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Genotype–environment interactions determine microbiota plasticity in the sea anemone Nematostella vectensis

Most multicellular organisms harbor microbial colonizers that provide various benefits to their hosts. Although these microbial communities may be host species- or even genotype-specific, the associated bacterial communities can respond plastically to environmental changes. In this study, we estimat...

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Autores principales: Baldassarre, Laura, Reitzel, Adam M., Fraune, Sebastian
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9894556/
https://www.ncbi.nlm.nih.gov/pubmed/36689558
http://dx.doi.org/10.1371/journal.pbio.3001726
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author Baldassarre, Laura
Reitzel, Adam M.
Fraune, Sebastian
author_facet Baldassarre, Laura
Reitzel, Adam M.
Fraune, Sebastian
author_sort Baldassarre, Laura
collection PubMed
description Most multicellular organisms harbor microbial colonizers that provide various benefits to their hosts. Although these microbial communities may be host species- or even genotype-specific, the associated bacterial communities can respond plastically to environmental changes. In this study, we estimated the relative contribution of environment and host genotype to bacterial community composition in Nematostella vectensis, an estuarine cnidarian. We sampled N. vectensis polyps from 5 different populations along a north–south gradient on the Atlantic coast of the United States and Canada. In addition, we sampled 3 populations at 3 different times of the year. While half of the polyps were immediately analyzed for their bacterial composition by 16S rRNA gene sequencing, the remaining polyps were cultured under laboratory conditions for 1 month. Bacterial community comparison analyses revealed that laboratory maintenance reduced bacterial diversity by 4-fold, but maintained a population-specific bacterial colonization. Interestingly, the differences between bacterial communities correlated strongly with seasonal variations, especially with ambient water temperature. To decipher the contribution of both ambient temperature and host genotype to bacterial colonization, we generated 12 clonal lines from 6 different populations in order to maintain each genotype at 3 different temperatures for 3 months. The bacterial community composition of the same N. vectensis clone differed greatly between the 3 different temperatures, highlighting the contribution of ambient temperature to bacterial community composition. To a lesser extent, bacterial community composition varied between different genotypes under identical conditions, indicating the influence of host genotype. In addition, we identified a significant genotype x environment interaction determining microbiota plasticity in N. vectensis. From our results we can conclude that N. vectensis-associated bacterial communities respond plastically to changes in ambient temperature, with the association of different bacterial taxa depending in part on the host genotype. Future research will reveal how this genotype-specific microbiota plasticity affects the ability to cope with changing environmental conditions.
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spelling pubmed-98945562023-02-03 Genotype–environment interactions determine microbiota plasticity in the sea anemone Nematostella vectensis Baldassarre, Laura Reitzel, Adam M. Fraune, Sebastian PLoS Biol Research Article Most multicellular organisms harbor microbial colonizers that provide various benefits to their hosts. Although these microbial communities may be host species- or even genotype-specific, the associated bacterial communities can respond plastically to environmental changes. In this study, we estimated the relative contribution of environment and host genotype to bacterial community composition in Nematostella vectensis, an estuarine cnidarian. We sampled N. vectensis polyps from 5 different populations along a north–south gradient on the Atlantic coast of the United States and Canada. In addition, we sampled 3 populations at 3 different times of the year. While half of the polyps were immediately analyzed for their bacterial composition by 16S rRNA gene sequencing, the remaining polyps were cultured under laboratory conditions for 1 month. Bacterial community comparison analyses revealed that laboratory maintenance reduced bacterial diversity by 4-fold, but maintained a population-specific bacterial colonization. Interestingly, the differences between bacterial communities correlated strongly with seasonal variations, especially with ambient water temperature. To decipher the contribution of both ambient temperature and host genotype to bacterial colonization, we generated 12 clonal lines from 6 different populations in order to maintain each genotype at 3 different temperatures for 3 months. The bacterial community composition of the same N. vectensis clone differed greatly between the 3 different temperatures, highlighting the contribution of ambient temperature to bacterial community composition. To a lesser extent, bacterial community composition varied between different genotypes under identical conditions, indicating the influence of host genotype. In addition, we identified a significant genotype x environment interaction determining microbiota plasticity in N. vectensis. From our results we can conclude that N. vectensis-associated bacterial communities respond plastically to changes in ambient temperature, with the association of different bacterial taxa depending in part on the host genotype. Future research will reveal how this genotype-specific microbiota plasticity affects the ability to cope with changing environmental conditions. Public Library of Science 2023-01-23 /pmc/articles/PMC9894556/ /pubmed/36689558 http://dx.doi.org/10.1371/journal.pbio.3001726 Text en https://creativecommons.org/publicdomain/zero/1.0/This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 (https://creativecommons.org/publicdomain/zero/1.0/) public domain dedication.
spellingShingle Research Article
Baldassarre, Laura
Reitzel, Adam M.
Fraune, Sebastian
Genotype–environment interactions determine microbiota plasticity in the sea anemone Nematostella vectensis
title Genotype–environment interactions determine microbiota plasticity in the sea anemone Nematostella vectensis
title_full Genotype–environment interactions determine microbiota plasticity in the sea anemone Nematostella vectensis
title_fullStr Genotype–environment interactions determine microbiota plasticity in the sea anemone Nematostella vectensis
title_full_unstemmed Genotype–environment interactions determine microbiota plasticity in the sea anemone Nematostella vectensis
title_short Genotype–environment interactions determine microbiota plasticity in the sea anemone Nematostella vectensis
title_sort genotype–environment interactions determine microbiota plasticity in the sea anemone nematostella vectensis
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9894556/
https://www.ncbi.nlm.nih.gov/pubmed/36689558
http://dx.doi.org/10.1371/journal.pbio.3001726
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