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Microbiome assembly in thawing permafrost and its feedbacks to climate

The physical and chemical changes that accompany permafrost thaw directly influence the microbial communities that mediate the decomposition of formerly frozen organic matter, leading to uncertainty in permafrost–climate feedbacks. Although changes to microbial metabolism and community structure are...

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Autores principales: Ernakovich, Jessica G., Barbato, Robyn A., Rich, Virginia I., Schädel, Christina, Hewitt, Rebecca E., Doherty, Stacey J., Whalen, Emily D., Abbott, Benjamin W., Barta, Jiri, Biasi, Christina, Chabot, Chris L., Hultman, Jenni, Knoblauch, Christian, Vetter, Maggie C. Y. Lau, Leewis, Mary‐Cathrine, Liebner, Susanne, Mackelprang, Rachel, Onstott, Tullis C., Richter, Andreas, Schütte, Ursel M. E., Siljanen, Henri M. P., Taş, Neslihan, Timling, Ina, Vishnivetskaya, Tatiana A., Waldrop, Mark P., Winkel, Matthias
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9541943/
https://www.ncbi.nlm.nih.gov/pubmed/35722720
http://dx.doi.org/10.1111/gcb.16231
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author Ernakovich, Jessica G.
Barbato, Robyn A.
Rich, Virginia I.
Schädel, Christina
Hewitt, Rebecca E.
Doherty, Stacey J.
Whalen, Emily D.
Abbott, Benjamin W.
Barta, Jiri
Biasi, Christina
Chabot, Chris L.
Hultman, Jenni
Knoblauch, Christian
Vetter, Maggie C. Y. Lau
Leewis, Mary‐Cathrine
Liebner, Susanne
Mackelprang, Rachel
Onstott, Tullis C.
Richter, Andreas
Schütte, Ursel M. E.
Siljanen, Henri M. P.
Taş, Neslihan
Timling, Ina
Vishnivetskaya, Tatiana A.
Waldrop, Mark P.
Winkel, Matthias
author_facet Ernakovich, Jessica G.
Barbato, Robyn A.
Rich, Virginia I.
Schädel, Christina
Hewitt, Rebecca E.
Doherty, Stacey J.
Whalen, Emily D.
Abbott, Benjamin W.
Barta, Jiri
Biasi, Christina
Chabot, Chris L.
Hultman, Jenni
Knoblauch, Christian
Vetter, Maggie C. Y. Lau
Leewis, Mary‐Cathrine
Liebner, Susanne
Mackelprang, Rachel
Onstott, Tullis C.
Richter, Andreas
Schütte, Ursel M. E.
Siljanen, Henri M. P.
Taş, Neslihan
Timling, Ina
Vishnivetskaya, Tatiana A.
Waldrop, Mark P.
Winkel, Matthias
author_sort Ernakovich, Jessica G.
collection PubMed
description The physical and chemical changes that accompany permafrost thaw directly influence the microbial communities that mediate the decomposition of formerly frozen organic matter, leading to uncertainty in permafrost–climate feedbacks. Although changes to microbial metabolism and community structure are documented following thaw, the generality of post‐thaw assembly patterns across permafrost soils of the world remains uncertain, limiting our ability to predict biogeochemistry and microbial community responses to climate change. Based on our review of the Arctic microbiome, permafrost microbiology, and community ecology, we propose that Assembly Theory provides a framework to better understand thaw‐mediated microbiome changes and the implications for community function and climate feedbacks. This framework posits that the prevalence of deterministic or stochastic processes indicates whether the community is well‐suited to thrive in changing environmental conditions. We predict that on a short timescale and following high‐disturbance thaw (e.g., thermokarst), stochasticity dominates post‐thaw microbiome assembly, suggesting that functional predictions will be aided by detailed information about the microbiome. At a longer timescale and lower‐intensity disturbance (e.g., active layer deepening), deterministic processes likely dominate, making environmental parameters sufficient for predicting function. We propose that the contribution of stochastic and deterministic processes to post‐thaw microbiome assembly depends on the characteristics of the thaw disturbance, as well as characteristics of the microbial community, such as the ecological and phylogenetic breadth of functional guilds, their functional redundancy, and biotic interactions. These propagate across space and time, potentially providing a means for predicting the microbial forcing of greenhouse gas feedbacks to global climate change.
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spelling pubmed-95419432022-10-14 Microbiome assembly in thawing permafrost and its feedbacks to climate Ernakovich, Jessica G. Barbato, Robyn A. Rich, Virginia I. Schädel, Christina Hewitt, Rebecca E. Doherty, Stacey J. Whalen, Emily D. Abbott, Benjamin W. Barta, Jiri Biasi, Christina Chabot, Chris L. Hultman, Jenni Knoblauch, Christian Vetter, Maggie C. Y. Lau Leewis, Mary‐Cathrine Liebner, Susanne Mackelprang, Rachel Onstott, Tullis C. Richter, Andreas Schütte, Ursel M. E. Siljanen, Henri M. P. Taş, Neslihan Timling, Ina Vishnivetskaya, Tatiana A. Waldrop, Mark P. Winkel, Matthias Glob Chang Biol Opinion The physical and chemical changes that accompany permafrost thaw directly influence the microbial communities that mediate the decomposition of formerly frozen organic matter, leading to uncertainty in permafrost–climate feedbacks. Although changes to microbial metabolism and community structure are documented following thaw, the generality of post‐thaw assembly patterns across permafrost soils of the world remains uncertain, limiting our ability to predict biogeochemistry and microbial community responses to climate change. Based on our review of the Arctic microbiome, permafrost microbiology, and community ecology, we propose that Assembly Theory provides a framework to better understand thaw‐mediated microbiome changes and the implications for community function and climate feedbacks. This framework posits that the prevalence of deterministic or stochastic processes indicates whether the community is well‐suited to thrive in changing environmental conditions. We predict that on a short timescale and following high‐disturbance thaw (e.g., thermokarst), stochasticity dominates post‐thaw microbiome assembly, suggesting that functional predictions will be aided by detailed information about the microbiome. At a longer timescale and lower‐intensity disturbance (e.g., active layer deepening), deterministic processes likely dominate, making environmental parameters sufficient for predicting function. We propose that the contribution of stochastic and deterministic processes to post‐thaw microbiome assembly depends on the characteristics of the thaw disturbance, as well as characteristics of the microbial community, such as the ecological and phylogenetic breadth of functional guilds, their functional redundancy, and biotic interactions. These propagate across space and time, potentially providing a means for predicting the microbial forcing of greenhouse gas feedbacks to global climate change. John Wiley and Sons Inc. 2022-06-20 2022-09 /pmc/articles/PMC9541943/ /pubmed/35722720 http://dx.doi.org/10.1111/gcb.16231 Text en © 2022 Her Majesty the Queen in Right of Canada. Global Change Biology published by John Wiley & Sons Ltd. Reproduced with the permission of the Minister of Agriculture and Agri‐Food Canada. This article has been contributed to by U.S. Government employees and their work is in the public domain in the USA. https://creativecommons.org/licenses/by/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Opinion
Ernakovich, Jessica G.
Barbato, Robyn A.
Rich, Virginia I.
Schädel, Christina
Hewitt, Rebecca E.
Doherty, Stacey J.
Whalen, Emily D.
Abbott, Benjamin W.
Barta, Jiri
Biasi, Christina
Chabot, Chris L.
Hultman, Jenni
Knoblauch, Christian
Vetter, Maggie C. Y. Lau
Leewis, Mary‐Cathrine
Liebner, Susanne
Mackelprang, Rachel
Onstott, Tullis C.
Richter, Andreas
Schütte, Ursel M. E.
Siljanen, Henri M. P.
Taş, Neslihan
Timling, Ina
Vishnivetskaya, Tatiana A.
Waldrop, Mark P.
Winkel, Matthias
Microbiome assembly in thawing permafrost and its feedbacks to climate
title Microbiome assembly in thawing permafrost and its feedbacks to climate
title_full Microbiome assembly in thawing permafrost and its feedbacks to climate
title_fullStr Microbiome assembly in thawing permafrost and its feedbacks to climate
title_full_unstemmed Microbiome assembly in thawing permafrost and its feedbacks to climate
title_short Microbiome assembly in thawing permafrost and its feedbacks to climate
title_sort microbiome assembly in thawing permafrost and its feedbacks to climate
topic Opinion
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9541943/
https://www.ncbi.nlm.nih.gov/pubmed/35722720
http://dx.doi.org/10.1111/gcb.16231
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