Article

Discovery of extremely halophilic, methyl-reducing euryarchaea provides insights into the evolutionary origin of methanogenesis

  • Nature Microbiology 2, Article number: 17081 (2017)
  • doi:10.1038/nmicrobiol.2017.81
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Abstract

Methanogenic archaea are major players in the global carbon cycle and in the biotechnology of anaerobic digestion. The phylum Euryarchaeota includes diverse groups of methanogens that are interspersed with non-methanogenic lineages. So far, methanogens inhabiting hypersaline environments have been identified only within the order Methanosarcinales. We report the discovery of a deep phylogenetic lineage of extremophilic methanogens in hypersaline lakes and present analysis of two nearly complete genomes from this group. Within the phylum Euryarchaeota, these isolates form a separate, class-level lineage ‘Methanonatronarchaeia’ that is most closely related to the class Halobacteria. Similar to the Halobacteria, ‘Methanonatronarchaeia’ are extremely halophilic and do not accumulate organic osmoprotectants. The high intracellular concentration of potassium implies that ‘Methanonatronarchaeia’ employ the ‘salt-in’ osmoprotection strategy. These methanogens are heterotrophic methyl-reducers that use C1-methylated compounds as electron acceptors and formate or hydrogen as electron donors. The genomes contain an incomplete and apparently inactivated set of genes encoding the upper branch of methyl group oxidation to CO2 as well as membrane-bound heterodisulfide reductase and cytochromes. These features differentiate ‘Methanonatronarchaeia’ from all known methyl-reducing methanogens. The discovery of extremely halophilic, methyl-reducing methanogens related to haloarchaea provides insights into the origin of methanogenesis and shows that the strategies employed by methanogens to thrive in salt-saturating conditions are not limited to the classical methylotrophic pathway.

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Acknowledgements

D.Y.S. was supported by STW (project no. 12226), the Gravitation-SIAM Program (grant no. 24002002 from the Dutch Ministry of Education and Science) and by RFBR (grant no. 16-04-00035). K.S.M., Y.I.W. and E.V.K. are supported by the intramural programme of the US Department of Health and Human Services (to the National Library of Medicine). The proteomic analysis was performed in the Proteomics Facility of The Spanish National Center for Biotechnology (CNB-CSIC), which belongs to ProteoRed (PRB2-ISCIII), supported by grant no. PT13/0001. This project received funding from the European Union's Horizon 2020 research and innovation programme (Blue Growth: Unlocking the potential of Seas and Oceans) under grant agreement no. 634486. This work was further funded by grant no. BIO2014-54494-R from the Spanish Ministry of Economy, Industry and Competitiveness.

Author information

Affiliations

  1. Winogradsky Institute of Microbiology, Centre for Biotechnology, Russian Academy of Sciences, Moscow, Russia

    • Dimitry Y. Sorokin
    •  & Alexander Y. Merkel
  2. Department of Biotechnology, Delft University of Technology, Delft, The Netherlands

    • Dimitry Y. Sorokin
    • , Ben Abbas
    •  & Mark C. M. van Loosdrecht
  3. National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, Maryland 20894, USA

    • Kira S. Makarova
    • , Yuri I. Wolf
    •  & Eugene V. Koonin
  4. Institute of Catalysis, CSIC, Madrid, Spain

    • Manuel Ferrer
  5. School of Biological Sciences, Bangor University, Gwynedd LL57 2UW, UK

    • Peter N. Golyshin
  6. Institute of Microbiology and Biotechnology, Rheinische Friedrich-Wilhelms University, Bonn, Germany

    • Erwin A. Galinski
  7. Proteomics Facility, Centro Nacional de Biotecnología, CSIC, Madrid, Spain

    • Sergio Ciordia
    •  & María Carmen Mena

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Contributions

D.Y.S. performed the fieldwork, the sediment activity incubations, enrichment and isolation of pure cultures and microbiological investigation of enriched and pure cultures. B.A. and A.Y.M. analysed the mcrA and 16S rRNA genes in sediments and methanogenic cultures. M.F., P.N.G., S.C. and M.C.M.v.L. were responsible for the proteomic analysis. E.A.G. analysed compatible solutes. K.S.M., Y.I.W. and E.V.K. performed genomic analysis and evolutionary reconstructions. D.Y.S., K.S.M. and E.V.K. wrote the paper. M.C.M.v.L. oversaw the project and participated in the data interpretation and discussion.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to Dimitry Y. Sorokin or Eugene V. Koonin.

Supplementary information

PDF files

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    Supplementary information

    Supplementary Figures 1–10; Supplementary Tables 1 and 2; Supplementary Data 1–4.

Excel files

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    Supplementary Table 3

    Comparative genomic analysis based on arCOG assignments.

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    Supplementary Table 4

    Reconstruction of gene gain and loss.

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    Supplementary Table 5

    Isoelectric point calculation data.

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    Supplementary Table 6

    Proteomic analysis for AMET1.

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    Supplementary Table 7

    Proteomic analysis for HMET1.