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Strong restructuration of skin microbiota during captivity challenges ex-situ conservation of amphibians

In response to the current worldwide amphibian extinction crisis, conservation instances have encouraged the establishment of ex-situ collections for endangered species. The resulting assurance populations are managed under strict biosecure protocols, often involving artificial cycles of temperature...

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Autores principales: Fieschi-Méric, Léa, Van Leeuwen, Pauline, Hopkins, Kevin, Bournonville, Marie, Denoël, Mathieu, Lesbarrères, David
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9986596/
https://www.ncbi.nlm.nih.gov/pubmed/36891392
http://dx.doi.org/10.3389/fmicb.2023.1111018
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author Fieschi-Méric, Léa
Van Leeuwen, Pauline
Hopkins, Kevin
Bournonville, Marie
Denoël, Mathieu
Lesbarrères, David
author_facet Fieschi-Méric, Léa
Van Leeuwen, Pauline
Hopkins, Kevin
Bournonville, Marie
Denoël, Mathieu
Lesbarrères, David
author_sort Fieschi-Méric, Léa
collection PubMed
description In response to the current worldwide amphibian extinction crisis, conservation instances have encouraged the establishment of ex-situ collections for endangered species. The resulting assurance populations are managed under strict biosecure protocols, often involving artificial cycles of temperature and humidity to induce active and overwintering phases, which likely affect the bacterial symbionts living on the amphibian skin. However, the skin microbiota is an important first line of defense against pathogens that can cause amphibian declines, such as the chytrid Batrachochytrium dendrobatidis (Bd). Determining whether current husbandry practices for assurance populations might deplete amphibians from their symbionts is therefore essential to conservation success. Here, we characterize the effect of the transitions from the wild to captivity, and between aquatic and overwintering phases, on the skin microbiota of two newt species. While our results confirm differential selectivity of skin microbiota between species, they underscore that captivity and phase-shifts similarly affect their community structure. More specifically, the translocation ex-situ is associated with rapid impoverishment, decrease in alpha diversity and strong species turnover of bacterial communities. Shifts between active and overwintering phases also cause changes in the diversity and composition of the microbiota, and on the prevalence of Bd-inhibitory phylotypes. Altogether, our results suggest that current husbandry practices strongly restructure the amphibian skin microbiota. Although it remains to be determined whether these changes are reversible or have deleterious effects on their hosts, we discuss methods to limit microbial diversity loss ex-situ and emphasize the importance of integrating bacterial communities to applied amphibian conservation.
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spelling pubmed-99865962023-03-07 Strong restructuration of skin microbiota during captivity challenges ex-situ conservation of amphibians Fieschi-Méric, Léa Van Leeuwen, Pauline Hopkins, Kevin Bournonville, Marie Denoël, Mathieu Lesbarrères, David Front Microbiol Microbiology In response to the current worldwide amphibian extinction crisis, conservation instances have encouraged the establishment of ex-situ collections for endangered species. The resulting assurance populations are managed under strict biosecure protocols, often involving artificial cycles of temperature and humidity to induce active and overwintering phases, which likely affect the bacterial symbionts living on the amphibian skin. However, the skin microbiota is an important first line of defense against pathogens that can cause amphibian declines, such as the chytrid Batrachochytrium dendrobatidis (Bd). Determining whether current husbandry practices for assurance populations might deplete amphibians from their symbionts is therefore essential to conservation success. Here, we characterize the effect of the transitions from the wild to captivity, and between aquatic and overwintering phases, on the skin microbiota of two newt species. While our results confirm differential selectivity of skin microbiota between species, they underscore that captivity and phase-shifts similarly affect their community structure. More specifically, the translocation ex-situ is associated with rapid impoverishment, decrease in alpha diversity and strong species turnover of bacterial communities. Shifts between active and overwintering phases also cause changes in the diversity and composition of the microbiota, and on the prevalence of Bd-inhibitory phylotypes. Altogether, our results suggest that current husbandry practices strongly restructure the amphibian skin microbiota. Although it remains to be determined whether these changes are reversible or have deleterious effects on their hosts, we discuss methods to limit microbial diversity loss ex-situ and emphasize the importance of integrating bacterial communities to applied amphibian conservation. Frontiers Media S.A. 2023-02-20 /pmc/articles/PMC9986596/ /pubmed/36891392 http://dx.doi.org/10.3389/fmicb.2023.1111018 Text en Copyright © 2023 Fieschi-Méric, Van Leeuwen, Hopkins, Bournonville, Denoël and Lesbarrères. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Fieschi-Méric, Léa
Van Leeuwen, Pauline
Hopkins, Kevin
Bournonville, Marie
Denoël, Mathieu
Lesbarrères, David
Strong restructuration of skin microbiota during captivity challenges ex-situ conservation of amphibians
title Strong restructuration of skin microbiota during captivity challenges ex-situ conservation of amphibians
title_full Strong restructuration of skin microbiota during captivity challenges ex-situ conservation of amphibians
title_fullStr Strong restructuration of skin microbiota during captivity challenges ex-situ conservation of amphibians
title_full_unstemmed Strong restructuration of skin microbiota during captivity challenges ex-situ conservation of amphibians
title_short Strong restructuration of skin microbiota during captivity challenges ex-situ conservation of amphibians
title_sort strong restructuration of skin microbiota during captivity challenges ex-situ conservation of amphibians
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9986596/
https://www.ncbi.nlm.nih.gov/pubmed/36891392
http://dx.doi.org/10.3389/fmicb.2023.1111018
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