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Glucocorticoids coordinate changes in gut microbiome composition in wild North American red squirrels

The gut microbiome impacts host health and fitness, in part through the diversification of gut metabolic function and pathogen protection. Elevations in glucocorticoids (GCs) appear to reduce gut microbiome diversity in experimental studies, suggesting that a loss of microbial diversity may be a neg...

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Autores principales: Petrullo, Lauren, Ren, Tiantian, Wu, Martin, Boonstra, Rudy, Palme, Rupert, Boutin, Stan, McAdam, Andrew G., Dantzer, Ben
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8850573/
https://www.ncbi.nlm.nih.gov/pubmed/35173201
http://dx.doi.org/10.1038/s41598-022-06359-5
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author Petrullo, Lauren
Ren, Tiantian
Wu, Martin
Boonstra, Rudy
Palme, Rupert
Boutin, Stan
McAdam, Andrew G.
Dantzer, Ben
author_facet Petrullo, Lauren
Ren, Tiantian
Wu, Martin
Boonstra, Rudy
Palme, Rupert
Boutin, Stan
McAdam, Andrew G.
Dantzer, Ben
author_sort Petrullo, Lauren
collection PubMed
description The gut microbiome impacts host health and fitness, in part through the diversification of gut metabolic function and pathogen protection. Elevations in glucocorticoids (GCs) appear to reduce gut microbiome diversity in experimental studies, suggesting that a loss of microbial diversity may be a negative consequence of increased GCs. However, given that ecological factors like food availability and population density may independently influence both GCs and microbial diversity, understanding how these factors structure the GC-microbiome relationship is crucial to interpreting its significance in wild populations. Here, we used an ecological framework to investigate the relationship between GCs and gut microbiome diversity in wild North American red squirrels (Tamiasciurus hudsonicus). As expected, higher GCs predicted lower gut microbiome diversity and an increase in metabolic taxa. Surprisingly, but in line with prior empirical studies on wild animals, gastrointestinal pathogens decreased as GCs increased. Both dietary heterogeneity and an upcoming food pulse exhibited direct effects on gut microbiome diversity, whereas conspecific density and reproductive activity impacted diversity indirectly via changes in host GCs. Our results provide evidence of a gut–brain axis in wild red squirrels and highlight the importance of situating the GC-gut microbiome relationship within an ecological framework.
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spelling pubmed-88505732022-02-17 Glucocorticoids coordinate changes in gut microbiome composition in wild North American red squirrels Petrullo, Lauren Ren, Tiantian Wu, Martin Boonstra, Rudy Palme, Rupert Boutin, Stan McAdam, Andrew G. Dantzer, Ben Sci Rep Article The gut microbiome impacts host health and fitness, in part through the diversification of gut metabolic function and pathogen protection. Elevations in glucocorticoids (GCs) appear to reduce gut microbiome diversity in experimental studies, suggesting that a loss of microbial diversity may be a negative consequence of increased GCs. However, given that ecological factors like food availability and population density may independently influence both GCs and microbial diversity, understanding how these factors structure the GC-microbiome relationship is crucial to interpreting its significance in wild populations. Here, we used an ecological framework to investigate the relationship between GCs and gut microbiome diversity in wild North American red squirrels (Tamiasciurus hudsonicus). As expected, higher GCs predicted lower gut microbiome diversity and an increase in metabolic taxa. Surprisingly, but in line with prior empirical studies on wild animals, gastrointestinal pathogens decreased as GCs increased. Both dietary heterogeneity and an upcoming food pulse exhibited direct effects on gut microbiome diversity, whereas conspecific density and reproductive activity impacted diversity indirectly via changes in host GCs. Our results provide evidence of a gut–brain axis in wild red squirrels and highlight the importance of situating the GC-gut microbiome relationship within an ecological framework. Nature Publishing Group UK 2022-02-16 /pmc/articles/PMC8850573/ /pubmed/35173201 http://dx.doi.org/10.1038/s41598-022-06359-5 Text en © This is a U.S. Government work and not under copyright protection in the US; foreign copyright protection may apply 2022 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 licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence 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 licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Petrullo, Lauren
Ren, Tiantian
Wu, Martin
Boonstra, Rudy
Palme, Rupert
Boutin, Stan
McAdam, Andrew G.
Dantzer, Ben
Glucocorticoids coordinate changes in gut microbiome composition in wild North American red squirrels
title Glucocorticoids coordinate changes in gut microbiome composition in wild North American red squirrels
title_full Glucocorticoids coordinate changes in gut microbiome composition in wild North American red squirrels
title_fullStr Glucocorticoids coordinate changes in gut microbiome composition in wild North American red squirrels
title_full_unstemmed Glucocorticoids coordinate changes in gut microbiome composition in wild North American red squirrels
title_short Glucocorticoids coordinate changes in gut microbiome composition in wild North American red squirrels
title_sort glucocorticoids coordinate changes in gut microbiome composition in wild north american red squirrels
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8850573/
https://www.ncbi.nlm.nih.gov/pubmed/35173201
http://dx.doi.org/10.1038/s41598-022-06359-5
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