Life at the Frozen Limit: Microbial Carbon Metabolism Across a Late Pleistocene Permafrost Chronosequence
Permafrost is an extreme habitat yet it hosts microbial populations that remain active over millennia. Using permafrost collected from a Pleistocene chronosequence (19 to 33 ka), we hypothesized that the functional genetic potential of microbial communities in permafrost would reflect microbial stra...
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ftdoajarticles:oai:doaj.org/article:ec5919b4b5f14d9d8bb94a671312cbc5 2023-05-15T17:55:16+02:00 Life at the Frozen Limit: Microbial Carbon Metabolism Across a Late Pleistocene Permafrost Chronosequence Mary-Cathrine Leewis Renaud Berlemont David C. Podgorski Archana Srinivas Phoebe Zito Robert G. M. Spencer Jack McFarland Thomas A. Douglas Christopher H. Conaway Mark Waldrop Rachel Mackelprang 2020-07-01T00:00:00Z https://doi.org/10.3389/fmicb.2020.01753 https://doaj.org/article/ec5919b4b5f14d9d8bb94a671312cbc5 EN eng Frontiers Media S.A. https://www.frontiersin.org/article/10.3389/fmicb.2020.01753/full https://doaj.org/toc/1664-302X 1664-302X doi:10.3389/fmicb.2020.01753 https://doaj.org/article/ec5919b4b5f14d9d8bb94a671312cbc5 Frontiers in Microbiology, Vol 11 (2020) permafrost Pleistocene carbohydrate active enzymes CAZyme carbon FT-ICR MS Microbiology QR1-502 article 2020 ftdoajarticles https://doi.org/10.3389/fmicb.2020.01753 2022-12-30T20:47:52Z Permafrost is an extreme habitat yet it hosts microbial populations that remain active over millennia. Using permafrost collected from a Pleistocene chronosequence (19 to 33 ka), we hypothesized that the functional genetic potential of microbial communities in permafrost would reflect microbial strategies to metabolize permafrost soluble organic matter (OM) in situ over geologic time. We also hypothesized that changes in the metagenome across the chronosequence would correlate with shifts in carbon chemistry, permafrost age, and paleoclimate at the time of permafrost formation. We combined high-resolution characterization of water-soluble OM by Fourier-transform ion-cyclotron-resonance mass spectrometry (FT-ICR MS), quantification of organic anions in permafrost water extracts, and metagenomic sequencing to better understand the relationships between the molecular-level composition of potentially bioavailable OM, the microbial community, and permafrost age. Both age and paleoclimate had marked effects on both the molecular composition of dissolved OM and the microbial community. The relative abundance of genes associated with hydrogenotrophic methanogenesis, carbohydrate active enzyme families, nominal oxidation state of carbon (NOSC), and number of identifiable molecular formulae significantly decreased with increasing age. In contrast, genes associated with fermentation of short chain fatty acids (SCFAs), the concentration of SCFAs and ammonium all significantly increased with age. We present a conceptual model of microbial metabolism in permafrost based on fermentation of OM and the buildup of organic acids that helps to explain the unique chemistry of ancient permafrost soils. These findings imply long-term in situ microbial turnover of ancient permafrost OM and that this pooled biolabile OM could prime ancient permafrost soils for a larger and more rapid microbial response to thaw compared to younger permafrost soils. Article in Journal/Newspaper permafrost Directory of Open Access Journals: DOAJ Articles Frontiers in Microbiology 11 |
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Open Polar |
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Directory of Open Access Journals: DOAJ Articles |
op_collection_id |
ftdoajarticles |
language |
English |
topic |
permafrost Pleistocene carbohydrate active enzymes CAZyme carbon FT-ICR MS Microbiology QR1-502 |
spellingShingle |
permafrost Pleistocene carbohydrate active enzymes CAZyme carbon FT-ICR MS Microbiology QR1-502 Mary-Cathrine Leewis Renaud Berlemont David C. Podgorski Archana Srinivas Phoebe Zito Robert G. M. Spencer Jack McFarland Thomas A. Douglas Christopher H. Conaway Mark Waldrop Rachel Mackelprang Life at the Frozen Limit: Microbial Carbon Metabolism Across a Late Pleistocene Permafrost Chronosequence |
topic_facet |
permafrost Pleistocene carbohydrate active enzymes CAZyme carbon FT-ICR MS Microbiology QR1-502 |
description |
Permafrost is an extreme habitat yet it hosts microbial populations that remain active over millennia. Using permafrost collected from a Pleistocene chronosequence (19 to 33 ka), we hypothesized that the functional genetic potential of microbial communities in permafrost would reflect microbial strategies to metabolize permafrost soluble organic matter (OM) in situ over geologic time. We also hypothesized that changes in the metagenome across the chronosequence would correlate with shifts in carbon chemistry, permafrost age, and paleoclimate at the time of permafrost formation. We combined high-resolution characterization of water-soluble OM by Fourier-transform ion-cyclotron-resonance mass spectrometry (FT-ICR MS), quantification of organic anions in permafrost water extracts, and metagenomic sequencing to better understand the relationships between the molecular-level composition of potentially bioavailable OM, the microbial community, and permafrost age. Both age and paleoclimate had marked effects on both the molecular composition of dissolved OM and the microbial community. The relative abundance of genes associated with hydrogenotrophic methanogenesis, carbohydrate active enzyme families, nominal oxidation state of carbon (NOSC), and number of identifiable molecular formulae significantly decreased with increasing age. In contrast, genes associated with fermentation of short chain fatty acids (SCFAs), the concentration of SCFAs and ammonium all significantly increased with age. We present a conceptual model of microbial metabolism in permafrost based on fermentation of OM and the buildup of organic acids that helps to explain the unique chemistry of ancient permafrost soils. These findings imply long-term in situ microbial turnover of ancient permafrost OM and that this pooled biolabile OM could prime ancient permafrost soils for a larger and more rapid microbial response to thaw compared to younger permafrost soils. |
format |
Article in Journal/Newspaper |
author |
Mary-Cathrine Leewis Renaud Berlemont David C. Podgorski Archana Srinivas Phoebe Zito Robert G. M. Spencer Jack McFarland Thomas A. Douglas Christopher H. Conaway Mark Waldrop Rachel Mackelprang |
author_facet |
Mary-Cathrine Leewis Renaud Berlemont David C. Podgorski Archana Srinivas Phoebe Zito Robert G. M. Spencer Jack McFarland Thomas A. Douglas Christopher H. Conaway Mark Waldrop Rachel Mackelprang |
author_sort |
Mary-Cathrine Leewis |
title |
Life at the Frozen Limit: Microbial Carbon Metabolism Across a Late Pleistocene Permafrost Chronosequence |
title_short |
Life at the Frozen Limit: Microbial Carbon Metabolism Across a Late Pleistocene Permafrost Chronosequence |
title_full |
Life at the Frozen Limit: Microbial Carbon Metabolism Across a Late Pleistocene Permafrost Chronosequence |
title_fullStr |
Life at the Frozen Limit: Microbial Carbon Metabolism Across a Late Pleistocene Permafrost Chronosequence |
title_full_unstemmed |
Life at the Frozen Limit: Microbial Carbon Metabolism Across a Late Pleistocene Permafrost Chronosequence |
title_sort |
life at the frozen limit: microbial carbon metabolism across a late pleistocene permafrost chronosequence |
publisher |
Frontiers Media S.A. |
publishDate |
2020 |
url |
https://doi.org/10.3389/fmicb.2020.01753 https://doaj.org/article/ec5919b4b5f14d9d8bb94a671312cbc5 |
genre |
permafrost |
genre_facet |
permafrost |
op_source |
Frontiers in Microbiology, Vol 11 (2020) |
op_relation |
https://www.frontiersin.org/article/10.3389/fmicb.2020.01753/full https://doaj.org/toc/1664-302X 1664-302X doi:10.3389/fmicb.2020.01753 https://doaj.org/article/ec5919b4b5f14d9d8bb94a671312cbc5 |
op_doi |
https://doi.org/10.3389/fmicb.2020.01753 |
container_title |
Frontiers in Microbiology |
container_volume |
11 |
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1766163184869179392 |