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Co-occurring genomic capacity for anaerobic methane and dissimilatory sulfur metabolisms discovered in the Korarchaeota

Nature Microbiology volume 4, pages 614–622 (2019)Cite this article

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Abstract

Phylogenetic and geological evidence supports the hypothesis that life on Earth originated in thermal environments and conserved energy through methanogenesis or sulfur reduction. Here we describe two populations of the deeply rooted archaeal phylum Korarchaeota, which were retrieved from the metagenome of a circumneutral, suboxic hot spring that contains high levels of sulfate, sulfide, methane, hydrogen and carbon dioxide. One population is closely related to ‘Candidatus Korarchaeum cryptofilum OPF8’, while the more abundant korarchaeote, ‘Candidatus Methanodesulfokores washburnensis’, contains genes that are necessary for anaerobic methane and dissimilatory sulfur metabolisms. Phylogenetic and ancestral reconstruction analyses suggest that methane metabolism originated in the Korarchaeota, whereas genes for dissimilatory sulfite reduction were horizontally transferred to the Korarchaeota from the Firmicutes. Interactions among enzymes involved in both metabolisms could facilitate exergonic, sulfite-dependent, anaerobic oxidation of methane to methanol; alternatively, ‘Ca. M. washburnensis’ could conduct methanogenesis and sulfur reduction independently. Metabolic reconstruction suggests that ‘Ca. M. washburnensis’ is a mixotroph, capable of amino acid uptake, assimilation of methane-derived carbon and/or CO2 fixation by archaeal type III-b RuBisCO for scavenging ribose carbon. Our findings link anaerobic methane metabolism and dissimilatory sulfur reduction within a single deeply rooted archaeal population and have implications for the evolution of these traits throughout the Archaea.

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Fig. 1: Tetranucleotide frequency display and comparison of genome sequence for three populations of Korarchaeota.
Fig. 2: Phylogeny of the Korarchaeota.
Fig. 3: Possible energy metabolisms for ‘Ca. M. washburnensis’.
Fig. 4: Carbon and intermediate metabolism in the Korarchaeota.

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Data availability

Metagenome sequences used in this study are available on IMG/M (DOE-Joint Genome Institute) under genome identifier 3300005860. Metagenome-assembled genomes are available under NCBI BioProject accession number PRJNA492148. Access to the tSNE-based nucleotide frequency analysis algorithm can be obtained from the Center for Genomics and Bioinformatics at Indiana University. Newick files for three-domain and archaea-only phylogenomic trees are available as Supplementary Data 1–13.

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Acknowledgements

The authors appreciate support from the NASA Postdoctoral Program through the NASA Astrobiology Institute (L.J.M.), the Montana Agricultural Experiment Station (project 911300; W.P.I.), the National Institutes of Health IDeA Program (COBRE grant GM110732; M.D.), the NSF Integrative Graduate Education and Research Traineeship Program (NSF DGE 0654336; Z.J.J.), the W. M. Keck Foundation (L.J.M., M.W.F., K.B.K. and W.P.I.), NSF 1736255 (L.J.M. and M.W.F.) and by the US Department of Energy—Ecosystems and Networks Integrated with Genes and Molecular Assemblies (contract number DE-AC02–05CH11231; M.W.F.). Metagenome sequencing of DNA from Washburn Hot Springs was conducted at the DOE-Joint Genome Institute under the Community Sequencing Program (CSP 701; W.P.I.). Computations were performed on the Hyalite High-Performance Computing System, operated and supported by MSU’s Information Technology Center. We thank the NSF EarthCube ECOGEO RCN (1440066) for metagenomics analysis support and individuals involved in the 2016 ‘Omics Workshop’ at the University of Hawaii; V. Krukenberg, G. Borrel, S. Gribaldo, R. Hatzenpichler, M. Lever and A. Teske for helpful discussions and J. Beam for assistance with sample collection and processing.

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  1. Tom O. Delmont

    Present address: Genoscope, Évry, France

Authors and Affiliations

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

    Luke J. McKay & William P. Inskeep

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

    Luke J. McKay, Matthew W. Fields, Zackary J. Jay & Korinne B. Klingelsmith

  3. Department of Microbiology and Immunology, Montana State University, Bozeman, MT, USA

    Mensur Dlakić & Matthew W. Fields

  4. Department of Medicine, University of Chicago, Chicago, IL, USA

    Tom O. Delmont & A. Murat Eren

  5. Josephine Bay Paul Center, Marine Biological Laboratory, Woods Hole, MA, USA

    A. Murat Eren

  6. Informatics Group, Indiana University, Bloomington, IN, USA

    Douglas B. Rusch

  7. Thermal Biology Institute, Montana State University, Bozeman, MT, USA

    William P. Inskeep

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Contributions

W.P.I. and L.J.M. designed the investigation. W.P.I. and Z.J.J. collected samples and performed initial metagenome processing. L.J.M. and M.D. performed clustering, coverage analyses and phylogenetic analyses. L.J.M., M.W.F. and W.P.I. built metabolic reconstructions. M.D. performed additional metagenome assemblies, phylogenomic, emergent self-organizing maps and sequence reconstruction analyses. T.O.D. and A.M.E. performed pangenomics and microdiversity analyses. M.D., K.B.K. and L.J.M. performed phylogenetic analyses of McrA and DsrAB protein sequences. K.B.K. and L.J.M. performed phylogenetic analysis of mcrA genes. D.B.R. and M.D. assisted with nucleotide frequency analyses. L.J.M., W.P.I. and M.D. wrote the manuscript and responses to reviewer comments. All authors contributed to manuscript editing.

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Correspondence to Luke J. McKay or William P. Inskeep.

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Supplementary information

Supplementary Information

Supplementary Tables 1 and 2, Supplementary Table 5, Supplementary Table 7, Supplementary Figures 1–12, Supplementary Discussion, Supplementary Data Legends and Supplementary References.

Reporting Summary

Supplementary Table 3

Gene clusters, clusters of orthologous genes identification numbers and functions corresponding to each of the Korarchaeota displayed in Fig. 1.

Supplementary Table 4

List of archaeal clusters of orthologous genes used in phylogenomic analysis.

Supplementary Table 6

Protein BLAST comparisons of ancestral dissimilatory sulfur reductase sequences to Candidatus Methanodesulfokores washburnensis and the NCBI protein database.

Supplementary Table 8

List of abbreviations used in metabolic reconstruction (Fig. 4).

Dataset 1

Newick tree files corresponding to Fig. 2a.

Dataset 2

Newick tree files corresponding to Supplementary Figure 5a.

Dataset 3

Newick tree files corresponding to Supplementary Figure 5b.

Dataset 4

Newick tree files corresponding to Supplementary Figure 5c.

Dataset 5

Newick tree files corresponding to Supplementary Figure 5d.

Dataset 6

Newick tree files corresponding to Supplementary Figure 5e.

Dataset 7

Newick tree files corresponding to Supplementary Figure 5f.

Dataset 8

Newick tree files corresponding to Supplementary Figure 5g.

Dataset 9

Newick tree files corresponding to Supplementary Figure 5h.

Dataset 10

Newick tree files corresponding to Supplementary Figure 5i.

Dataset 11

Newick tree files corresponding to Supplementary Figure 5j.

Dataset 12

Newick tree files corresponding to Supplementary Figure 5k.

Dataset 13

Concatenated alignment file (.afa) of 56 conserved proteins from three domains. File size = 2 MB.

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McKay, L.J., Dlakić, M., Fields, M.W. et al. Co-occurring genomic capacity for anaerobic methane and dissimilatory sulfur metabolisms discovered in the Korarchaeota. Nat Microbiol 4, 614–622 (2019). https://doi.org/10.1038/s41564-019-0362-4

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