Members of the Genus <italic toggle="yes">Methylobacter</italic> Are Inferred To Account for the Majority of Aerobic Methane Oxidation in Oxic Soils from a Freshwater Wetland

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-resolu...

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Autores principales:	Garrett J. Smith, Jordan C. Angle, Lindsey M. Solden, Mikayla A. Borton, Timothy H. Morin, Rebecca A. Daly, Michael D. Johnston, Kay C. Stefanik, Richard Wolfe, Bohrer Gil, Kelly C. Wrighton
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	denitrification metagenomics metatranscriptomics methane methanotrophs soil microbiology Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/08bd1d599f2d4036b81816c34bf17b4e
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spelling	oai:doaj.org-article:08bd1d599f2d4036b81816c34bf17b4e2021-11-15T15:52:19ZMembers of the Genus <italic toggle="yes">Methylobacter</italic> Are Inferred To Account for the Majority of Aerobic Methane Oxidation in Oxic Soils from a Freshwater Wetland10.1128/mBio.00815-182150-7511https://doaj.org/article/08bd1d599f2d4036b81816c34bf17b4e2018-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00815-18https://doaj.org/toc/2150-7511ABSTRACT 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.Garrett J. SmithJordan C. AngleLindsey M. SoldenMikayla A. BortonTimothy H. MorinRebecca A. DalyMichael D. JohnstonKay C. StefanikRichard WolfeBohrer GilKelly C. WrightonAmerican Society for Microbiologyarticledenitrificationmetagenomicsmetatranscriptomicsmethanemethanotrophssoil microbiologyMicrobiologyQR1-502ENmBio, Vol 9, Iss 6 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	denitrification metagenomics metatranscriptomics methane methanotrophs soil microbiology Microbiology QR1-502
spellingShingle	denitrification metagenomics metatranscriptomics methane methanotrophs soil microbiology Microbiology QR1-502 Garrett J. Smith Jordan C. Angle Lindsey M. Solden Mikayla A. Borton Timothy H. Morin Rebecca A. Daly Michael D. Johnston Kay C. Stefanik Richard Wolfe Bohrer Gil Kelly C. Wrighton Members of the Genus <italic toggle="yes">Methylobacter</italic> Are Inferred To Account for the Majority of Aerobic Methane Oxidation in Oxic Soils from a Freshwater Wetland
description	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.
format	article
author	Garrett J. Smith Jordan C. Angle Lindsey M. Solden Mikayla A. Borton Timothy H. Morin Rebecca A. Daly Michael D. Johnston Kay C. Stefanik Richard Wolfe Bohrer Gil Kelly C. Wrighton
author_facet	Garrett J. Smith Jordan C. Angle Lindsey M. Solden Mikayla A. Borton Timothy H. Morin Rebecca A. Daly Michael D. Johnston Kay C. Stefanik Richard Wolfe Bohrer Gil Kelly C. Wrighton
author_sort	Garrett J. Smith
title	Members of the Genus <italic toggle="yes">Methylobacter</italic> Are Inferred To Account for the Majority of Aerobic Methane Oxidation in Oxic Soils from a Freshwater Wetland
title_short	Members of the Genus <italic toggle="yes">Methylobacter</italic> Are Inferred To Account for the Majority of Aerobic Methane Oxidation in Oxic Soils from a Freshwater Wetland
title_full	Members of the Genus <italic toggle="yes">Methylobacter</italic> Are Inferred To Account for the Majority of Aerobic Methane Oxidation in Oxic Soils from a Freshwater Wetland
title_fullStr	Members of the Genus <italic toggle="yes">Methylobacter</italic> Are Inferred To Account for the Majority of Aerobic Methane Oxidation in Oxic Soils from a Freshwater Wetland
title_full_unstemmed	Members of the Genus <italic toggle="yes">Methylobacter</italic> Are Inferred To Account for the Majority of Aerobic Methane Oxidation in Oxic Soils from a Freshwater Wetland
title_sort	members of the genus <italic toggle="yes">methylobacter</italic> are inferred to account for the majority of aerobic methane oxidation in oxic soils from a freshwater wetland
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/08bd1d599f2d4036b81816c34bf17b4e
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Members of the Genus <italic toggle="yes">Methylobacter</italic> Are Inferred To Account for the Majority of Aerobic Methane Oxidation in Oxic Soils from a Freshwater Wetland

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