Lateral Gene Transfer Drives Metabolic Flexibility in the Anaerobic Methane-Oxidizing Archaeal Family <italic toggle="yes">Methanoperedenaceae</italic>

ABSTRACT Anaerobic oxidation of methane (AOM) is an important biological process responsible for controlling the flux of methane into the atmosphere. Members of the archaeal family Methanoperedenaceae (formerly ANME-2d) have been demonstrated to couple AOM to the reduction of nitrate, iron, and mang...

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Autores principales:	Andy O. Leu, Simon J. McIlroy, Jun Ye, Donovan H. Parks, Victoria J. Orphan, Gene W. Tyson
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	ANME AOM comparative genomics methane Methanoperedenaceae Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/26da6f3997eb47a88cc7c200bb1d380d
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spelling	oai:doaj.org-article:26da6f3997eb47a88cc7c200bb1d380d2021-11-15T15:56:46ZLateral Gene Transfer Drives Metabolic Flexibility in the Anaerobic Methane-Oxidizing Archaeal Family <italic toggle="yes">Methanoperedenaceae</italic>10.1128/mBio.01325-202150-7511https://doaj.org/article/26da6f3997eb47a88cc7c200bb1d380d2020-06-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01325-20https://doaj.org/toc/2150-7511ABSTRACT Anaerobic oxidation of methane (AOM) is an important biological process responsible for controlling the flux of methane into the atmosphere. Members of the archaeal family Methanoperedenaceae (formerly ANME-2d) have been demonstrated to couple AOM to the reduction of nitrate, iron, and manganese. Here, comparative genomic analysis of 16 Methanoperedenaceae metagenome-assembled genomes (MAGs), recovered from diverse environments, revealed novel respiratory strategies acquired through lateral gene transfer (LGT) events from diverse archaea and bacteria. Comprehensive phylogenetic analyses suggests that LGT has allowed members of the Methanoperedenaceae to acquire genes for the oxidation of hydrogen and formate and the reduction of arsenate, selenate, and elemental sulfur. Numerous membrane-bound multiheme c-type cytochrome complexes also appear to have been laterally acquired, which may be involved in the direct transfer of electrons to metal oxides, humic substances, and syntrophic partners. IMPORTANCE AOM by microorganisms limits the atmospheric release of the potent greenhouse gas methane and has consequent importance for the global carbon cycle and climate change modeling. While the oxidation of methane coupled to sulfate by consortia of anaerobic methanotrophic (ANME) archaea and bacteria is well documented, several other potential electron acceptors have also been reported to support AOM. In this study, we identify a number of novel respiratory strategies that appear to have been laterally acquired by members of the Methanoperedenaceae, as they are absent from related archaea and other ANME lineages. Expanding the known metabolic potential for members of the Methanoperedenaceae provides important insight into their ecology and suggests their role in linking methane oxidation to several global biogeochemical cycles.Andy O. LeuSimon J. McIlroyJun YeDonovan H. ParksVictoria J. OrphanGene W. TysonAmerican Society for MicrobiologyarticleANMEAOMcomparative genomicsmethaneMethanoperedenaceaeMicrobiologyQR1-502ENmBio, Vol 11, Iss 3 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	ANME AOM comparative genomics methane Methanoperedenaceae Microbiology QR1-502
spellingShingle	ANME AOM comparative genomics methane Methanoperedenaceae Microbiology QR1-502 Andy O. Leu Simon J. McIlroy Jun Ye Donovan H. Parks Victoria J. Orphan Gene W. Tyson Lateral Gene Transfer Drives Metabolic Flexibility in the Anaerobic Methane-Oxidizing Archaeal Family <italic toggle="yes">Methanoperedenaceae</italic>
description	ABSTRACT Anaerobic oxidation of methane (AOM) is an important biological process responsible for controlling the flux of methane into the atmosphere. Members of the archaeal family Methanoperedenaceae (formerly ANME-2d) have been demonstrated to couple AOM to the reduction of nitrate, iron, and manganese. Here, comparative genomic analysis of 16 Methanoperedenaceae metagenome-assembled genomes (MAGs), recovered from diverse environments, revealed novel respiratory strategies acquired through lateral gene transfer (LGT) events from diverse archaea and bacteria. Comprehensive phylogenetic analyses suggests that LGT has allowed members of the Methanoperedenaceae to acquire genes for the oxidation of hydrogen and formate and the reduction of arsenate, selenate, and elemental sulfur. Numerous membrane-bound multiheme c-type cytochrome complexes also appear to have been laterally acquired, which may be involved in the direct transfer of electrons to metal oxides, humic substances, and syntrophic partners. IMPORTANCE AOM by microorganisms limits the atmospheric release of the potent greenhouse gas methane and has consequent importance for the global carbon cycle and climate change modeling. While the oxidation of methane coupled to sulfate by consortia of anaerobic methanotrophic (ANME) archaea and bacteria is well documented, several other potential electron acceptors have also been reported to support AOM. In this study, we identify a number of novel respiratory strategies that appear to have been laterally acquired by members of the Methanoperedenaceae, as they are absent from related archaea and other ANME lineages. Expanding the known metabolic potential for members of the Methanoperedenaceae provides important insight into their ecology and suggests their role in linking methane oxidation to several global biogeochemical cycles.
format	article
author	Andy O. Leu Simon J. McIlroy Jun Ye Donovan H. Parks Victoria J. Orphan Gene W. Tyson
author_facet	Andy O. Leu Simon J. McIlroy Jun Ye Donovan H. Parks Victoria J. Orphan Gene W. Tyson
author_sort	Andy O. Leu
title	Lateral Gene Transfer Drives Metabolic Flexibility in the Anaerobic Methane-Oxidizing Archaeal Family <italic toggle="yes">Methanoperedenaceae</italic>
title_short	Lateral Gene Transfer Drives Metabolic Flexibility in the Anaerobic Methane-Oxidizing Archaeal Family <italic toggle="yes">Methanoperedenaceae</italic>
title_full	Lateral Gene Transfer Drives Metabolic Flexibility in the Anaerobic Methane-Oxidizing Archaeal Family <italic toggle="yes">Methanoperedenaceae</italic>
title_fullStr	Lateral Gene Transfer Drives Metabolic Flexibility in the Anaerobic Methane-Oxidizing Archaeal Family <italic toggle="yes">Methanoperedenaceae</italic>
title_full_unstemmed	Lateral Gene Transfer Drives Metabolic Flexibility in the Anaerobic Methane-Oxidizing Archaeal Family <italic toggle="yes">Methanoperedenaceae</italic>
title_sort	lateral gene transfer drives metabolic flexibility in the anaerobic methane-oxidizing archaeal family <italic toggle="yes">methanoperedenaceae</italic>
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/26da6f3997eb47a88cc7c200bb1d380d
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Lateral Gene Transfer Drives Metabolic Flexibility in the Anaerobic Methane-Oxidizing Archaeal Family <italic toggle="yes">Methanoperedenaceae</italic>

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