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 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 novelmore »
- Authors:
-
- Newcastle Univ., Newcastle Upon Tyne (United Kingdom); Shell International Exploration and Production Inc., Houston, TX (United States)
- Laval Univ., Quebec City, QC (Canada)
- Shell International Exploration and Production Inc., Houston, TX (United States)
- Shell Global Solutions International B.V., Rijswijk (Netherlands)
- USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
- Newcastle Univ., Newcastle Upon Tyne (United Kingdom)
- Univ. of British Columbia, Vancouver, BC (Canada)
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES)
- OSTI Identifier:
- 1559175
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- Accepted Manuscript
- Journal Name:
- mSystems
- Additional Journal Information:
- Journal Volume: 4; Journal Issue: 1; Journal ID: ISSN 2379-5077
- Publisher:
- American Society for Microbiology
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Vigneron, Adrien, Alsop, Eric B., Cruaud, Perrine, Philibert, Gwenaelle, King, Benjamin, Baksmaty, Leslie, Lavallee, David, Lomans, Bartholomeus P., Eloe-Fadrosh, Emiley, Kyrpides, Nikos C., Head, Ian M., Tsesmetzis, Nicolas, and Hallam, Steven J. Contrasting Pathways for Anaerobic Methane Oxidation in Gulf of Mexico Cold Seep Sediments. United States: N. p., 2019.
Web. doi:10.1128/mSystems.00091-18.
Vigneron, Adrien, Alsop, Eric B., Cruaud, Perrine, Philibert, Gwenaelle, King, Benjamin, Baksmaty, Leslie, Lavallee, David, Lomans, Bartholomeus P., Eloe-Fadrosh, Emiley, Kyrpides, Nikos C., Head, Ian M., Tsesmetzis, Nicolas, & Hallam, Steven J. Contrasting Pathways for Anaerobic Methane Oxidation in Gulf of Mexico Cold Seep Sediments. United States. https://doi.org/10.1128/mSystems.00091-18
Vigneron, Adrien, Alsop, Eric B., Cruaud, Perrine, Philibert, Gwenaelle, King, Benjamin, Baksmaty, Leslie, Lavallee, David, Lomans, Bartholomeus P., Eloe-Fadrosh, Emiley, Kyrpides, Nikos C., Head, Ian M., Tsesmetzis, Nicolas, and Hallam, Steven J. Tue .
"Contrasting Pathways for Anaerobic Methane Oxidation in Gulf of Mexico Cold Seep Sediments". United States. https://doi.org/10.1128/mSystems.00091-18. https://www.osti.gov/servlets/purl/1559175.
@article{osti_1559175,
title = {Contrasting Pathways for Anaerobic Methane Oxidation in Gulf of Mexico Cold Seep Sediments},
author = {Vigneron, Adrien and Alsop, Eric B. and Cruaud, Perrine and Philibert, Gwenaelle and King, Benjamin and Baksmaty, Leslie and Lavallee, David and Lomans, Bartholomeus P. and Eloe-Fadrosh, Emiley and Kyrpides, Nikos C. and Head, Ian M. and Tsesmetzis, Nicolas and Hallam, Steven J.},
abstractNote = {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. IMPORTANCECold 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.},
doi = {10.1128/mSystems.00091-18},
journal = {mSystems},
number = 1,
volume = 4,
place = {United States},
year = {Tue Feb 26 00:00:00 EST 2019},
month = {Tue Feb 26 00:00:00 EST 2019}
}
Web of Science
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