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Non‐native hosts of an invasive seaweed holobiont have more stable microbial communities compared to native hosts in response to thermal stress

Seaweeds are colonized by a microbial community, which can be directly linked to their performance. This community is shaped by an interplay of stochastic and deterministic processes, including mechanisms which the holobiont host deploys to manipulate its associated microbiota. The Anna Karenina pri...

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Autores principales: Bonthond, Guido, Neu, Anna‐Katrin, Bayer, Till, Krueger‐Hadfield, Stacy A., Künzel, Sven, Weinberger, Florian
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9873590/
https://www.ncbi.nlm.nih.gov/pubmed/36713485
http://dx.doi.org/10.1002/ece3.9753
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author Bonthond, Guido
Neu, Anna‐Katrin
Bayer, Till
Krueger‐Hadfield, Stacy A.
Künzel, Sven
Weinberger, Florian
author_facet Bonthond, Guido
Neu, Anna‐Katrin
Bayer, Till
Krueger‐Hadfield, Stacy A.
Künzel, Sven
Weinberger, Florian
author_sort Bonthond, Guido
collection PubMed
description Seaweeds are colonized by a microbial community, which can be directly linked to their performance. This community is shaped by an interplay of stochastic and deterministic processes, including mechanisms which the holobiont host deploys to manipulate its associated microbiota. The Anna Karenina principle predicts that when a holobiont is exposed to suboptimal or stressful conditions, these host mechanisms may be compromised. This leads to a relative increase of stochastic processes that may potentially result in the succession of a microbial community harmful to the host. Based on this principle, we used the variability in microbial communities (i.e., beta diversity) as a proxy for stability within the invasive holobiont Gracilaria vermiculophylla during a simulated invasion in a common garden experiment. Independent of host range, host performance declined at elevated temperature (22°C) and disease incidence and beta diversity increased. Under thermally stressful conditions, beta diversity increased more in epibiota from native populations, suggesting that epibiota from non‐native holobionts are thermally more stable. This pattern reflects an increase in deterministic processes acting on epibiota associated with non‐native hosts, which in the setting of a common garden can be assumed to originate from the host itself. Therefore, these experimental data suggest that the invasion process may have selected for hosts better able to maintain stable microbiota during stress. Future studies are needed to identify the underlying host mechanisms.
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spelling pubmed-98735902023-01-27 Non‐native hosts of an invasive seaweed holobiont have more stable microbial communities compared to native hosts in response to thermal stress Bonthond, Guido Neu, Anna‐Katrin Bayer, Till Krueger‐Hadfield, Stacy A. Künzel, Sven Weinberger, Florian Ecol Evol Research Articles Seaweeds are colonized by a microbial community, which can be directly linked to their performance. This community is shaped by an interplay of stochastic and deterministic processes, including mechanisms which the holobiont host deploys to manipulate its associated microbiota. The Anna Karenina principle predicts that when a holobiont is exposed to suboptimal or stressful conditions, these host mechanisms may be compromised. This leads to a relative increase of stochastic processes that may potentially result in the succession of a microbial community harmful to the host. Based on this principle, we used the variability in microbial communities (i.e., beta diversity) as a proxy for stability within the invasive holobiont Gracilaria vermiculophylla during a simulated invasion in a common garden experiment. Independent of host range, host performance declined at elevated temperature (22°C) and disease incidence and beta diversity increased. Under thermally stressful conditions, beta diversity increased more in epibiota from native populations, suggesting that epibiota from non‐native holobionts are thermally more stable. This pattern reflects an increase in deterministic processes acting on epibiota associated with non‐native hosts, which in the setting of a common garden can be assumed to originate from the host itself. Therefore, these experimental data suggest that the invasion process may have selected for hosts better able to maintain stable microbiota during stress. Future studies are needed to identify the underlying host mechanisms. John Wiley and Sons Inc. 2023-01-24 /pmc/articles/PMC9873590/ /pubmed/36713485 http://dx.doi.org/10.1002/ece3.9753 Text en © 2023 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd. 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 Research Articles
Bonthond, Guido
Neu, Anna‐Katrin
Bayer, Till
Krueger‐Hadfield, Stacy A.
Künzel, Sven
Weinberger, Florian
Non‐native hosts of an invasive seaweed holobiont have more stable microbial communities compared to native hosts in response to thermal stress
title Non‐native hosts of an invasive seaweed holobiont have more stable microbial communities compared to native hosts in response to thermal stress
title_full Non‐native hosts of an invasive seaweed holobiont have more stable microbial communities compared to native hosts in response to thermal stress
title_fullStr Non‐native hosts of an invasive seaweed holobiont have more stable microbial communities compared to native hosts in response to thermal stress
title_full_unstemmed Non‐native hosts of an invasive seaweed holobiont have more stable microbial communities compared to native hosts in response to thermal stress
title_short Non‐native hosts of an invasive seaweed holobiont have more stable microbial communities compared to native hosts in response to thermal stress
title_sort non‐native hosts of an invasive seaweed holobiont have more stable microbial communities compared to native hosts in response to thermal stress
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9873590/
https://www.ncbi.nlm.nih.gov/pubmed/36713485
http://dx.doi.org/10.1002/ece3.9753
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