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Wide diversity of methane and short-chain alkane metabolisms in uncultured archaea

Nature Microbiology volume 4, pages 603–613 (2019)Cite this article

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Abstract

Methanogenesis is an ancient metabolism of key ecological relevance, with direct impact on the evolution of Earth’s climate. Recent results suggest that the diversity of methane metabolisms and their derivations have probably been vastly underestimated. Here, by probing thousands of publicly available metagenomes for homologues of methyl-coenzyme M reductase complex (MCR), we have obtained ten metagenome-assembled genomes (MAGs) belonging to potential methanogenic, anaerobic methanotrophic and short-chain alkane-oxidizing archaea. Five of these MAGs represent under-sampled (Verstraetearchaeota, Methanonatronarchaeia, ANME-1 and GoM-Arc1) or previously genomically undescribed (ANME-2c) archaeal lineages. The remaining five MAGs correspond to lineages that are only distantly related to previously known methanogens and span the entire archaeal phylogeny. Comprehensive comparative annotation substantially expands the metabolic diversity and energy conservation systems of MCR-bearing archaea. It also suggests the potential existence of a yet uncharacterized type of methanogenesis linked to short-chain alkane/fatty acid oxidation in a previously undescribed class of archaea (‘Candidatus Methanoliparia’). We redefine a common core of marker genes specific to methanogenic, anaerobic methanotrophic and short-chain alkane-oxidizing archaea, and propose a possible scenario for the evolutionary and functional transitions that led to the emergence of such metabolic diversity.

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Fig. 1: Placement of nine MAGs described in this study in the reference phylogeny of Archaea.
Fig. 2: Phylogeny of the MCR/MCR-like complex and conservation of important positions in the catalytic site.
Fig. 3: Predicted methane and short-chain alkane metabolism of the MAGs described in this study, with the exception of NM1, which is presented in Fig. 4, and NM2, which has a low completeness.
Fig. 4: Predicted methane, short-chain alkane and long/medium-chain fatty acid metabolism of the two MAGs NM1a (‘Ca. Methanoliparum thermophilum’ completeness of 92.5%) and NM1b (‘Ca. Methanolliviera hydrocarbonicum’ completeness of 90.2%) belonging to the candidate class ‘Ca. Methanoliparia’.

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Data availability

MAG sequences are available in the BioProject PRJNA472146 and Biosamples SAMN10387997, SAMN10390728, SAMN10390732, SAMN10390733, SAMN10390735, SAMN10390736, SAMN10390737, SAMN10390738, SAMN10390739. NM2 sequences corresponding to markers reported in Table 2 are deposited under MK202738 to MK202758.

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Acknowledgements

We thank R. Thauer for feedback on an earlier version of the manuscript. G.B. acknowledges support from the Institut Pasteur through a Roux-Cantarini fellowship. P.S.A. is supported by a PhD fellowship from Paris Diderot University and by funds from the PhD Programme ‘Frontières du Vivant (FdV)-Programme Bettencourt’. S.G. acknowledges funding from the French National Agency for Research Grant ArchEvol (No. ANR-16-CE02-0005-01). This work used the computational and storage services (TARS cluster) provided by the IT department at Institut Pasteur, Paris. S.J.H. acknowledges support from the US Department of Energy (DOE) JGI supported by the Office of Science of US DOE Contract No. DE-AC02–05CH11231, the Natural Sciences and Engineering Research Council (NSERC) of Canada, Genome British Columbia, Genome Canada, Canada Foundation for Innovation (CFI) and the Tula Foundation. I.N.S.-G. and V.M.d.O. are grateful to São Paulo Research Foundation—FAPESP (process Nos. 2011/14501-6 and 2013/20436-8) and Petrobras for financial support and to N. Gray and I. Head from the School of Civil Engineering and Geosciences at Newcastle University for lab facilities. W-J.L. was supported by Key Projects of Ministry of Science and Technology (MOST) (Nos. 2013DFA31980 and 2015FY110100). G.M. was supported by the ERC Advanced Grant PARASOL (No. 322551). L.J.M. appreciates funding from the NASA Postdoctoral Programme through the NASA Astrobiology Institute and W.P.I. was supported by the Montana Agricultural Experiment Station (Project No. 911300).

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Authors and Affiliations

  1. Department of Microbiology, Unit Evolutionary Biology of the Microbial Cell, Institut Pasteur, Paris, France

    Guillaume Borrel, Panagiotis S. Adam & Simonetta Gribaldo

  2. Université Paris Diderot, Sorbonne Paris Cité, Paris, France

    Panagiotis S. Adam

  3. Center for Biofilm Engineering, Montana State University, Bozeman, MT, USA

    Luke J. McKay

  4. Department of Earth and Planetary Sciences, University of California, Berkeley, CA, USA

    Lin-Xing Chen, Christian M. K. Sieber & Jillian F. Banfield

  5. Microbial Resources Division, Research Center for Chemistry, Biology and Agriculture, Campinas University—UNICAMP, Campinas, Sao Paolo, Brazil

    Isabel Natalia Sierra-García & Valéria Maia de Oliveira

  6. Department of Energy Joint Genome Institute, Walnut Creek, CA, USA

    Christian M. K. Sieber

  7. Bioinformatics and Biostatistics Hub, C3BI, Institut Pasteur, Paris, France

    Quentin Letourneur & Amine Ghozlane

  8. Department of Environmental Science, Policy, and Management, University of California, Berkeley, CA, USA

    Gary L. Andersen

  9. State Key Laboratory of Biocontrol and Guangdong Provincial Key Laboratory of Plant Resources, School of Life Sciences, Sun Yat-Sen University, Guangzhou, China

    Wen-Jun Li

  10. Department of Microbiology & Immunology, ECOSCOPE Training Program, Graduate Program in Bioinformatics, and Genome Sciences and Technology Training Program, University of British Columbia, Vancouver, British Columbia, Canada

    Steven J. Hallam

  11. Microbial Systems Ecology, Department of Freshwater and Marine Ecology, Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, Amsterdam, The Netherlands

    Gerard Muyzer

  12. Department of Land Resources and Environmental Sciences, Montana State University, Bozeman, MT, USA

    William P. Inskeep

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  1. Guillaume Borrel
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Contributions

G.B. and S.G. conceived the study. L.J.M., L-X.C., I.N.S.-G., C.M.K.S., G.L.A., W.-J.L., S.J. H., G.M., V.M.d.O., W.P.I. and J.F.B. sequenced and assembled the metagenomes. G.B. screened the IMG database for McrA and identified these metagenomes. Q.L., A.G. and G.B. developed the pipeline Let-it-bin. G.B. performed the contig binning of NM1a, NM1b, NM2, NM3, NM4, Verst-YHS, and Mnatro-ASL MAGs. L-X.C. carried out the contig binning of ANME-1-THS MAG and C.M.K.S. those of GoM-Arc1-GOS and ANME-2c MAGs. G.B. inferred the metabolism associated to each MAG and performed all phylogenetic analyses. P.S.A. performed the congruence tests. G.B. and S.G. wrote the manuscript. All authors read and commented on the manuscript.

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Correspondence to Guillaume Borrel or Simonetta Gribaldo.

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Supplementary information

Supplementary Information

Supplementary Discussion, Supplementary References, Legends for Supplementary Tables, Supplementary Table 2, Supplementary Table 4, Supplementary Table 5, and Supplementary Figures 1–13.

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Supplementary Table 1

Presence/absence of genes involved in specific substrate utilization, energy metabolism, cofactor biosynthesis, secretion, sulfate assimilation, N2 fixation, dissimilatory reduction of inorganic compounds and motility. Pathways and systems are subdivided into different spreadsheets. In each spreadsheet and for each metagenome-assembled genome, protein accession numbers with the same colour indicate co-localized genes.

Supplementary Table 3

Occurrence in archaea of 38 genes previously suggested to be methanogenesis markers.

Supplementary Table 6

Genomes used to build the archaea reference tree (Fig. 1). The first spreadsheet shows the number of genomes available and selected for the phylogeny, and the second spreadsheet gives the NCBI accession numbers (if any) of the selected genomes.

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Borrel, G., Adam, P.S., McKay, L.J. et al. Wide diversity of methane and short-chain alkane metabolisms in uncultured archaea. Nat Microbiol 4, 603–613 (2019). https://doi.org/10.1038/s41564-019-0363-3

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