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Moving Beyond the Host: Unraveling the Skin Microbiome of Endangered Costa Rican Amphibians

Some neotropical amphibians, including a few species in Costa Rica, were presumed to be “extinct” after dramatic population declines in the late 1980s but have been rediscovered in isolated populations. Such populations seem to have evolved a resistance/tolerance to Batrachochytrium dendrobatidis (B...

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Autores principales: Jiménez, Randall R., Alvarado, Gilbert, Estrella, Josimar, Sommer, Simone
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6751270/
https://www.ncbi.nlm.nih.gov/pubmed/31572313
http://dx.doi.org/10.3389/fmicb.2019.02060
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author Jiménez, Randall R.
Alvarado, Gilbert
Estrella, Josimar
Sommer, Simone
author_facet Jiménez, Randall R.
Alvarado, Gilbert
Estrella, Josimar
Sommer, Simone
author_sort Jiménez, Randall R.
collection PubMed
description Some neotropical amphibians, including a few species in Costa Rica, were presumed to be “extinct” after dramatic population declines in the late 1980s but have been rediscovered in isolated populations. Such populations seem to have evolved a resistance/tolerance to Batrachochytrium dendrobatidis (Bd), a fungal pathogen that causes a deadly skin disease and is considered one of the main drivers of worldwide amphibian declines. The skin microbiome is an important component of the host’s innate immune system and is associated with Bd-resistance. However, the way that the bacterial diversity of the skin microbiome confers protection against Bd in surviving species remains unclear. We studied variation in the skin microbiome and the prevalence of putatively anti-Bd bacterial taxa in four co-habiting species in the highlands of the Juan Castro Blanco National Park in Costa Rica using 16S rRNA amplicon sequencing. Lithobates vibicarius, Craugastor escoces, and Isthmohyla rivularis have recently been rediscovered, whereas Isthmohyla pseudopuma has suffered population fluctuations but has never disappeared. To investigate the life stage at which the protective skin microbiome is shaped and when shifts occur in the diversity of putatively anti-Bd bacteria, we studied the skin microbiome of tadpoles, juveniles and adults of L. vibicarius. We show that the skin bacterial composition of sympatric species and hosts with distinct Bd-infection statuses differs at the phyla, family, and genus level. We detected 94 amplicon sequence variants (ASVs) with putative anti-Bd activity pertaining to distinct bacterial taxa, e.g., Pseudomonas spp., Acinetobacter johnsonii, and Stenotrophomonas maltophilia. Bd-uninfected L. vibicarius harbored 79% more putatively anti-Bd ASVs than Bd-infected individuals. Although microbiome composition and structure differed across life stages, the diversity of putative anti-Bd bacteria was similar between pre- and post-metamorphic stages of L. vibicarius. Despite low sample size, our results support the idea that the skin microbiome is dynamic and protects against ongoing Bd presence in endangered species persisting after their presumed extinction. Our study serves as a baseline to understand the microbial patterns in species of high conservation value. Identification of microbial signatures linked to variation in disease susceptibility might, therefore, inform mitigation strategies for combating the global decline of amphibians.
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spelling pubmed-67512702019-09-30 Moving Beyond the Host: Unraveling the Skin Microbiome of Endangered Costa Rican Amphibians Jiménez, Randall R. Alvarado, Gilbert Estrella, Josimar Sommer, Simone Front Microbiol Microbiology Some neotropical amphibians, including a few species in Costa Rica, were presumed to be “extinct” after dramatic population declines in the late 1980s but have been rediscovered in isolated populations. Such populations seem to have evolved a resistance/tolerance to Batrachochytrium dendrobatidis (Bd), a fungal pathogen that causes a deadly skin disease and is considered one of the main drivers of worldwide amphibian declines. The skin microbiome is an important component of the host’s innate immune system and is associated with Bd-resistance. However, the way that the bacterial diversity of the skin microbiome confers protection against Bd in surviving species remains unclear. We studied variation in the skin microbiome and the prevalence of putatively anti-Bd bacterial taxa in four co-habiting species in the highlands of the Juan Castro Blanco National Park in Costa Rica using 16S rRNA amplicon sequencing. Lithobates vibicarius, Craugastor escoces, and Isthmohyla rivularis have recently been rediscovered, whereas Isthmohyla pseudopuma has suffered population fluctuations but has never disappeared. To investigate the life stage at which the protective skin microbiome is shaped and when shifts occur in the diversity of putatively anti-Bd bacteria, we studied the skin microbiome of tadpoles, juveniles and adults of L. vibicarius. We show that the skin bacterial composition of sympatric species and hosts with distinct Bd-infection statuses differs at the phyla, family, and genus level. We detected 94 amplicon sequence variants (ASVs) with putative anti-Bd activity pertaining to distinct bacterial taxa, e.g., Pseudomonas spp., Acinetobacter johnsonii, and Stenotrophomonas maltophilia. Bd-uninfected L. vibicarius harbored 79% more putatively anti-Bd ASVs than Bd-infected individuals. Although microbiome composition and structure differed across life stages, the diversity of putative anti-Bd bacteria was similar between pre- and post-metamorphic stages of L. vibicarius. Despite low sample size, our results support the idea that the skin microbiome is dynamic and protects against ongoing Bd presence in endangered species persisting after their presumed extinction. Our study serves as a baseline to understand the microbial patterns in species of high conservation value. Identification of microbial signatures linked to variation in disease susceptibility might, therefore, inform mitigation strategies for combating the global decline of amphibians. Frontiers Media S.A. 2019-09-12 /pmc/articles/PMC6751270/ /pubmed/31572313 http://dx.doi.org/10.3389/fmicb.2019.02060 Text en Copyright © 2019 Jiménez, Alvarado, Estrella and Sommer. 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
Jiménez, Randall R.
Alvarado, Gilbert
Estrella, Josimar
Sommer, Simone
Moving Beyond the Host: Unraveling the Skin Microbiome of Endangered Costa Rican Amphibians
title Moving Beyond the Host: Unraveling the Skin Microbiome of Endangered Costa Rican Amphibians
title_full Moving Beyond the Host: Unraveling the Skin Microbiome of Endangered Costa Rican Amphibians
title_fullStr Moving Beyond the Host: Unraveling the Skin Microbiome of Endangered Costa Rican Amphibians
title_full_unstemmed Moving Beyond the Host: Unraveling the Skin Microbiome of Endangered Costa Rican Amphibians
title_short Moving Beyond the Host: Unraveling the Skin Microbiome of Endangered Costa Rican Amphibians
title_sort moving beyond the host: unraveling the skin microbiome of endangered costa rican amphibians
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6751270/
https://www.ncbi.nlm.nih.gov/pubmed/31572313
http://dx.doi.org/10.3389/fmicb.2019.02060
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