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Biological methane production and accumulation under sulfate-rich conditions at Cape Lookout Bight, NC

INTRODUCTION: Anaerobic oxidation of methane (AOM) is hypothesized to occur through reverse hydrogenotrophic methanogenesis in marine sediments because sulfate reducers pull hydrogen concentrations so low that reverse hydrogenotrophic methanogenesis is exergonic. If true, hydrogenotrophic methanogen...

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Autores principales: Coon, Gage R., Duesing, Paul D., Paul, Raegan, Baily, Jennifer A., Lloyd, Karen G.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10587565/
https://www.ncbi.nlm.nih.gov/pubmed/37869653
http://dx.doi.org/10.3389/fmicb.2023.1268361
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author Coon, Gage R.
Duesing, Paul D.
Paul, Raegan
Baily, Jennifer A.
Lloyd, Karen G.
author_facet Coon, Gage R.
Duesing, Paul D.
Paul, Raegan
Baily, Jennifer A.
Lloyd, Karen G.
author_sort Coon, Gage R.
collection PubMed
description INTRODUCTION: Anaerobic oxidation of methane (AOM) is hypothesized to occur through reverse hydrogenotrophic methanogenesis in marine sediments because sulfate reducers pull hydrogen concentrations so low that reverse hydrogenotrophic methanogenesis is exergonic. If true, hydrogenotrophic methanogenesis can theoretically co-occur with sulfate reduction if the organic matter is so labile that fermenters produce more hydrogen than sulfate reducers can consume, causing hydrogen concentrations to rise. Finding accumulation of biologically-produced methane in sulfate-containing organic-rich sediments would therefore support the theory that AOM occurs through reverse hydrogenotrophic methanogenesis since it would signal the absence of net AOM in the presence of sulfate. METHODS: 16S rRNA gene libraries were compared to geochemistry and incubations in high depth-resolution sediment cores collected from organic-rich Cape Lookout Bight, North Carolina. RESULTS: We found that methane began to accumulate while sulfate is still abundant (6–8 mM). Methane-cycling archaea ANME-1, Methanosarciniales, and Methanomicrobiales also increased at these depths. Incubations showed that methane production in the upper 16 cm in sulfate-rich sediments was biotic since it could be inhibited by 2-bromoethanosulfonoic acid (BES). DISCUSSION: We conclude that methanogens mediate biological methane production in these organic-rich sediments at sulfate concentrations that inhibit methanogenesis in sediments with less labile organic matter, and that methane accumulation and growth of methanogens can occur under these conditions as well. Our data supports the theory that H(2) concentrations, rather than the co-occurrence of sulfate and methane, control whether methanogenesis or AOM via reverse hydrogenotrophic methanogenesis occurs. We hypothesize that the high amount of labile organic matter at this site prevents AOM, allowing methane accumulation when sulfate is low but still present in mM concentrations.
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spelling pubmed-105875652023-10-21 Biological methane production and accumulation under sulfate-rich conditions at Cape Lookout Bight, NC Coon, Gage R. Duesing, Paul D. Paul, Raegan Baily, Jennifer A. Lloyd, Karen G. Front Microbiol Microbiology INTRODUCTION: Anaerobic oxidation of methane (AOM) is hypothesized to occur through reverse hydrogenotrophic methanogenesis in marine sediments because sulfate reducers pull hydrogen concentrations so low that reverse hydrogenotrophic methanogenesis is exergonic. If true, hydrogenotrophic methanogenesis can theoretically co-occur with sulfate reduction if the organic matter is so labile that fermenters produce more hydrogen than sulfate reducers can consume, causing hydrogen concentrations to rise. Finding accumulation of biologically-produced methane in sulfate-containing organic-rich sediments would therefore support the theory that AOM occurs through reverse hydrogenotrophic methanogenesis since it would signal the absence of net AOM in the presence of sulfate. METHODS: 16S rRNA gene libraries were compared to geochemistry and incubations in high depth-resolution sediment cores collected from organic-rich Cape Lookout Bight, North Carolina. RESULTS: We found that methane began to accumulate while sulfate is still abundant (6–8 mM). Methane-cycling archaea ANME-1, Methanosarciniales, and Methanomicrobiales also increased at these depths. Incubations showed that methane production in the upper 16 cm in sulfate-rich sediments was biotic since it could be inhibited by 2-bromoethanosulfonoic acid (BES). DISCUSSION: We conclude that methanogens mediate biological methane production in these organic-rich sediments at sulfate concentrations that inhibit methanogenesis in sediments with less labile organic matter, and that methane accumulation and growth of methanogens can occur under these conditions as well. Our data supports the theory that H(2) concentrations, rather than the co-occurrence of sulfate and methane, control whether methanogenesis or AOM via reverse hydrogenotrophic methanogenesis occurs. We hypothesize that the high amount of labile organic matter at this site prevents AOM, allowing methane accumulation when sulfate is low but still present in mM concentrations. Frontiers Media S.A. 2023-10-06 /pmc/articles/PMC10587565/ /pubmed/37869653 http://dx.doi.org/10.3389/fmicb.2023.1268361 Text en Copyright © 2023 Coon, Duesing, Paul, Baily and Lloyd. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Coon, Gage R.
Duesing, Paul D.
Paul, Raegan
Baily, Jennifer A.
Lloyd, Karen G.
Biological methane production and accumulation under sulfate-rich conditions at Cape Lookout Bight, NC
title Biological methane production and accumulation under sulfate-rich conditions at Cape Lookout Bight, NC
title_full Biological methane production and accumulation under sulfate-rich conditions at Cape Lookout Bight, NC
title_fullStr Biological methane production and accumulation under sulfate-rich conditions at Cape Lookout Bight, NC
title_full_unstemmed Biological methane production and accumulation under sulfate-rich conditions at Cape Lookout Bight, NC
title_short Biological methane production and accumulation under sulfate-rich conditions at Cape Lookout Bight, NC
title_sort biological methane production and accumulation under sulfate-rich conditions at cape lookout bight, nc
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10587565/
https://www.ncbi.nlm.nih.gov/pubmed/37869653
http://dx.doi.org/10.3389/fmicb.2023.1268361
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