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Cited by 62Methane Hydrates and Related PhenomenaMicrobial Fuel Cells and BioremediationMicrobial Community Ecology and Physiology

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Physiological potential and evolutionary trajectories of syntrophic sulfate-reducing bacterial partners of anaerobic methanotrophic archaea

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Murali, Ranjani, Yu, Hang, Speth, Daan R., Wu, Fabai, Metcalfe, Kyle S., Crémière, Antoine, Laso-Pèrez, Rafael, Malmstrom, Rex R., Goudeau, Danielle, Woyke, Tanja, Hatzenpichler, Roland, Chadwick, Grayson L., Connon, Stephanie A., Orphan, Victoria J.·2023·PLOS Biology
DOI 10.1371/journal.pbio.3002292PMC PMC10553843

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Abstract

Sulfate-coupled anaerobic oxidation of methane (AOM) is performed by multicellular consortia of anaerobic methanotrophic archaea (ANME) in obligate syntrophic partnership with sulfate-reducing bacteria (SRB). Diverse ANME and SRB clades co-associate but the physiological basis for their adaptation and diversification is not well understood. In this work, we used comparative metagenomics and phylogenetics to investigate the metabolic adaptation among the 4 main syntrophic SRB clades (HotSeep-1, Seep-SRB2, Seep-SRB1a, and Seep-SRB1g) and identified features associated with their syntrophic lifestyle that distinguish them from their non-syntrophic evolutionary neighbors in the phylum Desulfobacterota. We show that the protein complexes involved in direct interspecies electron transfer (DIET) from ANME to the SRB outer membrane are conserved between the syntrophic lineages. In contrast, the proteins involved in electron transfer within the SRB inner membrane differ between clades, indicative of convergent evolution in the adaptation to a syntrophic lifestyle. Our analysis suggests that in most cases, this adaptation likely occurred after the acquisition of the DIET complexes in an ancestral clade and involve horizontal gene transfers within pathways for electron transfer (CbcBA) and biofilm formation (Pel). We also provide evidence for unique adaptations within syntrophic SRB clades, which vary depending on the archaeal partner. Among the most widespread syntrophic SRB, Seep-SRB1a, subclades that specifically partner ANME-2a are missing the cobalamin synthesis pathway, suggestive of nutritional dependency on its partner, while closely related Seep-SRB1a partners of ANME-2c lack nutritional auxotrophies. Our work provides insight into the features associated with DIET-based syntrophy and the adaptation of SRB towards it.

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Metadata

Authors
Murali, R., Yu, H., Speth, D. R., Wu, F., Metcalfe, K. S., Crémière, A., Laso-Pèrez, R., Malmstrom, R. R., Goudeau, D., Woyke, T., Hatzenpichler, R., Chadwick, G. L., Connon, S. A., & Orphan, V. J.
Affiliations
  • California Institute of Technology (US)
  • University of Southern California (US)
  • Zhejiang University (CN)
  • University of California, Berkeley (US)
  • Joint Genome Institute (US)
  • Montana State University (US)
Corresponding author
  • Murali, Ranjani
  • Orphan, Victoria J.
ORCID
Venue
PLOS Biology
Publisher
Public Library of Science (PLoS)
Published
2023-09-25
Volume
21
Issue
9
Pages
e3002292
ISSN
  • 1544-9173 (ISSN-L)
  • 1545-7885
DOI
10.1371/journal.pbio.3002292
PMC
PMC10553843
OpenAlex
W4387011787
Cited by
62
References
2
Citations by year
2026: 22 · 2025: 23 · 2024: 13 · 2023: 4
FWCI
5.32
Type
journal article
Language
en
Update notices
new_version (2023-10-05)
Open access
Licence
Locations
  • PLoS Biology (publishedVersion, public-domain)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • eScholarship (California Digital Library) (submittedVersion, public-domain)
  • DIGITAL.CSIC (Spanish National Research Council (CSIC)) (submittedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • OSTI OAI (U.S. Department of Energy Office of Scientific and Technical Information) (submittedVersion)
Funders
  • Gordon and Betty Moore Foundation (GBMF Grant #9324)
  • Biological and Environmental Research (DE-SC0022991, 10.46936/fics.proj.2017.49956/60006219)
  • Office of Science of the U.S. Department of Energy (Contract No. DE-AC02-05CH11231)
  • National Science Foundation (OCE-1634002)
  • Science and Technology Center for Dark Energy Biosphere Investigations (C-DEBI, OCE-0939564)
  • Ministerio de Ciencia e Innovación (FJC2019-041362-I, RyC2021-031775-I)
  • European Union («NextGenerationEU»/PRTR)
Topics
  • Physical Sciences › Environmental Science › Environmental Chemistry › Methane Hydrates and Related Phenomena
  • Physical Sciences › Environmental Science › Environmental Engineering › Microbial Fuel Cells and Bioremediation
  • Physical Sciences › Environmental Science › Ecology › Microbial Community Ecology and Physiology
Keywords
anaerobic oxidation of methane, anaerobic methanotrophic archaea, sulfate-reducing bacteria, syntrophy, interspecies electron transfer, direct interspecies electron transfer, Desulfobacterota, cobalamin synthesis, horizontal gene transfer, convergent evolution, microbial consortia
MeSH terms
Anaerobiosis, Archaea, Bacteria, Oxidation-Reduction, Phylogeny, Sulfates, Geologic Sediments

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