Contrasting Pathways for Anaerobic Methane Oxidation in Gulf of Mexico Cold Seep Sediments

ABSTRACT Gulf of Mexico sediments harbor numerous hydrocarbon seeps associated with high sedimentation rates and thermal maturation of organic matter. These ecosystems host abundant and diverse microbial communities that directly or indirectly metabolize components of the emitted fluid. To investiga...

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Autores principales:	Adrien Vigneron, Eric B. Alsop, Perrine Cruaud, Gwenaelle Philibert, Benjamin King, Leslie Baksmaty, David Lavallee, Bartholomeus P. Lomans, Emiley Eloe-Fadrosh, Nikos C. Kyrpides, Ian M. Head, Nicolas Tsesmetzis
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	AOM metagenomic metatranscriptomic methane polysulfide Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/396eebc8155e4e69b48ca07d53fe64f2
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spelling	oai:doaj.org-article:396eebc8155e4e69b48ca07d53fe64f22021-12-02T19:46:18ZContrasting Pathways for Anaerobic Methane Oxidation in Gulf of Mexico Cold Seep Sediments10.1128/mSystems.00091-182379-5077https://doaj.org/article/396eebc8155e4e69b48ca07d53fe64f22019-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00091-18https://doaj.org/toc/2379-5077ABSTRACT Gulf of Mexico sediments harbor numerous hydrocarbon seeps associated with high sedimentation rates and thermal maturation of organic matter. These ecosystems host abundant and diverse microbial communities that directly or indirectly metabolize components of the emitted fluid. To investigate microbial function and activities in these ecosystems, metabolic potential (metagenomic) and gene expression (metatranscriptomic) analyses of two cold seep areas of the Gulf of Mexico were carried out. Seeps emitting biogenic methane harbored microbial communities dominated by archaeal anaerobic methane oxidizers of phylogenetic group 1 (ANME-1), whereas seeps producing fluids containing a complex mixture of thermogenic hydrocarbons were dominated by ANME-2 lineages. Metatranscriptome measurements in both communities indicated high levels of expression of genes for methane metabolism despite their distinct microbial communities and hydrocarbon composition. In contrast, the transcription level of sulfur cycle genes was quite different. In the thermogenic seep community, high levels of transcripts indicative of syntrophic anaerobic oxidation of methane (AOM) coupled to sulfate reduction were detected. This syntrophic partnership between the dominant ANME-2 and sulfate reducers potentially involves direct electron transfer through multiheme cytochromes. In the biogenic methane seep, genes from an ANME-1 lineage that are potentially involved in polysulfide reduction were highly expressed, suggesting a novel bacterium-independent anaerobic methane oxidation pathway coupled to polysulfide reduction. The observed divergence in AOM activities provides a new model for bacterium-independent AOM and emphasizes the variation that exists in AOM pathways between different ANME lineages. IMPORTANCE Cold seep sediments are complex and widespread marine ecosystems emitting large amounts of methane, a potent greenhouse gas, and other hydrocarbons. Within these sediments, microbial communities play crucial roles in production and degradation of hydrocarbons, modulating oil and gas emissions to seawater. Despite this ecological importance, our understanding of microbial functions and methane oxidation pathways in cold seep ecosystems is poor. Based on gene expression profiling of environmental seep sediment samples, the present work showed that (i) the composition of the emitted fluids shapes the microbial community in general and the anaerobic methanotroph community specifically and (ii) AOM by ANME-2 in this seep may be coupled to sulfate reduction by Deltaproteobacteria by electron transfer through multiheme cytochromes, whereas AOM by ANME-1 lineages in this seep may involve a different, bacterium-independent pathway, coupling methane oxidation to elemental sulfur/polysulfide reduction.Adrien VigneronEric B. AlsopPerrine CruaudGwenaelle PhilibertBenjamin KingLeslie BaksmatyDavid LavalleeBartholomeus P. LomansEmiley Eloe-FadroshNikos C. KyrpidesIan M. HeadNicolas TsesmetzisAmerican Society for MicrobiologyarticleAOMmetagenomicmetatranscriptomicmethanepolysulfideMicrobiologyQR1-502ENmSystems, Vol 4, Iss 1 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	AOM metagenomic metatranscriptomic methane polysulfide Microbiology QR1-502
spellingShingle	AOM metagenomic metatranscriptomic methane polysulfide Microbiology QR1-502 Adrien Vigneron Eric B. Alsop Perrine Cruaud Gwenaelle Philibert Benjamin King Leslie Baksmaty David Lavallee Bartholomeus P. Lomans Emiley Eloe-Fadrosh Nikos C. Kyrpides Ian M. Head Nicolas Tsesmetzis Contrasting Pathways for Anaerobic Methane Oxidation in Gulf of Mexico Cold Seep Sediments
description	ABSTRACT Gulf of Mexico sediments harbor numerous hydrocarbon seeps associated with high sedimentation rates and thermal maturation of organic matter. These ecosystems host abundant and diverse microbial communities that directly or indirectly metabolize components of the emitted fluid. To investigate microbial function and activities in these ecosystems, metabolic potential (metagenomic) and gene expression (metatranscriptomic) analyses of two cold seep areas of the Gulf of Mexico were carried out. Seeps emitting biogenic methane harbored microbial communities dominated by archaeal anaerobic methane oxidizers of phylogenetic group 1 (ANME-1), whereas seeps producing fluids containing a complex mixture of thermogenic hydrocarbons were dominated by ANME-2 lineages. Metatranscriptome measurements in both communities indicated high levels of expression of genes for methane metabolism despite their distinct microbial communities and hydrocarbon composition. In contrast, the transcription level of sulfur cycle genes was quite different. In the thermogenic seep community, high levels of transcripts indicative of syntrophic anaerobic oxidation of methane (AOM) coupled to sulfate reduction were detected. This syntrophic partnership between the dominant ANME-2 and sulfate reducers potentially involves direct electron transfer through multiheme cytochromes. In the biogenic methane seep, genes from an ANME-1 lineage that are potentially involved in polysulfide reduction were highly expressed, suggesting a novel bacterium-independent anaerobic methane oxidation pathway coupled to polysulfide reduction. The observed divergence in AOM activities provides a new model for bacterium-independent AOM and emphasizes the variation that exists in AOM pathways between different ANME lineages. IMPORTANCE Cold seep sediments are complex and widespread marine ecosystems emitting large amounts of methane, a potent greenhouse gas, and other hydrocarbons. Within these sediments, microbial communities play crucial roles in production and degradation of hydrocarbons, modulating oil and gas emissions to seawater. Despite this ecological importance, our understanding of microbial functions and methane oxidation pathways in cold seep ecosystems is poor. Based on gene expression profiling of environmental seep sediment samples, the present work showed that (i) the composition of the emitted fluids shapes the microbial community in general and the anaerobic methanotroph community specifically and (ii) AOM by ANME-2 in this seep may be coupled to sulfate reduction by Deltaproteobacteria by electron transfer through multiheme cytochromes, whereas AOM by ANME-1 lineages in this seep may involve a different, bacterium-independent pathway, coupling methane oxidation to elemental sulfur/polysulfide reduction.
format	article
author	Adrien Vigneron Eric B. Alsop Perrine Cruaud Gwenaelle Philibert Benjamin King Leslie Baksmaty David Lavallee Bartholomeus P. Lomans Emiley Eloe-Fadrosh Nikos C. Kyrpides Ian M. Head Nicolas Tsesmetzis
author_facet	Adrien Vigneron Eric B. Alsop Perrine Cruaud Gwenaelle Philibert Benjamin King Leslie Baksmaty David Lavallee Bartholomeus P. Lomans Emiley Eloe-Fadrosh Nikos C. Kyrpides Ian M. Head Nicolas Tsesmetzis
author_sort	Adrien Vigneron
title	Contrasting Pathways for Anaerobic Methane Oxidation in Gulf of Mexico Cold Seep Sediments
title_short	Contrasting Pathways for Anaerobic Methane Oxidation in Gulf of Mexico Cold Seep Sediments
title_full	Contrasting Pathways for Anaerobic Methane Oxidation in Gulf of Mexico Cold Seep Sediments
title_fullStr	Contrasting Pathways for Anaerobic Methane Oxidation in Gulf of Mexico Cold Seep Sediments
title_full_unstemmed	Contrasting Pathways for Anaerobic Methane Oxidation in Gulf of Mexico Cold Seep Sediments
title_sort	contrasting pathways for anaerobic methane oxidation in gulf of mexico cold seep sediments
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/396eebc8155e4e69b48ca07d53fe64f2
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Contrasting Pathways for Anaerobic Methane Oxidation in Gulf of Mexico Cold Seep Sediments

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