Carbon and nitrogen cycling in Yedoma permafrost controlled by microbial functional limitations

International audience Warming-induced microbial decomposition of organic matter in permafrost soils constitutes a climate-change feedback of uncertain magnitude. While physicochemical constraints on soil functioning are relatively well understood, the constraints attributable to microbial community...

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Published in:Nature Geoscience
Main Authors: Monteux, Sylvain, Keuper, Frida, Fontaine, Sébastien, Gavazov, Konstantin, Hallin, Sara, Juhanson, Jaanis, Krab, Eveline, Revaillot, Sandrine, Verbruggen, Erik, Walz, Josefine, Weedon, James, Dorrepaal, Ellen
Other Authors: Swedish University of Agricultural Sciences = Sveriges lantbruksuniversitet (SLU), Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), BioEcoAgro - Equipe 2 - Integrated functioning of the soil-plant system and exchanges between the ecosystem and the hydrosphere and the atmosphere, BioEcoAgro - UMR transfrontalière INRAe - UMRT1158, Université d'Artois (UA)-Université de Liège-Université de Picardie Jules Verne (UPJV)-Université du Littoral Côte d'Opale (ULCO)-Université de Lille-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-JUNIA (JUNIA), Université catholique de Lille (UCL)-Université catholique de Lille (UCL)-Université d'Artois (UA)-Université de Liège-Université de Picardie Jules Verne (UPJV)-Université du Littoral Côte d'Opale (ULCO)-Université de Lille-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-JUNIA (JUNIA), Université catholique de Lille (UCL)-Université catholique de Lille (UCL), Unité Mixte de Recherche sur l'Ecosystème Prairial - UMR (UREP), VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Swiss Federal Institute for Forest, Snow and Landscape Research WSL, Universiteit Antwerpen = University of Antwerpen Antwerpen, Vrije Universiteit Amsterdam Amsterdam (VU)
Format: Article in Journal/Newspaper
Language:English
Published: HAL CCSD 2020
Subjects:
Online Access:https://hal.inrae.fr/hal-03121697
https://doi.org/10.1038/s41561-020-00662-4
id ftunivclille:oai:HAL:hal-03121697v1
record_format openpolar
institution Open Polar
collection HAL de l'Université Catholique de Lille
op_collection_id ftunivclille
language English
topic soil organic-matter
thawing permafrost
fatty-acids
r package
communities
biomass
temperature
sensitivity
diversity
reveals
[SDE.MCG]Environmental Sciences/Global Changes
spellingShingle soil organic-matter
thawing permafrost
fatty-acids
r package
communities
biomass
temperature
sensitivity
diversity
reveals
[SDE.MCG]Environmental Sciences/Global Changes
Monteux, Sylvain
Keuper, Frida
Fontaine, Sébastien
Gavazov, Konstantin
Hallin, Sara
Juhanson, Jaanis
Krab, Eveline
Revaillot, Sandrine
Verbruggen, Erik
Walz, Josefine
Weedon, James
Dorrepaal, Ellen
Carbon and nitrogen cycling in Yedoma permafrost controlled by microbial functional limitations
topic_facet soil organic-matter
thawing permafrost
fatty-acids
r package
communities
biomass
temperature
sensitivity
diversity
reveals
[SDE.MCG]Environmental Sciences/Global Changes
description International audience Warming-induced microbial decomposition of organic matter in permafrost soils constitutes a climate-change feedback of uncertain magnitude. While physicochemical constraints on soil functioning are relatively well understood, the constraints attributable to microbial community composition remain unclear. Here we show that biogeochemical processes in permafrost can be impaired by missing functions in the microbial community-functional limitations-probably due to environmental filtering of the microbial community over millennia-long freezing. We inoculated Yedoma permafrost with a functionally diverse exogenous microbial community to test this mechanism by introducing potentially missing microbial functions. This initiated nitrification activity and increased CO2 production by 38% over 161 days. The changes in soil functioning were strongly associated with an altered microbial community composition, rather than with changes in soil chemistry or microbial biomass. The present permafrost microbial community composition thus constrains carbon and nitrogen biogeochemical processes, but microbial colonization, likely to occur upon permafrost thaw in situ, can alleviate such functional limitations. Accounting for functional limitations and their alleviation could strongly increase our estimate of the vulnerability of permafrost soil organic matter to decomposition and the resulting global climate feedback.
author2 Swedish University of Agricultural Sciences = Sveriges lantbruksuniversitet (SLU)
Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)
BioEcoAgro - Equipe 2 - Integrated functioning of the soil-plant system and exchanges between the ecosystem and the hydrosphere and the atmosphere
BioEcoAgro - UMR transfrontalière INRAe - UMRT1158
Université d'Artois (UA)-Université de Liège-Université de Picardie Jules Verne (UPJV)-Université du Littoral Côte d'Opale (ULCO)-Université de Lille-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-JUNIA (JUNIA)
Université catholique de Lille (UCL)-Université catholique de Lille (UCL)-Université d'Artois (UA)-Université de Liège-Université de Picardie Jules Verne (UPJV)-Université du Littoral Côte d'Opale (ULCO)-Université de Lille-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-JUNIA (JUNIA)
Université catholique de Lille (UCL)-Université catholique de Lille (UCL)
Unité Mixte de Recherche sur l'Ecosystème Prairial - UMR (UREP)
VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)
Swiss Federal Institute for Forest, Snow and Landscape Research WSL
Universiteit Antwerpen = University of Antwerpen Antwerpen
Vrije Universiteit Amsterdam Amsterdam (VU)
format Article in Journal/Newspaper
author Monteux, Sylvain
Keuper, Frida
Fontaine, Sébastien
Gavazov, Konstantin
Hallin, Sara
Juhanson, Jaanis
Krab, Eveline
Revaillot, Sandrine
Verbruggen, Erik
Walz, Josefine
Weedon, James
Dorrepaal, Ellen
author_facet Monteux, Sylvain
Keuper, Frida
Fontaine, Sébastien
Gavazov, Konstantin
Hallin, Sara
Juhanson, Jaanis
Krab, Eveline
Revaillot, Sandrine
Verbruggen, Erik
Walz, Josefine
Weedon, James
Dorrepaal, Ellen
author_sort Monteux, Sylvain
title Carbon and nitrogen cycling in Yedoma permafrost controlled by microbial functional limitations
title_short Carbon and nitrogen cycling in Yedoma permafrost controlled by microbial functional limitations
title_full Carbon and nitrogen cycling in Yedoma permafrost controlled by microbial functional limitations
title_fullStr Carbon and nitrogen cycling in Yedoma permafrost controlled by microbial functional limitations
title_full_unstemmed Carbon and nitrogen cycling in Yedoma permafrost controlled by microbial functional limitations
title_sort carbon and nitrogen cycling in yedoma permafrost controlled by microbial functional limitations
publisher HAL CCSD
publishDate 2020
url https://hal.inrae.fr/hal-03121697
https://doi.org/10.1038/s41561-020-00662-4
genre permafrost
genre_facet permafrost
op_source ISSN: 1752-0894
Nature Geoscience
https://hal.inrae.fr/hal-03121697
Nature Geoscience, 2020, 13 (12), pp.794-798. ⟨10.1038/s41561-020-00662-4⟩
op_relation info:eu-repo/semantics/altIdentifier/doi/10.1038/s41561-020-00662-4
hal-03121697
https://hal.inrae.fr/hal-03121697
doi:10.1038/s41561-020-00662-4
WOS: 000594838900006
op_doi https://doi.org/10.1038/s41561-020-00662-4
container_title Nature Geoscience
container_volume 13
container_issue 12
container_start_page 794
op_container_end_page 798
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spelling ftunivclille:oai:HAL:hal-03121697v1 2024-06-23T07:56:02+00:00 Carbon and nitrogen cycling in Yedoma permafrost controlled by microbial functional limitations Monteux, Sylvain Keuper, Frida Fontaine, Sébastien Gavazov, Konstantin Hallin, Sara Juhanson, Jaanis Krab, Eveline Revaillot, Sandrine Verbruggen, Erik Walz, Josefine Weedon, James Dorrepaal, Ellen Swedish University of Agricultural Sciences = Sveriges lantbruksuniversitet (SLU) Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE) BioEcoAgro - Equipe 2 - Integrated functioning of the soil-plant system and exchanges between the ecosystem and the hydrosphere and the atmosphere BioEcoAgro - UMR transfrontalière INRAe - UMRT1158 Université d'Artois (UA)-Université de Liège-Université de Picardie Jules Verne (UPJV)-Université du Littoral Côte d'Opale (ULCO)-Université de Lille-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-JUNIA (JUNIA) Université catholique de Lille (UCL)-Université catholique de Lille (UCL)-Université d'Artois (UA)-Université de Liège-Université de Picardie Jules Verne (UPJV)-Université du Littoral Côte d'Opale (ULCO)-Université de Lille-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-JUNIA (JUNIA) Université catholique de Lille (UCL)-Université catholique de Lille (UCL) Unité Mixte de Recherche sur l'Ecosystème Prairial - UMR (UREP) VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE) Swiss Federal Institute for Forest, Snow and Landscape Research WSL Universiteit Antwerpen = University of Antwerpen Antwerpen Vrije Universiteit Amsterdam Amsterdam (VU) 2020-12 https://hal.inrae.fr/hal-03121697 https://doi.org/10.1038/s41561-020-00662-4 en eng HAL CCSD Nature Publishing Group info:eu-repo/semantics/altIdentifier/doi/10.1038/s41561-020-00662-4 hal-03121697 https://hal.inrae.fr/hal-03121697 doi:10.1038/s41561-020-00662-4 WOS: 000594838900006 ISSN: 1752-0894 Nature Geoscience https://hal.inrae.fr/hal-03121697 Nature Geoscience, 2020, 13 (12), pp.794-798. ⟨10.1038/s41561-020-00662-4⟩ soil organic-matter thawing permafrost fatty-acids r package communities biomass temperature sensitivity diversity reveals [SDE.MCG]Environmental Sciences/Global Changes info:eu-repo/semantics/article Journal articles 2020 ftunivclille https://doi.org/10.1038/s41561-020-00662-4 2024-06-05T23:33:53Z International audience Warming-induced microbial decomposition of organic matter in permafrost soils constitutes a climate-change feedback of uncertain magnitude. While physicochemical constraints on soil functioning are relatively well understood, the constraints attributable to microbial community composition remain unclear. Here we show that biogeochemical processes in permafrost can be impaired by missing functions in the microbial community-functional limitations-probably due to environmental filtering of the microbial community over millennia-long freezing. We inoculated Yedoma permafrost with a functionally diverse exogenous microbial community to test this mechanism by introducing potentially missing microbial functions. This initiated nitrification activity and increased CO2 production by 38% over 161 days. The changes in soil functioning were strongly associated with an altered microbial community composition, rather than with changes in soil chemistry or microbial biomass. The present permafrost microbial community composition thus constrains carbon and nitrogen biogeochemical processes, but microbial colonization, likely to occur upon permafrost thaw in situ, can alleviate such functional limitations. Accounting for functional limitations and their alleviation could strongly increase our estimate of the vulnerability of permafrost soil organic matter to decomposition and the resulting global climate feedback. Article in Journal/Newspaper permafrost HAL de l'Université Catholique de Lille Nature Geoscience 13 12 794 798