sciences. Mar Geol 352:25–58Google Scholar
  99. Saghaï A, Gutiérrez-Preciado A, Deschamps P, Moreira D, Bertolino P, Ragon M, López-García P (2017) Unveiling microbial interactions in stratified mat communities from a warm saline shallow pond. Environ Microbiol 19:2405.  https://doi.org/10.1111/1462-2920.13754CrossRefPubMedGoogle Scholar
  100. Scholten JCM, Joye SB, Hollibaugh JT, Murrell JC (2005) Molecular analysis of the sulfate reducing and archaeal community in a meromictic soda lake (Mono Lake, California) by targeting 16S rRNA, mcrA, apsA, and dsrAB genes. Microb Ecol 50:29–39PubMedGoogle Scholar
  101. Shih C-J, Lai M-C (2007) Analysis of the AAA+ chaperone clpB gene and stress-response expression in the halophilic methanogenic archaeon Methanohalophilus portucalensis. Microbiology 153:2572–2583PubMedGoogle Scholar
  102. Skyring GW, Lynch RM, Smith GD (1989) Quantitative relationships between carbon, hydrogen, and sulphur metabolism in cyanobacterial mats. In: Cohen Y, Rosenberg E (eds) Microbial mats: physiological ecology of benthic microbial communities. American Society for Microbiology, Washington, DC, pp 170–179Google Scholar
  103. Smith JM, Green SJ, Kelley CA, Prufert-Bebout L, Bebout BM (2008) Shifts in methanogen community structure and function associated with long-term manipulation of sulfate and salinity in a hypersaline microbial mat. Environ Microbiol 10:386–394PubMedGoogle Scholar
  104. Sokolov AP, Trotsenko YA (1995) Methane consumption in (hyper)saline habitats of Crimea (Ukraine). FEMS Microbiol Ecol 18:299–304Google Scholar
  105. Sørensen KB, Canfield DE, Oren A (2004) Salinity responses of benthic microbial communities in a solar saltern (Eilat, Israel). Appl Environ Microbiol 70:1608–1616PubMedPubMedCentralGoogle Scholar
  106. Sørensen K, Øeháková K, Zapomìlová E, Oren A (2009) Distribution of benthic phototrophs, sulfate reducers, and methanogens in two adjacent salt ponds in Eilat, Israel. Aquat Microb Ecol 56:275–284Google Scholar
  107. Sorokin DY, Abbas B, Geleijnse M, Pimenov NV, Sukhacheva MV, van Loosdrecht MCM (2015a) Methanogenesis at extremely haloalkaline conditions in soda lakes of Kulunda Steppe (Altai, Russia). FEMS Microbiol Ecol 91.  https://doi.org/10.1093/femsec/fiv016
  108. Sorokin DY, Abbas BA, Sinninghe Damsté JS, Sukhacheva MV, van Loosdrecht MCM (2015b) Methanocalculus alkaliphilus sp. nov., and Methanosalsum natronophilus sp. nov., novel haloalkaliphilic methanogens from hypersaline soda lakes. Int J Syst Evol Microbiol 65:3739–3745PubMedGoogle Scholar
  109. Sorokin DY, Banciu H, Muyzer G (2015c) Functional microbiology of soda lakes. Curr Opin Microbiol 25:88–96PubMedGoogle Scholar
  110. Sorokin DY, Abbas B, Geleijnse M, Kolganova TV, Kleerebezem R, van Loosdrecht MCM (2016) Syntrophic associations from hypersaline soda lakes converting organic acids and alcohols to methane at extremely haloalkaline conditions. Environ Microbiol 18:3189–3202PubMedGoogle Scholar
  111. Sorokin DY, Makarova K, Abbas B, Ferrer M, Golyshin PN, Galinski EA, Ciordia S, Mena MC, Merkel AY, Wolf YI, van Loosdrecht MCM, Koonin EV (2017) Discovery of extremely halophilic methyl-reducing euryarchaea provides insight into the evolutionary origin of methanogenesis. Nat Microbiol 2:17081.  https://doi.org/10.1038/nmicrobiol.2017.81CrossRefPubMedPubMedCentralGoogle Scholar
  112. Spring S, Scheuner C, Lapidus A, Lucas S, Del Rio TG, Tice H et al. (2010) The genome sequence of Methanohalophilus mahii SLPT reveals differences in the energy metabolism among members of the Methanosarcinaceae inhabiting freshwater and saline environments. Archaea. Article ID:690737Google Scholar
  113. Stevenson A, Cray JA, Williams JP, Santos R, Sahay R, Neuenkirchen N et al (2015) Is there a common water-activity limit for the three domains of life? ISME J 9:1333–1351PubMedGoogle Scholar
  114. Vandaele AC, Neefs E, Drummond R, Thomas IR, Daerden F, Lopez-Moreno J-J et al (2015) Science objectives and performances of NOMAD, a spectrometer suite for the ExoMars TGO mission. Planet Space Sci 119:233–249Google Scholar
  115. van der Wielen PWJJ, Bolhuis H, Borin S, Daffonchio D, Corselli C, Giuliano L, de Lange GJ, Huebner A, Varnavas SP, Thomson J, Tamburini C, Marty D, McGenity TJ, Timmis KN (2005) The enigma of prokaryotic life in deep hypersaline anoxic basins. Science 307:121–123PubMedGoogle Scholar
  116. van Leerdam RC, Bonilla-Salinas M, de Bok FAM, Bruning H, Lens PNL, Stams AJM, Janssen AJH (2008) Anaerobic methanethiol degradation and methanogenic community analysis in an alkaline (pH 10) biological process for liquefied petroleum gas (LPG) desulfurization. Biotechnol Bioeng 101:691–701PubMedGoogle Scholar
  117. 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 1:16170PubMedGoogle Scholar
  118. Waldron PJ, Petsch ST, Martini AM, Nuslein K (2007) Salinity constraints on subsurface archaeal diversity and methanogenesis in sedimentary rock rich in organic matter. Appl Environ Microbiol 73:4171–4179PubMedPubMedCentralGoogle Scholar
  119. Walsh DA, Papke RT, Doolittle WF (2005) Archaeal diversity along a soil salinity gradient prone to disturbance. Environ Microbiol 7:1655–1666PubMedGoogle Scholar
  120. Watkins AJ, Roussel EG, Parkes RJ, Sass H (2014) Glycine betaine as a direct substrate for methanogens (Methanococcoides spp.). Appl Environ Microbiol 80:289–293PubMedPubMedCentralGoogle Scholar
  121. Welsh DT (2000) Ecological significance of compatible solute accumulation by micro-organisms: from single cells to global climate. FEMS Microbiol Rev 24:263–290PubMedGoogle Scholar
  122. Wilms R, Sass H, Köpke B, Cypionka H, Engelen B (2007) Methane and sulfate profiles within the sub-surface of a tidal flat are reflected by the distribution of sulfate-reducing bacteria and methanogenic archaea. FEMS Microbiol Ecol 59:611–621PubMedGoogle Scholar
  123. Winfrey MR, Ward DM (1983) Substrates for sulphate reduction and methane production in hypersaline sediments. Appl Environ Microbiol 45:193–199PubMedPubMedCentralGoogle Scholar
  124. Wong HL, Visscher PT, White RA III, Smith DL, Patterson MM, Burns BP (2017) Dynamics of archaea at fine spatial scales in Shark Bay mat microbiomes. Sci Rep 7:46160PubMedPubMedCentralGoogle Scholar
  125. Wu W-L, Lai S-J, Yang J-T, Chern J, Liang S-Y, Chou C-C et al (2016) Phosphoproteomic analysis of Methanohalophilus portucalensis FDF1T identified the role of protein phosphorylation in methanogenesis and osmoregulation. Sci Rep 6:29013PubMedPubMedCentralGoogle Scholar
  126. Wuchter C, Banning E, Mincer TJ, Drenzek NJ, Coolen MJL (2013) Microbial diversity and methanogenic activity of Antrim Shale formation waters from recently fractured wells. Front Microbiol 4:367PubMedPubMedCentralGoogle Scholar
  127. Yakimov MM, Giuliano L, Cappello S, Denaro R, Golyshin PN (2007a) Microbial community of a hydrothermal mud vent underneath the deep-sea anoxic brine lake Urania (Eastern Mediterranean). Orig Life Evol Biosph 37:177–188PubMedGoogle Scholar
  128. Yakimov MM, La Cono V, Denaro R, D’Auria G, Decembrini F, Timmis KN, Golyshin PN, Giuliano L (2007b) Primary producing prokaryotic communities of brine, interface and seawater above the halocline of deep anoxic lake L’Atalante, Eastern Mediterranean Sea. ISME J 1:743–755PubMedGoogle Scholar
  129. Yakimov MM, La Cono V, Slepak VZ, La Spada G, Arcadi E, Messina E, Borghini M, Monticelli LS, Rojo D, Barbas C, Golyshina OV, Ferrer M, Golyshin PN, Giuliano L (2013) Microbial life in the Lake Medee, the largest deep-sea salt-saturated formation. Sci Rep 3:3554PubMedPubMedCentralGoogle Scholar
  130. Yakimov MM, La Cono V, Spada GL, Bortoluzzi G, Messina E, Smedile F et al (2015) Microbial community of the deep-sea brine Lake Kryos seawater-brine interface is active below the chaotropicity limit of life as revealed by recovery of mRNA. Environ Microbiol 17:364–382PubMedGoogle Scholar
  131. Yu IK, Kawamura F (1987) Halomethanococcus doii gen. nov., sp. nov.: an obligate halophilic methanogenic bacterium from solar salt ponds. J Gen Appl Microbiol 33:303–310Google Scholar
  132. Zavarzin GA, Zhilina TN, Pikuta EV (1996) Secondary anaerobes in haloalkaliphilic communities in lakes of Tuva. Microbiology (Russia) 65:480–486Google Scholar
  133. Zharkov MA (1981) History of paleozoic salt. Springer, BerlinGoogle Scholar
  134. Zhilina TN (1983) New obligate halophilic methane- producing bacterium. Microbiology 52:290–297Google Scholar
  135. Zhilina TN (2001) Genus III Methanohalobium. In: Garrity GM (ed) Bergey’s manual of systematic bacteriology, 2nd edn, vol 1: The archaea and the deeply branching and phototrophic Bacteria. Springer, New York, pp 279–281Google Scholar
  136. Zhilina TN, Zavarzin GA (1987) Methanohalobium evestigatum gen. nov., sp. nov., extremely halophilic methane-producing archaebacteria. Dokl Akad Nauk SSSR 293:464–468Google Scholar
  137. Zhilina TN, Zavarzin GA (1990) Extremely halophilic, methylotrophic, anaerobic bacteria. FEMS Microbiol Rev 87:315–322Google Scholar
  138. Zhilina TN, Zavarzina DG, Kevbrin VV, Kolganova TV (2013) Methanocalculus natronophilus sp. nov., a new alkaliphilic hydrogenotrophic methanogenic archaeon from soda lake and proposal of the new family Methanocalculaceae. Microbiology (Moscow, English translation) 82:698–706Google Scholar
  139. Ziegenbalg SB, Birgel D, Hoffmann-Sell L, Pierre C, Roche JM, Peckmann J (2012) Anaerobic oxidation of methane in hypersaline Messinian environments revealed by 13C-depleted molecular fossils. Chem Geol 292–293:140–148Google Scholar
  140. Zhuang G-C, Elling FJ, Nigro LM, Samarkin V, Joye SB, Teske A, Hinrichs K-U (2016) Multiple evidence for methylotrophic methanogenesis as the dominant methanogenic pathway in hypersaline sediments from the Orca Basin, Gulf of Mexico. Geochim Cosmochim Acta 107:1–20Google Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.School of Biological SciencesUniversity of EssexColchesterUK
  2. 2.Winogradsky Institute of Microbiology, Research Centre of BiotechnologyRussian Academy of SciencesMoscowRussia
  3. 3.Department of BiotechnologyTU DelftDelftThe Netherlands

Personalised recommendations