Methylotrophy in the Mire: direct and indirect routes for methane production in thawing permafrost
AbstractWhile wetlands are major sources of biogenic methane (CH 4 ), our understanding of resident microbial metabolism is incomplete, which compromises the prediction of CH 4 emissions under ongoing climate change. Here, we employed genome-resolved multi-omics to expand our understanding of methan...
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American Society for Microbiology
2023
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ftqueensland:oai:eprints.qut.edu.au:245204 2024-01-14T10:05:00+01:00 Methylotrophy in the Mire: direct and indirect routes for methane production in thawing permafrost Ellenbogen, Jared B Borton, Mikayla A. McGivern, Bridget B Cronin, Dylan R. Hoyt, David W Freire-Zapata, Viviana McCalley, Carmody K. Varner, Ruth K. Crill, Patrick M. Wehr, Richard A. Chanton, Jeffrey P. Woodcroft, Ben J Tfaily, Malak M Tyson, Gene W Rich, Virginia I Wrighton, Kelly C. 2023-12-08 https://eprints.qut.edu.au/245204/ unknown American Society for Microbiology doi:10.1128/msystems.00698-23 Ellenbogen, Jared B, Borton, Mikayla A., McGivern, Bridget B, Cronin, Dylan R., Hoyt, David W, Freire-Zapata, Viviana, McCalley, Carmody K., Varner, Ruth K., Crill, Patrick M., Wehr, Richard A., Chanton, Jeffrey P., Woodcroft, Ben J, Tfaily, Malak M, Tyson, Gene W, Rich, Virginia I, & Wrighton, Kelly C. (2023) Methylotrophy in the Mire: direct and indirect routes for methane production in thawing permafrost. mSystems, Article number: e0069823. https://eprints.qut.edu.au/245204/ Faculty of Health; School of Biomedical Sciences 2023 The Authors This work is covered by copyright. Unless the document is being made available under a Creative Commons Licence, you must assume that re-use is limited to personal use and that permission from the copyright owner must be obtained for all other uses. If the document is available under a Creative Commons License (or other specified license) then refer to the Licence for details of permitted re-use. It is a condition of access that users recognise and abide by the legal requirements associated with these rights. If you believe that this work infringes copyright please provide details by email to qut.copyright@qut.edu.au mSystems Contribution to Journal 2023 ftqueensland https://doi.org/10.1128/msystems.00698-23 2023-12-18T23:26:31Z AbstractWhile wetlands are major sources of biogenic methane (CH 4 ), our understanding of resident microbial metabolism is incomplete, which compromises the prediction of CH 4 emissions under ongoing climate change. Here, we employed genome-resolved multi-omics to expand our understanding of methanogenesis in the thawing permafrost peatland of Stordalen Mire in Arctic Sweden. In quadrupling the genomic representation of the site’s methanogens and examining their encoded metabolism, we revealed that nearly 20% of the metagenome-assembled genomes (MAGs) encoded the potential for methylotrophic methanogenesis. Further, 27% of the transcriptionally active methanogens expressed methylotrophic genes; for Methanosarcinales and Methanobacteriales MAGs, these data indicated the use of methylated oxygen compounds (e.g., methanol), while for Methanomassiliicoccales , they primarily implicated methyl sulfides and methylamines. In addition to methanogenic methylotrophy, >1,700 bacterial MAGs across 19 phyla encoded anaerobic methylotrophic potential, with expression across 12 phyla. Metabolomic analyses revealed the presence of diverse methylated compounds in the Mire, including some known methylotrophic substrates. Active methylotrophy was observed across all stages of a permafrost thaw gradient in Stordalen, with the most frozen non-methanogenic palsa found to host bacterial methylotrophy and the partially thawed bog and fully thawed fen seen to house both methanogenic and bacterial methylotrophic activities. Methanogenesis across increasing permafrost thaw is thus revised from the sole dominance of hydrogenotrophic production and the appearance of acetoclastic at full thaw to consider the co-occurrence of methylotrophy throughout. Collectively, these findings indicate that methanogenic and bacterial methylotrophy may be an important and previously underappreciated component of carbon cycling and emissions in these rapidly changing wetland habitats. ImportanceWetlands are the biggest natural source of atmospheric ... Article in Journal/Newspaper Arctic Climate change palsa permafrost Queensland University of Technology: QUT ePrints Arctic Stordalen ENVELOPE(7.337,7.337,62.510,62.510) mSystems |
institution |
Open Polar |
collection |
Queensland University of Technology: QUT ePrints |
op_collection_id |
ftqueensland |
language |
unknown |
description |
AbstractWhile wetlands are major sources of biogenic methane (CH 4 ), our understanding of resident microbial metabolism is incomplete, which compromises the prediction of CH 4 emissions under ongoing climate change. Here, we employed genome-resolved multi-omics to expand our understanding of methanogenesis in the thawing permafrost peatland of Stordalen Mire in Arctic Sweden. In quadrupling the genomic representation of the site’s methanogens and examining their encoded metabolism, we revealed that nearly 20% of the metagenome-assembled genomes (MAGs) encoded the potential for methylotrophic methanogenesis. Further, 27% of the transcriptionally active methanogens expressed methylotrophic genes; for Methanosarcinales and Methanobacteriales MAGs, these data indicated the use of methylated oxygen compounds (e.g., methanol), while for Methanomassiliicoccales , they primarily implicated methyl sulfides and methylamines. In addition to methanogenic methylotrophy, >1,700 bacterial MAGs across 19 phyla encoded anaerobic methylotrophic potential, with expression across 12 phyla. Metabolomic analyses revealed the presence of diverse methylated compounds in the Mire, including some known methylotrophic substrates. Active methylotrophy was observed across all stages of a permafrost thaw gradient in Stordalen, with the most frozen non-methanogenic palsa found to host bacterial methylotrophy and the partially thawed bog and fully thawed fen seen to house both methanogenic and bacterial methylotrophic activities. Methanogenesis across increasing permafrost thaw is thus revised from the sole dominance of hydrogenotrophic production and the appearance of acetoclastic at full thaw to consider the co-occurrence of methylotrophy throughout. Collectively, these findings indicate that methanogenic and bacterial methylotrophy may be an important and previously underappreciated component of carbon cycling and emissions in these rapidly changing wetland habitats. ImportanceWetlands are the biggest natural source of atmospheric ... |
format |
Article in Journal/Newspaper |
author |
Ellenbogen, Jared B Borton, Mikayla A. McGivern, Bridget B Cronin, Dylan R. Hoyt, David W Freire-Zapata, Viviana McCalley, Carmody K. Varner, Ruth K. Crill, Patrick M. Wehr, Richard A. Chanton, Jeffrey P. Woodcroft, Ben J Tfaily, Malak M Tyson, Gene W Rich, Virginia I Wrighton, Kelly C. |
spellingShingle |
Ellenbogen, Jared B Borton, Mikayla A. McGivern, Bridget B Cronin, Dylan R. Hoyt, David W Freire-Zapata, Viviana McCalley, Carmody K. Varner, Ruth K. Crill, Patrick M. Wehr, Richard A. Chanton, Jeffrey P. Woodcroft, Ben J Tfaily, Malak M Tyson, Gene W Rich, Virginia I Wrighton, Kelly C. Methylotrophy in the Mire: direct and indirect routes for methane production in thawing permafrost |
author_facet |
Ellenbogen, Jared B Borton, Mikayla A. McGivern, Bridget B Cronin, Dylan R. Hoyt, David W Freire-Zapata, Viviana McCalley, Carmody K. Varner, Ruth K. Crill, Patrick M. Wehr, Richard A. Chanton, Jeffrey P. Woodcroft, Ben J Tfaily, Malak M Tyson, Gene W Rich, Virginia I Wrighton, Kelly C. |
author_sort |
Ellenbogen, Jared B |
title |
Methylotrophy in the Mire: direct and indirect routes for methane production in thawing permafrost |
title_short |
Methylotrophy in the Mire: direct and indirect routes for methane production in thawing permafrost |
title_full |
Methylotrophy in the Mire: direct and indirect routes for methane production in thawing permafrost |
title_fullStr |
Methylotrophy in the Mire: direct and indirect routes for methane production in thawing permafrost |
title_full_unstemmed |
Methylotrophy in the Mire: direct and indirect routes for methane production in thawing permafrost |
title_sort |
methylotrophy in the mire: direct and indirect routes for methane production in thawing permafrost |
publisher |
American Society for Microbiology |
publishDate |
2023 |
url |
https://eprints.qut.edu.au/245204/ |
long_lat |
ENVELOPE(7.337,7.337,62.510,62.510) |
geographic |
Arctic Stordalen |
geographic_facet |
Arctic Stordalen |
genre |
Arctic Climate change palsa permafrost |
genre_facet |
Arctic Climate change palsa permafrost |
op_source |
mSystems |
op_relation |
doi:10.1128/msystems.00698-23 Ellenbogen, Jared B, Borton, Mikayla A., McGivern, Bridget B, Cronin, Dylan R., Hoyt, David W, Freire-Zapata, Viviana, McCalley, Carmody K., Varner, Ruth K., Crill, Patrick M., Wehr, Richard A., Chanton, Jeffrey P., Woodcroft, Ben J, Tfaily, Malak M, Tyson, Gene W, Rich, Virginia I, & Wrighton, Kelly C. (2023) Methylotrophy in the Mire: direct and indirect routes for methane production in thawing permafrost. mSystems, Article number: e0069823. https://eprints.qut.edu.au/245204/ Faculty of Health; School of Biomedical Sciences |
op_rights |
2023 The Authors This work is covered by copyright. Unless the document is being made available under a Creative Commons Licence, you must assume that re-use is limited to personal use and that permission from the copyright owner must be obtained for all other uses. If the document is available under a Creative Commons License (or other specified license) then refer to the Licence for details of permitted re-use. It is a condition of access that users recognise and abide by the legal requirements associated with these rights. If you believe that this work infringes copyright please provide details by email to qut.copyright@qut.edu.au |
op_doi |
https://doi.org/10.1128/msystems.00698-23 |
container_title |
mSystems |
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