Cargando…

Habitat disturbance influences the skin microbiome of a rediscovered neotropical-montane frog

BACKGROUND: The skin microbiome serves as a first line defense against pathogens in vertebrates. In amphibians, it has the potential to protect against the chytrid fungus Batrachochytrium dendrobatis (Bd), a likely agent of amphibian declines. Alteration of the microbiome associated with unfavorable...

Descripción completa

Detalles Bibliográficos
Autores principales: Jiménez, Randall R., Alvarado, Gilbert, Sandoval, José, Sommer, Simone
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7509932/
https://www.ncbi.nlm.nih.gov/pubmed/32962670
http://dx.doi.org/10.1186/s12866-020-01979-1
_version_ 1783585689659506688
author Jiménez, Randall R.
Alvarado, Gilbert
Sandoval, José
Sommer, Simone
author_facet Jiménez, Randall R.
Alvarado, Gilbert
Sandoval, José
Sommer, Simone
author_sort Jiménez, Randall R.
collection PubMed
description BACKGROUND: The skin microbiome serves as a first line defense against pathogens in vertebrates. In amphibians, it has the potential to protect against the chytrid fungus Batrachochytrium dendrobatis (Bd), a likely agent of amphibian declines. Alteration of the microbiome associated with unfavorable environmental changes produced by anthropogenic activities may make the host more susceptible to pathogens. Some amphibian species that were thought to be “extinct” have been rediscovered years after population declines in the late 1980s probably due to evolved Bd-resistance and are now threatened by anthropogenic land-use changes. Understanding the effects of habitat disturbance on the host skin microbiome is relevant for understanding the health of these species, along with its susceptibility to pathogens such as Bd. Here, we investigate the influence of habitat alteration on the skin bacterial communities as well as specifically the putative Bd-inhibitory bacterial communities of the montane frog Lithobates vibicarius. This species, after years of not being observed, was rediscovered in small populations inhabiting undisturbed and disturbed landscapes, and with continuous presence of Bd. RESULTS: We found that cutaneous bacterial communities of tadpoles and adults differed between undisturbed and disturbed habitats. The adults from disturbed habitats exhibited greater community dispersion than those from undisturbed habitats. We observed a higher richness of putative Bd-inhibitory bacterial strains in adults from disturbed habitats than in those from undisturbed habitats, as well as a greater number of these potential protective bacteria with a high relative abundance. CONCLUSIONS: Our findings support the microbial “Anna Karenina principle”, in which disturbance is hypothesized to cause greater microbial dispersion in communities, a so-called dysbiosis, which is a response of animal microbiomes to stress factors that decrease the ability of the host or its microbiome to regulate community composition. On the positive side, the high richness and relative abundance of putative Bd-inhibitory bacteria may indicate the development of a defense mechanism that enhances Bd-protection, attributed to a co-occurrence of more than 30-years of host and pathogen in these disturbed habitats. Our results provide important insight into the influence of human-modified landscapes on the skin microbiome and health implications of Bd-survivor species.
format Online
Article
Text
id pubmed-7509932
institution National Center for Biotechnology Information
language English
publishDate 2020
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-75099322020-09-24 Habitat disturbance influences the skin microbiome of a rediscovered neotropical-montane frog Jiménez, Randall R. Alvarado, Gilbert Sandoval, José Sommer, Simone BMC Microbiol Research Article BACKGROUND: The skin microbiome serves as a first line defense against pathogens in vertebrates. In amphibians, it has the potential to protect against the chytrid fungus Batrachochytrium dendrobatis (Bd), a likely agent of amphibian declines. Alteration of the microbiome associated with unfavorable environmental changes produced by anthropogenic activities may make the host more susceptible to pathogens. Some amphibian species that were thought to be “extinct” have been rediscovered years after population declines in the late 1980s probably due to evolved Bd-resistance and are now threatened by anthropogenic land-use changes. Understanding the effects of habitat disturbance on the host skin microbiome is relevant for understanding the health of these species, along with its susceptibility to pathogens such as Bd. Here, we investigate the influence of habitat alteration on the skin bacterial communities as well as specifically the putative Bd-inhibitory bacterial communities of the montane frog Lithobates vibicarius. This species, after years of not being observed, was rediscovered in small populations inhabiting undisturbed and disturbed landscapes, and with continuous presence of Bd. RESULTS: We found that cutaneous bacterial communities of tadpoles and adults differed between undisturbed and disturbed habitats. The adults from disturbed habitats exhibited greater community dispersion than those from undisturbed habitats. We observed a higher richness of putative Bd-inhibitory bacterial strains in adults from disturbed habitats than in those from undisturbed habitats, as well as a greater number of these potential protective bacteria with a high relative abundance. CONCLUSIONS: Our findings support the microbial “Anna Karenina principle”, in which disturbance is hypothesized to cause greater microbial dispersion in communities, a so-called dysbiosis, which is a response of animal microbiomes to stress factors that decrease the ability of the host or its microbiome to regulate community composition. On the positive side, the high richness and relative abundance of putative Bd-inhibitory bacteria may indicate the development of a defense mechanism that enhances Bd-protection, attributed to a co-occurrence of more than 30-years of host and pathogen in these disturbed habitats. Our results provide important insight into the influence of human-modified landscapes on the skin microbiome and health implications of Bd-survivor species. BioMed Central 2020-09-22 /pmc/articles/PMC7509932/ /pubmed/32962670 http://dx.doi.org/10.1186/s12866-020-01979-1 Text en © The Author(s) 2020 Open AccessThis 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/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Jiménez, Randall R.
Alvarado, Gilbert
Sandoval, José
Sommer, Simone
Habitat disturbance influences the skin microbiome of a rediscovered neotropical-montane frog
title Habitat disturbance influences the skin microbiome of a rediscovered neotropical-montane frog
title_full Habitat disturbance influences the skin microbiome of a rediscovered neotropical-montane frog
title_fullStr Habitat disturbance influences the skin microbiome of a rediscovered neotropical-montane frog
title_full_unstemmed Habitat disturbance influences the skin microbiome of a rediscovered neotropical-montane frog
title_short Habitat disturbance influences the skin microbiome of a rediscovered neotropical-montane frog
title_sort habitat disturbance influences the skin microbiome of a rediscovered neotropical-montane frog
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7509932/
https://www.ncbi.nlm.nih.gov/pubmed/32962670
http://dx.doi.org/10.1186/s12866-020-01979-1
work_keys_str_mv AT jimenezrandallr habitatdisturbanceinfluencestheskinmicrobiomeofarediscoveredneotropicalmontanefrog
AT alvaradogilbert habitatdisturbanceinfluencestheskinmicrobiomeofarediscoveredneotropicalmontanefrog
AT sandovaljose habitatdisturbanceinfluencestheskinmicrobiomeofarediscoveredneotropicalmontanefrog
AT sommersimone habitatdisturbanceinfluencestheskinmicrobiomeofarediscoveredneotropicalmontanefrog