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Physiological adaptation of sulfate reducing bacteria in syntrophic partnership with anaerobic methanotrophic archaea

Murali, Ranjani and Yu, Hang and Speth, Daan R. and Wu, Fabai and Metcalfe, Kyle S. and Crémière, Antoine and Laso-Pérez, Rafael and Malmstrom, Rex R. and Goudeau, Danielle and Woyke, Tanja and Hatzenpichler, Roland and Chadwick, Grayson L. and Orphan, Victoria J. (2022) Physiological adaptation of sulfate reducing bacteria in syntrophic partnership with anaerobic methanotrophic archaea. . (Unpublished)

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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 explore the metabolic adaptation of four syntrophic SRB clades (HotSeep-1, Seep-SRB2, Seep-SRB1a and Seep-SRB1g) from a phylogenomics perspective, tracing the evolution of conserved proteins in the syntrophic SRB clades, and comparing the genomes of syntrophic SRB to their nearest evolutionary neighbors in the phylum Desulfobacterota. We note several examples of gain, loss or biochemical adaptation of proteins within pathways involved in extracellular electron transfer, electron transport chain, nutrient sharing, biofilm formation and cell adhesion. We demonstrate that the metabolic adaptations in each of these syntrophic clades are unique, suggesting that they have independently evolved, converging to a syntrophic partnership with ANME. Within the clades we also investigated the specialization of different syntrophic SRB species to partnerships with different ANME clades, using metagenomic sequences obtained from ANME and SRB partners in individual consortia after fluorescent-sorting of cell aggregates from anaerobic sediments. In one instance of metabolic adaptation to different partnerships, we show that Seep-SRB1a partners of ANME-2c appear to lack nutritional auxotrophies, while the related Seep-SRB1a partners of a different methanotrophic archaeal lineage, ANME-2a, are missing the cobalamin synthesis pathway, suggesting that the Seep-SRB1a partners of ANME-2a may have a nutritional dependence on its partner. Together, our paired genomic analysis of AOM consortia highlights the specific adaptation and diversification of syntrophic SRB clades linked to their associated ANME lineages.

Item Type:Report or Paper (Discussion Paper)
Related URLs:
URLURL TypeDescription Paper
Murali, Ranjani0000-0003-4073-9910
Yu, Hang0000-0002-7600-1582
Speth, Daan R.0000-0002-2361-5935
Wu, Fabai0000-0001-5812-5621
Metcalfe, Kyle S.0000-0002-2963-765X
Crémière, Antoine0000-0001-7382-2097
Laso-Pérez, Rafael0000-0002-6912-7865
Malmstrom, Rex R.0000-0002-4758-7369
Goudeau, Danielle0000-0002-3785-032X
Woyke, Tanja0000-0002-9485-5637
Hatzenpichler, Roland0000-0002-5489-3444
Chadwick, Grayson L.0000-0003-0700-9350
Orphan, Victoria J.0000-0002-5374-6178
Additional Information:The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license. We thank the DOE and the Moore Foundation for funding this research (Principle Investigator: Dr. Victoria J. Orphan). We acknowledge the Dalio Foundation and Woods Hole Oceanographic Institute for supporting the NA091 research cruise to South Pescadero Basin on E/V Nautilus operated by the Ocean Exploration Trust in October-November 2017. The work (Award doi: 10.46936/fics.proj.2017.49956/60006219) conducted by the U.S. Department of Energy Joint Genome Institute (, a DOE Office of Science User Facility, is supported by the Office of Science of the U.S. Department of Energy operated under Contract No. DE-AC02-05CH11231. We would also like to thank Magdalena Mayr for her thoughtful comments on this manuscript and Fernanda Jimenez-Otero for sharing her thoughts and expertise in the field of extracellular electron transfer. We are also grateful to Alon Philosof, Aditi Narayan, Kriti Sharma and James Hemp for many productive discussions on broad scientific questions in microbial ecology and evolution, metabolism and scientific writing that lent itself to the framing of this manuscript. The authors have declared no competing interest.
Funding AgencyGrant Number
Department of Energy (DOE)DE-AC02-05CH11231
Gordon and Betty Moore FoundationUNSPECIFIED
Dalio FoundationUNSPECIFIED
Woods Hole Oceanographic InstitutionUNSPECIFIED
Record Number:CaltechAUTHORS:20230316-182819000.64
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Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:120173
Deposited By: George Porter
Deposited On:17 Mar 2023 22:53
Last Modified:17 Mar 2023 22:53

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