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The amphibian microbiome exhibits poor resilience following pathogen-induced disturbance

Infectious pathogens can disrupt the microbiome in addition to directly affecting the host. Impacts of disease may be dependent on the ability of the microbiome to recover from such disturbance, yet remarkably little is known about microbiome recovery after disease, particularly in nonhuman animals....

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Autores principales: Jani, Andrea J., Bushell, Jessie, Arisdakessian, Cédric G., Belcaid, Mahdi, Boiano, Daniel M., Brown, Cathy, Knapp, Roland A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8163836/
https://www.ncbi.nlm.nih.gov/pubmed/33564111
http://dx.doi.org/10.1038/s41396-020-00875-w
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author Jani, Andrea J.
Bushell, Jessie
Arisdakessian, Cédric G.
Belcaid, Mahdi
Boiano, Daniel M.
Brown, Cathy
Knapp, Roland A.
author_facet Jani, Andrea J.
Bushell, Jessie
Arisdakessian, Cédric G.
Belcaid, Mahdi
Boiano, Daniel M.
Brown, Cathy
Knapp, Roland A.
author_sort Jani, Andrea J.
collection PubMed
description Infectious pathogens can disrupt the microbiome in addition to directly affecting the host. Impacts of disease may be dependent on the ability of the microbiome to recover from such disturbance, yet remarkably little is known about microbiome recovery after disease, particularly in nonhuman animals. We assessed the resilience of the amphibian skin microbial community after disturbance by the pathogen, Batrachochytrium dendrobatidis (Bd). Skin microbial communities of laboratory-reared mountain yellow-legged frogs were tracked through three experimental phases: prior to Bd infection, after Bd infection (disturbance), and after clearing Bd infection (recovery period). Bd infection disturbed microbiome composition and altered the relative abundances of several dominant bacterial taxa. After Bd infection, frogs were treated with an antifungal drug that cleared Bd infection, but this did not lead to recovery of microbiome composition (measured as Unifrac distance) or relative abundances of dominant bacterial groups. These results indicate that Bd infection can lead to an alternate stable state in the microbiome of sensitive amphibians, or that microbiome recovery is extremely slow—in either case resilience is low. Furthermore, antifungal treatment and clearance of Bd infection had the additional effect of reducing microbial community variability, which we hypothesize results from similarity across frogs in the taxa that colonize community vacancies resulting from the removal of Bd. Our results indicate that the skin microbiota of mountain yellow-legged frogs has low resilience following Bd-induced disturbance and is further altered by the process of clearing Bd infection, which may have implications for the conservation of this endangered amphibian.
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spelling pubmed-81638362021-06-10 The amphibian microbiome exhibits poor resilience following pathogen-induced disturbance Jani, Andrea J. Bushell, Jessie Arisdakessian, Cédric G. Belcaid, Mahdi Boiano, Daniel M. Brown, Cathy Knapp, Roland A. ISME J Article Infectious pathogens can disrupt the microbiome in addition to directly affecting the host. Impacts of disease may be dependent on the ability of the microbiome to recover from such disturbance, yet remarkably little is known about microbiome recovery after disease, particularly in nonhuman animals. We assessed the resilience of the amphibian skin microbial community after disturbance by the pathogen, Batrachochytrium dendrobatidis (Bd). Skin microbial communities of laboratory-reared mountain yellow-legged frogs were tracked through three experimental phases: prior to Bd infection, after Bd infection (disturbance), and after clearing Bd infection (recovery period). Bd infection disturbed microbiome composition and altered the relative abundances of several dominant bacterial taxa. After Bd infection, frogs were treated with an antifungal drug that cleared Bd infection, but this did not lead to recovery of microbiome composition (measured as Unifrac distance) or relative abundances of dominant bacterial groups. These results indicate that Bd infection can lead to an alternate stable state in the microbiome of sensitive amphibians, or that microbiome recovery is extremely slow—in either case resilience is low. Furthermore, antifungal treatment and clearance of Bd infection had the additional effect of reducing microbial community variability, which we hypothesize results from similarity across frogs in the taxa that colonize community vacancies resulting from the removal of Bd. Our results indicate that the skin microbiota of mountain yellow-legged frogs has low resilience following Bd-induced disturbance and is further altered by the process of clearing Bd infection, which may have implications for the conservation of this endangered amphibian. Nature Publishing Group UK 2021-02-09 2021-06 /pmc/articles/PMC8163836/ /pubmed/33564111 http://dx.doi.org/10.1038/s41396-020-00875-w 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
Jani, Andrea J.
Bushell, Jessie
Arisdakessian, Cédric G.
Belcaid, Mahdi
Boiano, Daniel M.
Brown, Cathy
Knapp, Roland A.
The amphibian microbiome exhibits poor resilience following pathogen-induced disturbance
title The amphibian microbiome exhibits poor resilience following pathogen-induced disturbance
title_full The amphibian microbiome exhibits poor resilience following pathogen-induced disturbance
title_fullStr The amphibian microbiome exhibits poor resilience following pathogen-induced disturbance
title_full_unstemmed The amphibian microbiome exhibits poor resilience following pathogen-induced disturbance
title_short The amphibian microbiome exhibits poor resilience following pathogen-induced disturbance
title_sort amphibian microbiome exhibits poor resilience following pathogen-induced disturbance
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8163836/
https://www.ncbi.nlm.nih.gov/pubmed/33564111
http://dx.doi.org/10.1038/s41396-020-00875-w
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