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Title: Lateral Gene Transfer Drives Metabolic Flexibility in the Anaerobic Methane-Oxidizing Archaeal Family Methanoperedenaceae

Abstract

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 identifymore » 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.« less

Authors:
; ORCiD logo; ; ; ; ;
Publication Date:
Sponsoring Org.:
USDOE
OSTI Identifier:
1635309
Grant/Contract Number:  
SC0016469
Resource Type:
Published Article
Journal Name:
mBio (Online)
Additional Journal Information:
Journal Name: mBio (Online) Journal Volume: 11 Journal Issue: 3; Journal ID: ISSN 2150-7511
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English

Citation Formats

Leu, Andy O., McIlroy, Simon J., Ye, Jun, Parks, Donovan H., Orphan, Victoria J., Tyson, Gene W., and Bailey, ed., Mark J. Lateral Gene Transfer Drives Metabolic Flexibility in the Anaerobic Methane-Oxidizing Archaeal Family Methanoperedenaceae. United States: N. p., 2020. Web. doi:10.1128/mBio.01325-20.
Leu, Andy O., McIlroy, Simon J., Ye, Jun, Parks, Donovan H., Orphan, Victoria J., Tyson, Gene W., & Bailey, ed., Mark J. Lateral Gene Transfer Drives Metabolic Flexibility in the Anaerobic Methane-Oxidizing Archaeal Family Methanoperedenaceae. United States. doi:https://doi.org/10.1128/mBio.01325-20
Leu, Andy O., McIlroy, Simon J., Ye, Jun, Parks, Donovan H., Orphan, Victoria J., Tyson, Gene W., and Bailey, ed., Mark J. Tue . "Lateral Gene Transfer Drives Metabolic Flexibility in the Anaerobic Methane-Oxidizing Archaeal Family Methanoperedenaceae". United States. doi:https://doi.org/10.1128/mBio.01325-20.
@article{osti_1635309,
title = {Lateral Gene Transfer Drives Metabolic Flexibility in the Anaerobic Methane-Oxidizing Archaeal Family Methanoperedenaceae},
author = {Leu, Andy O. and McIlroy, Simon J. and Ye, Jun and Parks, Donovan H. and Orphan, Victoria J. and Tyson, Gene W. and Bailey, ed., Mark J.},
abstractNote = {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.},
doi = {10.1128/mBio.01325-20},
journal = {mBio (Online)},
number = 3,
volume = 11,
place = {United States},
year = {2020},
month = {6}
}

Journal Article:
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DOI: https://doi.org/10.1128/mBio.01325-20

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