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

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 a...

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Autores: Murali, Ranjani, Yu, Hang, Speth, Daan R., Wu, Fabai, Metcalfe, Kyle S., Crémière, Antoine, Laso-Pérez, Rafael, Malmstrom, Rex R., Goudeau, Danielle, Woyke, Tanja, Hatzenpichler, Roland, Chadwick, Grayson L., Connon, Stephanie A., Orphan, Victoria J.
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2023
País:España
Institución:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/351296
Acceso en línea:http://hdl.handle.net/10261/351296
https://api.elsevier.com/content/abstract/scopus_id/85173487312
Access Level:acceso abierto
Palabra clave:sulfate-reducing bacteria
Electron transfer
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spelling Physiological potential and evolutionary trajectories of syntrophic sulfate-reducing bacterial partners of anaerobic methanotrophic archaeaMurali, RanjaniYu, HangSpeth, Daan R.Wu, FabaiMetcalfe, Kyle S.Crémière, AntoineLaso-Pérez, RafaelMalmstrom, Rex R.Goudeau, DanielleWoyke, TanjaHatzenpichler, RolandChadwick, Grayson L.Connon, Stephanie A.Orphan, Victoria J.sulfate-reducing bacteriaElectron transferSulfate-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.Peer reviewedLaso-Pérez, Rafael [0000-0002-6912-7865]Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]202420242023info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionhttp://hdl.handle.net/10261/351296https://api.elsevier.com/content/abstract/scopus_id/85173487312reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)InglésPLoS BiologySíinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/3512962026-05-22T06:33:51Z
dc.title.none.fl_str_mv Physiological potential and evolutionary trajectories of syntrophic sulfate-reducing bacterial partners of anaerobic methanotrophic archaea
title Physiological potential and evolutionary trajectories of syntrophic sulfate-reducing bacterial partners of anaerobic methanotrophic archaea
spellingShingle Physiological potential and evolutionary trajectories of syntrophic sulfate-reducing bacterial partners of anaerobic methanotrophic archaea
Murali, Ranjani
sulfate-reducing bacteria
Electron transfer
title_short Physiological potential and evolutionary trajectories of syntrophic sulfate-reducing bacterial partners of anaerobic methanotrophic archaea
title_full Physiological potential and evolutionary trajectories of syntrophic sulfate-reducing bacterial partners of anaerobic methanotrophic archaea
title_fullStr Physiological potential and evolutionary trajectories of syntrophic sulfate-reducing bacterial partners of anaerobic methanotrophic archaea
title_full_unstemmed Physiological potential and evolutionary trajectories of syntrophic sulfate-reducing bacterial partners of anaerobic methanotrophic archaea
title_sort Physiological potential and evolutionary trajectories of syntrophic sulfate-reducing bacterial partners of anaerobic methanotrophic archaea
dc.creator.none.fl_str_mv Murali, Ranjani
Yu, Hang
Speth, Daan R.
Wu, Fabai
Metcalfe, Kyle S.
Crémière, Antoine
Laso-Pérez, Rafael
Malmstrom, Rex R.
Goudeau, Danielle
Woyke, Tanja
Hatzenpichler, Roland
Chadwick, Grayson L.
Connon, Stephanie A.
Orphan, Victoria J.
author Murali, Ranjani
author_facet Murali, Ranjani
Yu, Hang
Speth, Daan R.
Wu, Fabai
Metcalfe, Kyle S.
Crémière, Antoine
Laso-Pérez, Rafael
Malmstrom, Rex R.
Goudeau, Danielle
Woyke, Tanja
Hatzenpichler, Roland
Chadwick, Grayson L.
Connon, Stephanie A.
Orphan, Victoria J.
author_role author
author2 Yu, Hang
Speth, Daan R.
Wu, Fabai
Metcalfe, Kyle S.
Crémière, Antoine
Laso-Pérez, Rafael
Malmstrom, Rex R.
Goudeau, Danielle
Woyke, Tanja
Hatzenpichler, Roland
Chadwick, Grayson L.
Connon, Stephanie A.
Orphan, Victoria J.
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Laso-Pérez, Rafael [0000-0002-6912-7865]
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv sulfate-reducing bacteria
Electron transfer
topic sulfate-reducing bacteria
Electron transfer
description 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.
publishDate 2023
dc.date.none.fl_str_mv 2023
2024
2024
dc.type.none.fl_str_mv info:eu-repo/semantics/article
http://purl.org/coar/resource_type/c_6501
Publisher's version
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/351296
https://api.elsevier.com/content/abstract/scopus_id/85173487312
url http://hdl.handle.net/10261/351296
https://api.elsevier.com/content/abstract/scopus_id/85173487312
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv PLoS Biology
Sí
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.source.none.fl_str_mv reponame:DIGITAL.CSIC. Repositorio Institucional del CSIC
instname:Consejo Superior de Investigaciones Científicas (CSIC)
instname_str Consejo Superior de Investigaciones Científicas (CSIC)
reponame_str DIGITAL.CSIC. Repositorio Institucional del CSIC
collection DIGITAL.CSIC. Repositorio Institucional del CSIC
repository.name.fl_str_mv
repository.mail.fl_str_mv
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score 15,811543

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