1887

Abstract

Methanogenic enrichments from hypersaline lakes at moderate thermophilic conditions have resulted in the cultivation of an unknown deep lineage of euryarchaeota related to the class Halobacteria . Eleven soda lake isolates and three salt lake enrichment cultures were methyl-reducing methanogens that utilize C1 methylated compounds as electron acceptors and H2 or formate as electron donors, but they were unable to grow on either substrates alone or to form methane from acetate. They are extreme halophiles, growing optimally at 4 M total Na and the first representatives of methanogens employing the ‘salt-in’ osmoprotective mechanism. The salt lake subgroup is neutrophilic, whereas the soda lake isolates are obligate alkaliphiles, with an optimum around pH 9.5. Both grow optimally at 50 °C. The genetic diversity inside the two subgroups is very low, indicating that the soda and salt lake clusters consist of a single genetic species each. The phylogenetic distance between the two subgroups is in the range of distant genera, whereas the distance to other euryarchaea is below 83 % identity of the 16S rRNA gene. These isolates and enriched methanogens, together with closely related environmental clones from hypersaline habitats (the SA1 group), form a novel class-level clade in the phylum Euryarchaeota. On the basis of distinct phenotypic and genetic properties, the soda lake isolates are classified into a new genus and species, Methanonatronarchaeum thermophilum, with the type strain AMET1 (DSM 28684=NBRC 110805=UNIQEM U982), and the salt lake methanogens into a candidate genus and species ‘Candidatus Methanohalarchaeum thermophilum’. These organisms are proposed to form novel family, order and class Methanonatronarchaeaceae fam. nov., Methanonatronarchaeales ord. nov. and Methanonatronarchaeia classis nov., within the phylum Euryarchaeota .

Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.002810
2018-05-29
2019-10-21
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/68/7/2199.html?itemId=/content/journal/ijsem/10.1099/ijsem.0.002810&mimeType=html&fmt=ahah

References

  1. Oremland RS, King GM. Methanogenesis in hypersaline environments. In Cohen Y, Rosenberg E. (editors) Microbial Mats. Physiological Ecology of Benthic Microbial Communities Washington, DC: American Society for Microbiology; 1989; pp. 180– 190
    [Google Scholar]
  2. McGenity TJ. Methanogens and methanogenesis in hypersaline environments. In Timmis KN. (editor) Handbook of Hydrocarbon and Lipid Microbiology Berlin, Heidelberg: Springer-Verlag; 2010; pp. 665– 679 [Crossref]
    [Google Scholar]
  3. Paterek JR, Smith PH. Methanophilus mahii gen. nov., sp. nov., a methylotrophic halophilic methanogen. Int J Syst Bacteriol 1988; 38: 122– 123 [CrossRef]
    [Google Scholar]
  4. Zhilina TN, Zavarzin GA. Methanohalobium evestigatus, gen. nov. sp. nov., the extremely halophilic methanogenic archaebacterium. Dokl Akad Nauk USSR 1987; 293: 464– 468
    [Google Scholar]
  5. Boone DR, Baker CC. Genus VI. Methanosalsum gen. nov. In Boone DR. (editor) Bergey's Manual of Systematic Bacteriology, 2nd ed.vol. 1 New York: Springer-Verlag; pp. 287– 289
    [Google Scholar]
  6. Mathrani IM, Boone DR, Mah RA, Fox GE, Lau PP. Methanohalophilus zhilinae sp. nov., an alkaliphilic, halophilic, methylotrophic methanogen. Int J Syst Bacteriol 1988; 38: 139– 142 [CrossRef] [PubMed]
    [Google Scholar]
  7. Kevbrin VV, Lysenko AM, Zhilina TN. Physiology of alkaliphilic methanogen Z-7936, a new strain of Methanosalsus zhilinae isolated from Lake Magadi. Microbiology 1997; 66: 261– 266
    [Google Scholar]
  8. Sorokin DY, Abbas BA, Sinninghe Damsté JS, Sukhacheva MV, van Loosdrecht MCM. Methanocalculus alkaliphilus sp. nov., and Methanosalsum natronophilus sp. nov., novel haloalkaliphilic methanogens from hypersaline soda lakes. Int J Syst Evol Microbiol 2015; 65: 3739– 3745 [Crossref]
    [Google Scholar]
  9. Lai MC, Sowers KR, Robertson DE, Roberts MF, Gunsalus RP. Distribution of compatible solutes in the halophilic methanogenic archaebacteria. J Bacteriol 1991; 173: 5352– 5358 [CrossRef] [PubMed]
    [Google Scholar]
  10. Menaia J. Osmotics of halophilic methanogenic archaeobacteria. Scholar Archive paper 1992; 133:
    [Google Scholar]
  11. Roberts MF, Lai MC, Gunsalus RP. Biosynthetic pathways of the osmolytes Nε-acetyl-β-lysine, β-glutamine, and betaine in Methanohalophilus strain FDF1 suggested by nuclear magnetic resonance analyses. J Bacteriol 1992; 174: 6688– 6693 [CrossRef] [PubMed]
    [Google Scholar]
  12. Kraegeloh A, Kunte HJ. Novel insights into the role of potassium for osmoregulation in Halomonas elongata. Extremophiles 2002; 6: 453– 462 [CrossRef] [PubMed]
    [Google Scholar]
  13. Youssef NH, Savage-Ashlock KN, McCully AL, Luedtke B, Shaw EI et al. Trehalose/2-sulfotrehalose biosynthesis and glycine-betaine uptake are widely spread mechanisms for osmoadaptation in the Halobacteriales. ISME J 2014; 8: 636– 649 [CrossRef] [PubMed]
    [Google Scholar]
  14. Sorokin DY, Makarova KS, Abbas B, Ferrer M, Golyshin PN et al. Discovery of extremely halophilic, methyl-reducing euryarchaea provides insights into the evolutionary origin of methanogenesis. Nat Microbiol 2017; 2: 17081 [CrossRef] [PubMed]
    [Google Scholar]
  15. Fricke WF, Seedorf H, Henne A, Krüer M, Liesegang H et al. The genome sequence of Methanosphaera stadtmanae reveals why this human intestinal archaeon is restricted to methanol and H2 for methane formation and ATP synthesis. J Bacteriol 2006; 188: 642– 658 [CrossRef] [PubMed]
    [Google Scholar]
  16. Sprenger WW, van Belzen MC, Rosenberg J, Hackstein JH, Keltjens JT. Methanomicrococcus blatticola gen. nov., sp. nov., a methanol- and methylamine-reducing methanogen from the hindgut of the cockroach Periplaneta americana. Int J Syst Evol Microbiol 2000; 50: 1989– 1999 [CrossRef] [PubMed]
    [Google Scholar]
  17. Hedderich R, Whitman WB. Physiology and biochemistry of the methane-producing Archaea. In Rosenberg E. (editor) The Prokaryotes – Prokaryotic Physiology and Biochemistry Berlin, Heidelberg: Springer-Verlag; 2013; pp. 635– 662
    [Google Scholar]
  18. Dridi B, Fardeau ML, Ollivier B, Raoult D, Drancourt M. Methanomassiliicoccus luminyensis gen. nov., sp. nov., a methanogenic archaeon isolated from human faeces. Int J Syst Evol Microbiol 2012; 62: 1902– 1907 [CrossRef] [PubMed]
    [Google Scholar]
  19. Borrel G, Harris HM, Tottey W, Mihajlovski A, Parisot N et al. Genome sequence of "Candidatus Methanomethylophilus alvus" Mx1201, a methanogenic archaeon from the human gut belonging to a seventh order of methanogens. J Bacteriol 2012; 194: 6944– 6945 [CrossRef] [PubMed]
    [Google Scholar]
  20. Iino T, Tamaki H, Tamazawa S, Ueno Y, Ohkuma M et al. Candidatus Methanogranum caenicola: a novel methanogen from the anaerobic digested sludge, and proposal of Methanomassiliicoccaceae fam. nov. and Methanomassiliicoccales ord. nov., for a methanogenic lineage of the class Thermoplasmata. Microbes Environ 2013; 28: 244– 250 [PubMed] [Crossref]
    [Google Scholar]
  21. Borrel G, Parisot N, Harris HM, Peyretaillade E, Gaci N et al. Comparative genomics highlights the unique biology of Methanomassiliicoccales, a Thermoplasmatales-related seventh order of methanogenic archaea that encodes pyrrolysine. BMC Genomics 2014; 15: 679 [CrossRef] [PubMed]
    [Google Scholar]
  22. Paul K, Nonoh JO, Mikulski L, Brune A. "Methanoplasmatales," Thermoplasmatales-related archaea in termite guts and other environments, are the seventh order of methanogens. Appl Environ Microbiol 2012; 78: 8245– 8253 [CrossRef] [PubMed]
    [Google Scholar]
  23. Nobu MK, Narihiro T, Kuroda K, Mei R, Liu WT. Chasing the elusive Euryarchaeota class WSA2: genomes reveal a uniquely fastidious methyl-reducing methanogen. Isme J 2016; 10: 2478– 2487 [CrossRef] [PubMed]
    [Google Scholar]
  24. Evans PN, Parks DH, Chadwick GL, Robbins SJ, Orphan VJ et al. Methane metabolism in the archaeal phylum Bathyarchaeota revealed by genome-centric metagenomics. Science 2015; 350: 434– 438 [CrossRef] [PubMed]
    [Google Scholar]
  25. Vanwonterghem I, Evans PN, Parks DH, Jensen PD, Woodcroft BJ et al. Methylotrophic methanogenesis discovered in the archaeal phylum Verstraetearchaeota. Nat Microbiol 2016; 1: 16170 [CrossRef] [PubMed]
    [Google Scholar]
  26. Weijers JWH, Panoto E, van Bleijswijk J, Schouten S, Balk M et al. Constraints on the biological source(s) of the orphan branched tetraether membrane lipids. Geomicrobiol J 2009; 26: 402– 414 [Crossref]
    [Google Scholar]
  27. Damsté JS, Rijpstra WI, Hopmans EC, Jung MY, Kim JG et al. Intact polar and core glycerol dibiphytanyl glycerol tetraether lipids of group I.1a and I.1b thaumarchaeota in soil. Appl Environ Microbiol 2012; 78: 6866– 6874 [CrossRef] [PubMed]
    [Google Scholar]
  28. Sorokin DY, Kublanov IV, Yakimov MM, Rijpstra WI, Sinninghe Damsté JS. Halanaeroarchaeum sulfurireducens gen. nov., sp. nov., the first obligately anaerobic sulfur-respiring haloarchaeon, isolated from a hypersaline lake. Int J Syst Evol Microbiol 2016; 66: 2377– 2381 [CrossRef] [PubMed]
    [Google Scholar]
  29. Oremland RS, Marsh L, Desmarais DJ. Methanogenesis in big soda lake, nevada: an alkaline, moderately hypersaline desert lake. Appl Environ Microbiol 1982; 43: 462– 468 [PubMed]
    [Google Scholar]
  30. Becker EA, Seitzer PM, Tritt A, Larsen D, Krusor M et al. Phylogenetically driven sequencing of extremely halophilic archaea reveals strategies for static and dynamic osmo-response. PLoS Genet 2014; 10: e1004784 [CrossRef] [PubMed]
    [Google Scholar]
  31. Dawson KS, Freeman KH, Macalady JL. Molecular characterization of core lipids from halophilic archaea grown under different salinity conditions. Org Chem 2012; 48: 1– 8
    [Google Scholar]
  32. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W et al. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 2010; 59: 307– 321 [CrossRef] [PubMed]
    [Google Scholar]
  33. Hordijk W, Gascuel O. Improving the efficiency of SPR moves in phylogenetic tree search methods based on maximum likelihood. Bioinformatics 2005; 21: 4338– 4347 [CrossRef] [PubMed]
    [Google Scholar]
  34. Anisimova M, Gascuel O. Approximate likelihood-ratio test for branches: a fast, accurate, and powerful alternative. Syst Biol 2006; 55: 539– 552 [CrossRef] [PubMed]
    [Google Scholar]
  35. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 2013; 41: D590– D596 [CrossRef] [PubMed]
    [Google Scholar]
  36. Eder W, Schmidt M, Koch M, Garbe-Schönberg D, Huber R. Prokaryotic phylogenetic diversity and corresponding geochemical data of the brine-seawater interface of the Shaban Deep, Red Sea. Environ Microbiol 2002; 4: 758– 763 [CrossRef] [PubMed]
    [Google Scholar]
  37. Ferrer M, Werner J, Chernikova TN, Bargiela R, Fernández L et al. Unveiling microbial life in the new deep-sea hypersaline Lake Thetis. Part II: a metagenomic study. Environ Microbiol 2012; 14: 268– 281 [CrossRef] [PubMed]
    [Google Scholar]
  38. Jiang H, Dong H, Yu B, Liu X, Li Y et al. Microbial response to salinity change in Lake Chaka, a hypersaline lake on Tibetan plateau. Environ Microbiol 2007; 9: 2603– 2621 [CrossRef] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijsem.0.002810
Loading
/content/journal/ijsem/10.1099/ijsem.0.002810
Loading

Data & Media loading...

Supplements

Supplementary File 1

PDF

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error