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

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 Halobac...

Full description

Bibliographic Details
Main Authors: Grayson L Chadwick, Connor T Skennerton, Rafael Laso-Pérez, Andy O Leu, Daan R Speth, Hang Yu, Connor Morgan-Lang, Roland Hatzenpichler, Danielle Goudeau, Rex Malmstrom, William J Brazelton, Tanja Woyke, Steven J Hallam, Gene W Tyson, Gunter Wegener, Antje Boetius, Victoria J Orphan
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2022-01-01
Series:PLoS Biology
Online Access:https://doi.org/10.1371/journal.pbio.3001508
_version_ 1811292769577074688
author Grayson L Chadwick
Connor T Skennerton
Rafael Laso-Pérez
Andy O Leu
Daan R Speth
Hang Yu
Connor Morgan-Lang
Roland Hatzenpichler
Danielle Goudeau
Rex Malmstrom
William J Brazelton
Tanja Woyke
Steven J Hallam
Gene W Tyson
Gunter Wegener
Antje Boetius
Victoria J Orphan
author_facet Grayson L Chadwick
Connor T Skennerton
Rafael Laso-Pérez
Andy O Leu
Daan R Speth
Hang Yu
Connor Morgan-Lang
Roland Hatzenpichler
Danielle Goudeau
Rex Malmstrom
William J Brazelton
Tanja Woyke
Steven J Hallam
Gene W Tyson
Gunter Wegener
Antje Boetius
Victoria J Orphan
author_sort Grayson L Chadwick
collection DOAJ
description 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.
first_indexed 2024-04-13T04:51:24Z
format Article
id doaj.art-26c3bee9c55c4549a91b05700e3a3b8d
institution Directory Open Access Journal
issn 1544-9173
1545-7885
language English
last_indexed 2024-04-13T04:51:24Z
publishDate 2022-01-01
publisher Public Library of Science (PLoS)
record_format Article
series PLoS Biology
spelling doaj.art-26c3bee9c55c4549a91b05700e3a3b8d2022-12-22T03:01:40ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852022-01-01201e300150810.1371/journal.pbio.3001508Comparative genomics reveals electron transfer and syntrophic mechanisms differentiating methanotrophic and methanogenic archaea.Grayson L ChadwickConnor T SkennertonRafael Laso-PérezAndy O LeuDaan R SpethHang YuConnor Morgan-LangRoland HatzenpichlerDanielle GoudeauRex MalmstromWilliam J BrazeltonTanja WoykeSteven J HallamGene W TysonGunter WegenerAntje BoetiusVictoria J OrphanThe 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.https://doi.org/10.1371/journal.pbio.3001508
spellingShingle Grayson L Chadwick
Connor T Skennerton
Rafael Laso-Pérez
Andy O Leu
Daan R Speth
Hang Yu
Connor Morgan-Lang
Roland Hatzenpichler
Danielle Goudeau
Rex Malmstrom
William J Brazelton
Tanja Woyke
Steven J Hallam
Gene W Tyson
Gunter Wegener
Antje Boetius
Victoria J Orphan
Comparative genomics reveals electron transfer and syntrophic mechanisms differentiating methanotrophic and methanogenic archaea.
PLoS Biology
title Comparative genomics reveals electron transfer and syntrophic mechanisms differentiating methanotrophic and methanogenic archaea.
title_full Comparative genomics reveals electron transfer and syntrophic mechanisms differentiating methanotrophic and methanogenic archaea.
title_fullStr Comparative genomics reveals electron transfer and syntrophic mechanisms differentiating methanotrophic and methanogenic archaea.
title_full_unstemmed Comparative genomics reveals electron transfer and syntrophic mechanisms differentiating methanotrophic and methanogenic archaea.
title_short Comparative genomics reveals electron transfer and syntrophic mechanisms differentiating methanotrophic and methanogenic archaea.
title_sort comparative genomics reveals electron transfer and syntrophic mechanisms differentiating methanotrophic and methanogenic archaea
url https://doi.org/10.1371/journal.pbio.3001508
work_keys_str_mv AT graysonlchadwick comparativegenomicsrevealselectrontransferandsyntrophicmechanismsdifferentiatingmethanotrophicandmethanogenicarchaea
AT connortskennerton comparativegenomicsrevealselectrontransferandsyntrophicmechanismsdifferentiatingmethanotrophicandmethanogenicarchaea
AT rafaellasoperez comparativegenomicsrevealselectrontransferandsyntrophicmechanismsdifferentiatingmethanotrophicandmethanogenicarchaea
AT andyoleu comparativegenomicsrevealselectrontransferandsyntrophicmechanismsdifferentiatingmethanotrophicandmethanogenicarchaea
AT daanrspeth comparativegenomicsrevealselectrontransferandsyntrophicmechanismsdifferentiatingmethanotrophicandmethanogenicarchaea
AT hangyu comparativegenomicsrevealselectrontransferandsyntrophicmechanismsdifferentiatingmethanotrophicandmethanogenicarchaea
AT connormorganlang comparativegenomicsrevealselectrontransferandsyntrophicmechanismsdifferentiatingmethanotrophicandmethanogenicarchaea
AT rolandhatzenpichler comparativegenomicsrevealselectrontransferandsyntrophicmechanismsdifferentiatingmethanotrophicandmethanogenicarchaea
AT daniellegoudeau comparativegenomicsrevealselectrontransferandsyntrophicmechanismsdifferentiatingmethanotrophicandmethanogenicarchaea
AT rexmalmstrom comparativegenomicsrevealselectrontransferandsyntrophicmechanismsdifferentiatingmethanotrophicandmethanogenicarchaea
AT williamjbrazelton comparativegenomicsrevealselectrontransferandsyntrophicmechanismsdifferentiatingmethanotrophicandmethanogenicarchaea
AT tanjawoyke comparativegenomicsrevealselectrontransferandsyntrophicmechanismsdifferentiatingmethanotrophicandmethanogenicarchaea
AT stevenjhallam comparativegenomicsrevealselectrontransferandsyntrophicmechanismsdifferentiatingmethanotrophicandmethanogenicarchaea
AT genewtyson comparativegenomicsrevealselectrontransferandsyntrophicmechanismsdifferentiatingmethanotrophicandmethanogenicarchaea
AT gunterwegener comparativegenomicsrevealselectrontransferandsyntrophicmechanismsdifferentiatingmethanotrophicandmethanogenicarchaea
AT antjeboetius comparativegenomicsrevealselectrontransferandsyntrophicmechanismsdifferentiatingmethanotrophicandmethanogenicarchaea
AT victoriajorphan comparativegenomicsrevealselectrontransferandsyntrophicmechanismsdifferentiatingmethanotrophicandmethanogenicarchaea