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Genomic evidence that microbial carbon degradation is dominated by iron redox metabolism in thawing permafrost
Microorganisms drive many aspects of organic carbon cycling in thawing permafrost soils, but the compositional trajectory of the post-thaw microbiome and its metabolic activity remain uncertain, which limits our ability to predict permafrost–climate feedbacks in a warming world. Using quantitative m...
Autores principales: | , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Nature Publishing Group UK
2023
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10667234/ https://www.ncbi.nlm.nih.gov/pubmed/37996661 http://dx.doi.org/10.1038/s43705-023-00326-5 |
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author | Romanowicz, Karl J. Crump, Byron C. Kling, George W. |
author_facet | Romanowicz, Karl J. Crump, Byron C. Kling, George W. |
author_sort | Romanowicz, Karl J. |
collection | PubMed |
description | Microorganisms drive many aspects of organic carbon cycling in thawing permafrost soils, but the compositional trajectory of the post-thaw microbiome and its metabolic activity remain uncertain, which limits our ability to predict permafrost–climate feedbacks in a warming world. Using quantitative metabarcoding and metagenomic sequencing, we determined relative and absolute changes in microbiome composition and functional gene abundance during thaw incubations of wet sedge tundra collected from northern Alaska, USA. Organic soils from the tundra active-layer (0–50 cm), transition-zone (50–70 cm), and permafrost (70+ cm) depths were incubated under reducing conditions at 4 °C for 30 days to mimic an extended thaw duration. Following extended thaw, we found that iron (Fe)-cycling Gammaproteobacteria, specifically the heterotrophic Fe(III)-reducing Rhodoferax sp. and chemoautotrophic Fe(II)-oxidizing Gallionella sp., increased by 3–5 orders of magnitude in absolute abundance within the transition-zone and permafrost microbiomes, accounting for 65% of community abundance. We also found that the abundance of genes for Fe(III) reduction (e.g., MtrE) and Fe(II) oxidation (e.g., Cyc1) increased concurrently with genes for benzoate degradation and pyruvate metabolism, in which pyruvate is used to generate acetate that can be oxidized, along with benzoate, to CO(2) when coupled with Fe(III) reduction. Gene abundance for CH(4) metabolism decreased following extended thaw, suggesting dissimilatory Fe(III) reduction suppresses acetoclastic methanogenesis under reducing conditions. Our genomic evidence indicates that microbial carbon degradation is dominated by iron redox metabolism via an increase in gene abundance associated with Fe(III) reduction and Fe(II) oxidation during initial permafrost thaw, likely increasing microbial respiration while suppressing methanogenesis in wet sedge tundra. |
format | Online Article Text |
id | pubmed-10667234 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | Nature Publishing Group UK |
record_format | MEDLINE/PubMed |
spelling | pubmed-106672342023-11-23 Genomic evidence that microbial carbon degradation is dominated by iron redox metabolism in thawing permafrost Romanowicz, Karl J. Crump, Byron C. Kling, George W. ISME Commun Article Microorganisms drive many aspects of organic carbon cycling in thawing permafrost soils, but the compositional trajectory of the post-thaw microbiome and its metabolic activity remain uncertain, which limits our ability to predict permafrost–climate feedbacks in a warming world. Using quantitative metabarcoding and metagenomic sequencing, we determined relative and absolute changes in microbiome composition and functional gene abundance during thaw incubations of wet sedge tundra collected from northern Alaska, USA. Organic soils from the tundra active-layer (0–50 cm), transition-zone (50–70 cm), and permafrost (70+ cm) depths were incubated under reducing conditions at 4 °C for 30 days to mimic an extended thaw duration. Following extended thaw, we found that iron (Fe)-cycling Gammaproteobacteria, specifically the heterotrophic Fe(III)-reducing Rhodoferax sp. and chemoautotrophic Fe(II)-oxidizing Gallionella sp., increased by 3–5 orders of magnitude in absolute abundance within the transition-zone and permafrost microbiomes, accounting for 65% of community abundance. We also found that the abundance of genes for Fe(III) reduction (e.g., MtrE) and Fe(II) oxidation (e.g., Cyc1) increased concurrently with genes for benzoate degradation and pyruvate metabolism, in which pyruvate is used to generate acetate that can be oxidized, along with benzoate, to CO(2) when coupled with Fe(III) reduction. Gene abundance for CH(4) metabolism decreased following extended thaw, suggesting dissimilatory Fe(III) reduction suppresses acetoclastic methanogenesis under reducing conditions. Our genomic evidence indicates that microbial carbon degradation is dominated by iron redox metabolism via an increase in gene abundance associated with Fe(III) reduction and Fe(II) oxidation during initial permafrost thaw, likely increasing microbial respiration while suppressing methanogenesis in wet sedge tundra. Nature Publishing Group UK 2023-11-23 /pmc/articles/PMC10667234/ /pubmed/37996661 http://dx.doi.org/10.1038/s43705-023-00326-5 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . |
spellingShingle | Article Romanowicz, Karl J. Crump, Byron C. Kling, George W. Genomic evidence that microbial carbon degradation is dominated by iron redox metabolism in thawing permafrost |
title | Genomic evidence that microbial carbon degradation is dominated by iron redox metabolism in thawing permafrost |
title_full | Genomic evidence that microbial carbon degradation is dominated by iron redox metabolism in thawing permafrost |
title_fullStr | Genomic evidence that microbial carbon degradation is dominated by iron redox metabolism in thawing permafrost |
title_full_unstemmed | Genomic evidence that microbial carbon degradation is dominated by iron redox metabolism in thawing permafrost |
title_short | Genomic evidence that microbial carbon degradation is dominated by iron redox metabolism in thawing permafrost |
title_sort | genomic evidence that microbial carbon degradation is dominated by iron redox metabolism in thawing permafrost |
topic | Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10667234/ https://www.ncbi.nlm.nih.gov/pubmed/37996661 http://dx.doi.org/10.1038/s43705-023-00326-5 |
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