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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 principales: 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.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10553843/
https://www.ncbi.nlm.nih.gov/pubmed/37747940
http://dx.doi.org/10.1371/journal.pbio.3002292
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author 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.
author_facet 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.
author_sort Murali, Ranjani
collection PubMed
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.
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spelling pubmed-105538432023-10-06 Physiological potential and evolutionary trajectories of syntrophic sulfate-reducing bacterial partners of anaerobic methanotrophic archaea 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. PLoS Biol Research Article 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. Public Library of Science 2023-09-25 /pmc/articles/PMC10553843/ /pubmed/37747940 http://dx.doi.org/10.1371/journal.pbio.3002292 Text en https://creativecommons.org/publicdomain/zero/1.0/This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 (https://creativecommons.org/publicdomain/zero/1.0/) public domain dedication.
spellingShingle Research Article
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.
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
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_short 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
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10553843/
https://www.ncbi.nlm.nih.gov/pubmed/37747940
http://dx.doi.org/10.1371/journal.pbio.3002292
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