Unique high Arctic methane metabolizing community revealed through in situ ¹³CH₄-DNA-SIP enrichment in concert with genome binning
Greenhouse gas (GHG) emissions from Arctic permafrost soils create a positive feedback loop of climate warming and further GHG emissions. Active methane uptake in these soils can reduce the impact of GHG on future Arctic warming potential. Aerobic methane oxidizers are thought to be responsible for...
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Springer Nature Limited
2022
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Online Access: | https://doi.org/10.1038/s41598-021-04486-z https://nrc-publications.canada.ca/eng/view/ft/?id=da140a51-613d-4cba-b53d-f446c6ff3034 https://nrc-publications.canada.ca/eng/view/object/?id=da140a51-613d-4cba-b53d-f446c6ff3034 https://nrc-publications.canada.ca/fra/voir/objet/?id=da140a51-613d-4cba-b53d-f446c6ff3034 |
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ftnrccanada:oai:cisti-icist.nrc-cnrc.ca:cistinparc:da140a51-613d-4cba-b53d-f446c6ff3034 2023-05-15T14:31:47+02:00 Unique high Arctic methane metabolizing community revealed through in situ ¹³CH₄-DNA-SIP enrichment in concert with genome binning Altshuler, Ianina Raymond-Bouchard, Isabelle Magnuson, Elisse Tremblay, Julien Greer, Charles W. Whyte, Lyle G. 2022-01-21 text https://doi.org/10.1038/s41598-021-04486-z https://nrc-publications.canada.ca/eng/view/ft/?id=da140a51-613d-4cba-b53d-f446c6ff3034 https://nrc-publications.canada.ca/eng/view/object/?id=da140a51-613d-4cba-b53d-f446c6ff3034 https://nrc-publications.canada.ca/fra/voir/objet/?id=da140a51-613d-4cba-b53d-f446c6ff3034 eng eng Springer Nature Limited issn:2045-2322 Scientific Reports, Volume: 12, Issue: 1, Publication date: 2022-01-21 doi:10.1038/s41598-021-04486-z Creative Commons, Attribution 4.0 Generic (CC BY 4.0) (https://creativecommons.org/licenses/by/4.0/) Creative Commons, Attribution 4.0 Générique (CC BY 4.0) (https://creativecommons.org/licenses/by/4.0/deed.fr) CC-BY article 2022 ftnrccanada https://doi.org/10.1038/s41598-021-04486-z 2022-03-20T00:00:57Z Greenhouse gas (GHG) emissions from Arctic permafrost soils create a positive feedback loop of climate warming and further GHG emissions. Active methane uptake in these soils can reduce the impact of GHG on future Arctic warming potential. Aerobic methane oxidizers are thought to be responsible for this apparent methane sink, though Arctic representatives of these organisms have resisted culturing efforts. Here, we first used in situ gas flux measurements and qPCR to identify relative methane sink hotspots at a high Arctic cytosol site, we then labeled the active microbiome in situ using DNA Stable Isotope Probing (SIP) with heavy ¹³CH₄ (at 100 ppm and 1000 ppm). This was followed by amplicon and metagenome sequencing to identify active organisms involved in CH₄ metabolism in these high Arctic cryosols. Sequencing of ¹³C-labeled pmoA genes demonstrated that type II methanotrophs (Methylocapsa) were overall the dominant active methane oxidizers in these mineral cryosols, while type I methanotrophs (Methylomarinovum) were only detected in the 100 ppm SIP treatment. From the SIP-¹³C-labeled DNA, we retrieved nine high to intermediate quality metagenome-assembled genomes (MAGs) belonging to the Proteobacteria, Gemmatimonadetes, and Chloroflexi, with three of these MAGs containing genes associated with methanotrophy. A novel Chloroflexi MAG contained a mmoX gene along with other methane oxidation pathway genes, identifying it as a potential uncultured methane oxidizer. This MAG also contained genes for copper import, synthesis of biopolymers, mercury detoxification, and ammonia uptake, indicating that this bacterium is strongly adapted to conditions in active layer permafrost and providing new insights into methane biogeochemical cycling. In addition, Betaproteobacterial MAGs were also identified as potential cross-feeders with methanotrophs in these Arctic cryosols. Overall, in situ SIP labeling combined with metagenomics and genome binning demonstrated to be a useful tool for discovering and characterizing novel organisms related to specific microbial functions or biogeochemical cycles of interest. Our findings reveal a unique and active Arctic cryosol microbial community potentially involved in CH₄ cycling. Peer reviewed: Yes NRC publication: Yes Article in Journal/Newspaper arctic methane Arctic permafrost National Research Council Canada: NRC Publications Archive Arctic Scientific Reports 12 1 |
institution |
Open Polar |
collection |
National Research Council Canada: NRC Publications Archive |
op_collection_id |
ftnrccanada |
language |
English |
description |
Greenhouse gas (GHG) emissions from Arctic permafrost soils create a positive feedback loop of climate warming and further GHG emissions. Active methane uptake in these soils can reduce the impact of GHG on future Arctic warming potential. Aerobic methane oxidizers are thought to be responsible for this apparent methane sink, though Arctic representatives of these organisms have resisted culturing efforts. Here, we first used in situ gas flux measurements and qPCR to identify relative methane sink hotspots at a high Arctic cytosol site, we then labeled the active microbiome in situ using DNA Stable Isotope Probing (SIP) with heavy ¹³CH₄ (at 100 ppm and 1000 ppm). This was followed by amplicon and metagenome sequencing to identify active organisms involved in CH₄ metabolism in these high Arctic cryosols. Sequencing of ¹³C-labeled pmoA genes demonstrated that type II methanotrophs (Methylocapsa) were overall the dominant active methane oxidizers in these mineral cryosols, while type I methanotrophs (Methylomarinovum) were only detected in the 100 ppm SIP treatment. From the SIP-¹³C-labeled DNA, we retrieved nine high to intermediate quality metagenome-assembled genomes (MAGs) belonging to the Proteobacteria, Gemmatimonadetes, and Chloroflexi, with three of these MAGs containing genes associated with methanotrophy. A novel Chloroflexi MAG contained a mmoX gene along with other methane oxidation pathway genes, identifying it as a potential uncultured methane oxidizer. This MAG also contained genes for copper import, synthesis of biopolymers, mercury detoxification, and ammonia uptake, indicating that this bacterium is strongly adapted to conditions in active layer permafrost and providing new insights into methane biogeochemical cycling. In addition, Betaproteobacterial MAGs were also identified as potential cross-feeders with methanotrophs in these Arctic cryosols. Overall, in situ SIP labeling combined with metagenomics and genome binning demonstrated to be a useful tool for discovering and characterizing novel organisms related to specific microbial functions or biogeochemical cycles of interest. Our findings reveal a unique and active Arctic cryosol microbial community potentially involved in CH₄ cycling. Peer reviewed: Yes NRC publication: Yes |
format |
Article in Journal/Newspaper |
author |
Altshuler, Ianina Raymond-Bouchard, Isabelle Magnuson, Elisse Tremblay, Julien Greer, Charles W. Whyte, Lyle G. |
spellingShingle |
Altshuler, Ianina Raymond-Bouchard, Isabelle Magnuson, Elisse Tremblay, Julien Greer, Charles W. Whyte, Lyle G. Unique high Arctic methane metabolizing community revealed through in situ ¹³CH₄-DNA-SIP enrichment in concert with genome binning |
author_facet |
Altshuler, Ianina Raymond-Bouchard, Isabelle Magnuson, Elisse Tremblay, Julien Greer, Charles W. Whyte, Lyle G. |
author_sort |
Altshuler, Ianina |
title |
Unique high Arctic methane metabolizing community revealed through in situ ¹³CH₄-DNA-SIP enrichment in concert with genome binning |
title_short |
Unique high Arctic methane metabolizing community revealed through in situ ¹³CH₄-DNA-SIP enrichment in concert with genome binning |
title_full |
Unique high Arctic methane metabolizing community revealed through in situ ¹³CH₄-DNA-SIP enrichment in concert with genome binning |
title_fullStr |
Unique high Arctic methane metabolizing community revealed through in situ ¹³CH₄-DNA-SIP enrichment in concert with genome binning |
title_full_unstemmed |
Unique high Arctic methane metabolizing community revealed through in situ ¹³CH₄-DNA-SIP enrichment in concert with genome binning |
title_sort |
unique high arctic methane metabolizing community revealed through in situ ¹³ch₄-dna-sip enrichment in concert with genome binning |
publisher |
Springer Nature Limited |
publishDate |
2022 |
url |
https://doi.org/10.1038/s41598-021-04486-z https://nrc-publications.canada.ca/eng/view/ft/?id=da140a51-613d-4cba-b53d-f446c6ff3034 https://nrc-publications.canada.ca/eng/view/object/?id=da140a51-613d-4cba-b53d-f446c6ff3034 https://nrc-publications.canada.ca/fra/voir/objet/?id=da140a51-613d-4cba-b53d-f446c6ff3034 |
geographic |
Arctic |
geographic_facet |
Arctic |
genre |
arctic methane Arctic permafrost |
genre_facet |
arctic methane Arctic permafrost |
op_relation |
issn:2045-2322 Scientific Reports, Volume: 12, Issue: 1, Publication date: 2022-01-21 doi:10.1038/s41598-021-04486-z |
op_rights |
Creative Commons, Attribution 4.0 Generic (CC BY 4.0) (https://creativecommons.org/licenses/by/4.0/) Creative Commons, Attribution 4.0 Générique (CC BY 4.0) (https://creativecommons.org/licenses/by/4.0/deed.fr) |
op_rightsnorm |
CC-BY |
op_doi |
https://doi.org/10.1038/s41598-021-04486-z |
container_title |
Scientific Reports |
container_volume |
12 |
container_issue |
1 |
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1766305324412698624 |