Comparative genomics reveals electron transfer and syntrophic mechanisms differentiating methanotrophic and methanogenic archaea

PLoS Biol. 2022 Jan 5;20(1):e3001508. doi: 10.1371/journal.pbio.3001508. eCollection 2022 Jan.

Abstract

The anaerobic oxidation of methane coupled to sulfate reduction is a microbially mediated process requiring a syntrophic partnership between anaerobic methanotrophic (ANME) archaea and sulfate-reducing bacteria (SRB). Based on genome taxonomy, ANME lineages are polyphyletic within the phylum Halobacterota, none of which have been isolated in pure culture. Here, we reconstruct 28 ANME genomes from environmental metagenomes and flow sorted syntrophic consortia. Together with a reanalysis of previously published datasets, these genomes enable a comparative analysis of all marine ANME clades. We review the genomic features that separate ANME from their methanogenic relatives and identify what differentiates ANME clades. Large multiheme cytochromes and bioenergetic complexes predicted to be involved in novel electron bifurcation reactions are well distributed and conserved in the ANME archaea, while significant variations in the anabolic C1 pathways exists between clades. Our analysis raises the possibility that methylotrophic methanogenesis may have evolved from a methanotrophic ancestor.

Publication types

  • Review
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Anaerobiosis
  • Archaea* / genetics
  • Archaea* / metabolism
  • Electrons*
  • Genomics
  • Geologic Sediments / microbiology
  • Methane / metabolism
  • Oxidation-Reduction
  • Phylogeny
  • Sulfates / metabolism

Substances

  • Sulfates
  • Methane

Grants and funding

The work conducted by the U.S. Department of Energy Joint Genome Institute [https://jgi.doe.gov/], a Department of Energy Office of Science User Facility, is supported under Contract No. DE-AC02-05CH11231. Funding for this study was received by the DFG Leibniz grant [https://www.dfg.de/en/funded_projects/prizewinners/leibniz_prize/index.html] and by the Max Planck Society [https://www.mpg.de/] to A.B. Genomes of BONCAT-FACS sorted ANME-consortia were generated via a Joint Genome Institute Director Discretionary Project Award to R.H. and V.J.O. [https://jgi.doe.gov/]. Work with the fosmid libraries was performed under the auspices of the Natural Sciences and Engineering Research Council of Canada, Genome British Columbia, the Canada Foundation for Innovation, Compute/Calcul Canada, and the U.S. Department of Energy Joint Genome Institute supported by the Office of Science of U.S. Department of Energy Contract DE-AC02-05CH11231 to S.H. The National Science Foundation provided support for the Lost City cruise and metagenome sequencing to W.B. (OCE- 1536702/1536405). [https://www.nsf.gov/]. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.