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Title: Members of the Genus Methylobacter Are Inferred To Account for the Majority of Aerobic Methane Oxidation in Oxic Soils from a Freshwater Wetland

Abstract

ABSTRACT Microbial carbon degradation and methanogenesis in wetland soils generate a large proportion of atmospheric methane, a highly potent greenhouse gas. Despite their potential to mitigate greenhouse gas emissions, knowledge about methane-consuming methanotrophs is often limited to lower-resolution single-gene surveys that fail to capture the taxonomic and metabolic diversity of these microorganisms in soils. Here our objective was to use genome-enabled approaches to investigate methanotroph membership, distribution, and in situ activity across spatial and seasonal gradients in a freshwater wetland near Lake Erie. 16S rRNA gene analyses demonstrated that members of the methanotrophic Methylococcales were dominant, with the dominance largely driven by the relative abundance of four taxa, and enriched in oxic surface soils. Three methanotroph genomes from assembled soil metagenomes were assigned to the genus Methylobacter and represented the most abundant methanotrophs across the wetland. Paired metatranscriptomes confirmed that these Old Woman Creek (OWC) Methylobacter members accounted for nearly all the aerobic methanotrophic activity across two seasons. In addition to having the capacity to couple methane oxidation to aerobic respiration, these new genomes encoded denitrification potential that may sustain energy generation in soils with lower dissolved oxygen concentrations. We further show that Methylobacter members that were closely related tomore » the OWC members were present in many other high-methane-emitting freshwater and soil sites, suggesting that this lineage could participate in methane consumption in analogous ecosystems. This work contributes to the growing body of research suggesting that Methylobacter may represent critical mediators of methane fluxes in freshwater saturated sediments and soils worldwide. IMPORTANCE Here we used soil metagenomics and metatranscriptomics to uncover novel members within the genus Methylobacter . We denote these closely related genomes as members of the lineage OWC Methylobacter . Despite the incredibly high microbial diversity in soils, here we present findings that unexpectedly showed that methane cycling was primarily mediated by a single genus for both methane production (“ Candidatus Methanothrix paradoxum”) and methane consumption (OWC Methylobacter ). Metatranscriptomic analyses revealed that decreased methanotrophic activity rather than increased methanogenic activity possibly contributed to the greater methane emissions that we had previously observed in summer months, findings important for biogeochemical methane models. Although members of this Methylococcales order have been cultivated for decades, multi-omic approaches continue to illuminate the methanotroph phylogenetic and metabolic diversity harbored in terrestrial and marine ecosystems.« less

Authors:
ORCiD logo; ; ; ; ; ; ; ; ; ; ; ;
Publication Date:
Research Org.:
The Ohio State Univ., Columbus, OH (United States); Univ. of California, Oakland, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1481031
Alternate Identifier(s):
OSTI ID: 1612814
Grant/Contract Number:  
SC0018022; AC02-05CH11231
Resource Type:
Published Article
Journal Name:
mBio (Online)
Additional Journal Information:
Journal Name: mBio (Online) Journal Volume: 9 Journal Issue: 6; Journal ID: ISSN 2150-7511
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Microbiology; denitrification; metagenomics; metatranscriptomics; methane; methanotrophs; soil microbiology

Citation Formats

Smith, Garrett J., Angle, Jordan C., Solden, Lindsey M., Borton, Mikayla A., Morin, Timothy H., Daly, Rebecca A., Johnston, Michael D., Stefanik, Kay C., Wolfe, Richard, Gil, Bohrer, Wrighton, Kelly C., Bailey, ed., Vanessa, and Jansson, ed., Janet K. Members of the Genus Methylobacter Are Inferred To Account for the Majority of Aerobic Methane Oxidation in Oxic Soils from a Freshwater Wetland. United States: N. p., 2018. Web. doi:10.1128/mBio.00815-18.
Smith, Garrett J., Angle, Jordan C., Solden, Lindsey M., Borton, Mikayla A., Morin, Timothy H., Daly, Rebecca A., Johnston, Michael D., Stefanik, Kay C., Wolfe, Richard, Gil, Bohrer, Wrighton, Kelly C., Bailey, ed., Vanessa, & Jansson, ed., Janet K. Members of the Genus Methylobacter Are Inferred To Account for the Majority of Aerobic Methane Oxidation in Oxic Soils from a Freshwater Wetland. United States. doi:10.1128/mBio.00815-18.
Smith, Garrett J., Angle, Jordan C., Solden, Lindsey M., Borton, Mikayla A., Morin, Timothy H., Daly, Rebecca A., Johnston, Michael D., Stefanik, Kay C., Wolfe, Richard, Gil, Bohrer, Wrighton, Kelly C., Bailey, ed., Vanessa, and Jansson, ed., Janet K. Tue . "Members of the Genus Methylobacter Are Inferred To Account for the Majority of Aerobic Methane Oxidation in Oxic Soils from a Freshwater Wetland". United States. doi:10.1128/mBio.00815-18.
@article{osti_1481031,
title = {Members of the Genus Methylobacter Are Inferred To Account for the Majority of Aerobic Methane Oxidation in Oxic Soils from a Freshwater Wetland},
author = {Smith, Garrett J. and Angle, Jordan C. and Solden, Lindsey M. and Borton, Mikayla A. and Morin, Timothy H. and Daly, Rebecca A. and Johnston, Michael D. and Stefanik, Kay C. and Wolfe, Richard and Gil, Bohrer and Wrighton, Kelly C. and Bailey, ed., Vanessa and Jansson, ed., Janet K.},
abstractNote = {ABSTRACT Microbial carbon degradation and methanogenesis in wetland soils generate a large proportion of atmospheric methane, a highly potent greenhouse gas. Despite their potential to mitigate greenhouse gas emissions, knowledge about methane-consuming methanotrophs is often limited to lower-resolution single-gene surveys that fail to capture the taxonomic and metabolic diversity of these microorganisms in soils. Here our objective was to use genome-enabled approaches to investigate methanotroph membership, distribution, and in situ activity across spatial and seasonal gradients in a freshwater wetland near Lake Erie. 16S rRNA gene analyses demonstrated that members of the methanotrophic Methylococcales were dominant, with the dominance largely driven by the relative abundance of four taxa, and enriched in oxic surface soils. Three methanotroph genomes from assembled soil metagenomes were assigned to the genus Methylobacter and represented the most abundant methanotrophs across the wetland. Paired metatranscriptomes confirmed that these Old Woman Creek (OWC) Methylobacter members accounted for nearly all the aerobic methanotrophic activity across two seasons. In addition to having the capacity to couple methane oxidation to aerobic respiration, these new genomes encoded denitrification potential that may sustain energy generation in soils with lower dissolved oxygen concentrations. We further show that Methylobacter members that were closely related to the OWC members were present in many other high-methane-emitting freshwater and soil sites, suggesting that this lineage could participate in methane consumption in analogous ecosystems. This work contributes to the growing body of research suggesting that Methylobacter may represent critical mediators of methane fluxes in freshwater saturated sediments and soils worldwide. IMPORTANCE Here we used soil metagenomics and metatranscriptomics to uncover novel members within the genus Methylobacter . We denote these closely related genomes as members of the lineage OWC Methylobacter . Despite the incredibly high microbial diversity in soils, here we present findings that unexpectedly showed that methane cycling was primarily mediated by a single genus for both methane production (“ Candidatus Methanothrix paradoxum”) and methane consumption (OWC Methylobacter ). Metatranscriptomic analyses revealed that decreased methanotrophic activity rather than increased methanogenic activity possibly contributed to the greater methane emissions that we had previously observed in summer months, findings important for biogeochemical methane models. Although members of this Methylococcales order have been cultivated for decades, multi-omic approaches continue to illuminate the methanotroph phylogenetic and metabolic diversity harbored in terrestrial and marine ecosystems.},
doi = {10.1128/mBio.00815-18},
journal = {mBio (Online)},
number = 6,
volume = 9,
place = {United States},
year = {2018},
month = {11}
}

Journal Article:
Free Publicly Available Full Text
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DOI: 10.1128/mBio.00815-18

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Cited by: 7 works
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