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The role of host promiscuity in the invasion process of a seaweed holobiont

Invasive species are co-introduced with microbiota from their native range and also interact with microbiota found in the novel environment to which they are introduced. Host flexibility toward microbiota, or host promiscuity, is an important trait underlying terrestrial plant invasions. To test whe...

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Autores principales: Bonthond, Guido, Bayer, Till, Krueger-Hadfield, Stacy A., Stärck, Nadja, Wang, Gaoge, Nakaoka, Masahiro, Künzel, Sven, Weinberger, Florian
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8163768/
https://www.ncbi.nlm.nih.gov/pubmed/33479490
http://dx.doi.org/10.1038/s41396-020-00878-7
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author Bonthond, Guido
Bayer, Till
Krueger-Hadfield, Stacy A.
Stärck, Nadja
Wang, Gaoge
Nakaoka, Masahiro
Künzel, Sven
Weinberger, Florian
author_facet Bonthond, Guido
Bayer, Till
Krueger-Hadfield, Stacy A.
Stärck, Nadja
Wang, Gaoge
Nakaoka, Masahiro
Künzel, Sven
Weinberger, Florian
author_sort Bonthond, Guido
collection PubMed
description Invasive species are co-introduced with microbiota from their native range and also interact with microbiota found in the novel environment to which they are introduced. Host flexibility toward microbiota, or host promiscuity, is an important trait underlying terrestrial plant invasions. To test whether host promiscuity may be important in macroalgal invasions, we experimentally simulated an invasion in a common garden setting, using the widespread invasive macroalga Agarophyton vermiculophyllum as a model invasive seaweed holobiont. After disturbing the microbiota of individuals from native and non-native populations with antibiotics, we monitored the microbial succession trajectories in the presence of a new source of microbes. Microbial communities were strongly impacted by the treatment and changed compositionally and in terms of diversity but recovered functionally by the end of the experiment in most respects. Beta-diversity in disturbed holobionts strongly decreased, indicating that different populations configure more similar –or more common– microbial communities when exposed to the same conditions. This decline in beta-diversity occurred not only more rapidly, but was also more pronounced in non-native populations, while individuals from native populations retained communities more similar to those observed in the field. This study demonstrates that microbial communities of non-native A. vermiculophyllum are more flexibly adjusted to the environment and suggests that an intraspecific increase in host promiscuity has promoted the invasion process of A. vermiculophyllum. This phenomenon may be important among invasive macroalgal holobionts in general.
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spelling pubmed-81637682021-06-10 The role of host promiscuity in the invasion process of a seaweed holobiont Bonthond, Guido Bayer, Till Krueger-Hadfield, Stacy A. Stärck, Nadja Wang, Gaoge Nakaoka, Masahiro Künzel, Sven Weinberger, Florian ISME J Article Invasive species are co-introduced with microbiota from their native range and also interact with microbiota found in the novel environment to which they are introduced. Host flexibility toward microbiota, or host promiscuity, is an important trait underlying terrestrial plant invasions. To test whether host promiscuity may be important in macroalgal invasions, we experimentally simulated an invasion in a common garden setting, using the widespread invasive macroalga Agarophyton vermiculophyllum as a model invasive seaweed holobiont. After disturbing the microbiota of individuals from native and non-native populations with antibiotics, we monitored the microbial succession trajectories in the presence of a new source of microbes. Microbial communities were strongly impacted by the treatment and changed compositionally and in terms of diversity but recovered functionally by the end of the experiment in most respects. Beta-diversity in disturbed holobionts strongly decreased, indicating that different populations configure more similar –or more common– microbial communities when exposed to the same conditions. This decline in beta-diversity occurred not only more rapidly, but was also more pronounced in non-native populations, while individuals from native populations retained communities more similar to those observed in the field. This study demonstrates that microbial communities of non-native A. vermiculophyllum are more flexibly adjusted to the environment and suggests that an intraspecific increase in host promiscuity has promoted the invasion process of A. vermiculophyllum. This phenomenon may be important among invasive macroalgal holobionts in general. Nature Publishing Group UK 2021-01-21 2021-06 /pmc/articles/PMC8163768/ /pubmed/33479490 http://dx.doi.org/10.1038/s41396-020-00878-7 Text en © The Author(s) 2021 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 license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license 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 license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Bonthond, Guido
Bayer, Till
Krueger-Hadfield, Stacy A.
Stärck, Nadja
Wang, Gaoge
Nakaoka, Masahiro
Künzel, Sven
Weinberger, Florian
The role of host promiscuity in the invasion process of a seaweed holobiont
title The role of host promiscuity in the invasion process of a seaweed holobiont
title_full The role of host promiscuity in the invasion process of a seaweed holobiont
title_fullStr The role of host promiscuity in the invasion process of a seaweed holobiont
title_full_unstemmed The role of host promiscuity in the invasion process of a seaweed holobiont
title_short The role of host promiscuity in the invasion process of a seaweed holobiont
title_sort role of host promiscuity in the invasion process of a seaweed holobiont
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8163768/
https://www.ncbi.nlm.nih.gov/pubmed/33479490
http://dx.doi.org/10.1038/s41396-020-00878-7
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