Stability of microbiota facilitated by host immune regulation: informing probiotic strategies to manage amphibian disease.

Microbial communities can augment host immune responses and probiotic therapies are under development to prevent or treat diseases of humans, crops, livestock, and wildlife including an emerging fungal disease of amphibians, chytridiomycosis. However, little is known about the stability of host-asso...

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Autores principales: Denise Küng, Laurent Bigler, Leyla R Davis, Brian Gratwicke, Edgardo Griffith, Douglas C Woodhams
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Publicado: Public Library of Science (PLoS) 2014
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Acceso en línea:https://doaj.org/article/badf098a2ccb47848af2d3df3cf8f119
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spelling oai:doaj.org-article:badf098a2ccb47848af2d3df3cf8f1192021-11-18T08:35:05ZStability of microbiota facilitated by host immune regulation: informing probiotic strategies to manage amphibian disease.1932-620310.1371/journal.pone.0087101https://doaj.org/article/badf098a2ccb47848af2d3df3cf8f1192014-01-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/24489847/pdf/?tool=EBIhttps://doaj.org/toc/1932-6203Microbial communities can augment host immune responses and probiotic therapies are under development to prevent or treat diseases of humans, crops, livestock, and wildlife including an emerging fungal disease of amphibians, chytridiomycosis. However, little is known about the stability of host-associated microbiota, or how the microbiota is structured by innate immune factors including antimicrobial peptides (AMPs) abundant in the skin secretions of many amphibians. Thus, conservation medicine including therapies targeting the skin will benefit from investigations of amphibian microbial ecology that provide a model for vertebrate host-symbiont interactions on mucosal surfaces. Here, we tested whether the cutaneous microbiota of Panamanian rocket frogs, Colostethus panamansis, was resistant to colonization or altered by treatment. Under semi-natural outdoor mesocosm conditions in Panama, we exposed frogs to one of three treatments including: (1) probiotic - the potentially beneficial bacterium Lysinibacillus fusiformis, (2) transplant - skin washes from the chytridiomycosis-resistant glass frog Espadarana prosoblepon, and (3) control - sterile water. Microbial assemblages were analyzed by a culture-independent T-RFLP analysis. We found that skin microbiota of C. panamansis was resistant to colonization and did not differ among treatments, but shifted through time in the mesocosms. We describe regulation of host AMPs that may function to maintain microbial community stability. Colonization resistance was metabolically costly and microbe-treated frogs lost 7-12% of body mass. The discovery of strong colonization resistance of skin microbiota suggests a well-regulated, rather than dynamic, host-symbiont relationship, and suggests that probiotic therapies aiming to enhance host immunity may require an approach that circumvents host mechanisms maintaining equilibrium in microbial communities.Denise KüngLaurent BiglerLeyla R DavisBrian GratwickeEdgardo GriffithDouglas C WoodhamsPublic Library of Science (PLoS)articleMedicineRScienceQENPLoS ONE, Vol 9, Iss 1, p e87101 (2014)
institution DOAJ
collection DOAJ
language EN
topic Medicine
R
Science
Q
spellingShingle Medicine
R
Science
Q
Denise Küng
Laurent Bigler
Leyla R Davis
Brian Gratwicke
Edgardo Griffith
Douglas C Woodhams
Stability of microbiota facilitated by host immune regulation: informing probiotic strategies to manage amphibian disease.
description Microbial communities can augment host immune responses and probiotic therapies are under development to prevent or treat diseases of humans, crops, livestock, and wildlife including an emerging fungal disease of amphibians, chytridiomycosis. However, little is known about the stability of host-associated microbiota, or how the microbiota is structured by innate immune factors including antimicrobial peptides (AMPs) abundant in the skin secretions of many amphibians. Thus, conservation medicine including therapies targeting the skin will benefit from investigations of amphibian microbial ecology that provide a model for vertebrate host-symbiont interactions on mucosal surfaces. Here, we tested whether the cutaneous microbiota of Panamanian rocket frogs, Colostethus panamansis, was resistant to colonization or altered by treatment. Under semi-natural outdoor mesocosm conditions in Panama, we exposed frogs to one of three treatments including: (1) probiotic - the potentially beneficial bacterium Lysinibacillus fusiformis, (2) transplant - skin washes from the chytridiomycosis-resistant glass frog Espadarana prosoblepon, and (3) control - sterile water. Microbial assemblages were analyzed by a culture-independent T-RFLP analysis. We found that skin microbiota of C. panamansis was resistant to colonization and did not differ among treatments, but shifted through time in the mesocosms. We describe regulation of host AMPs that may function to maintain microbial community stability. Colonization resistance was metabolically costly and microbe-treated frogs lost 7-12% of body mass. The discovery of strong colonization resistance of skin microbiota suggests a well-regulated, rather than dynamic, host-symbiont relationship, and suggests that probiotic therapies aiming to enhance host immunity may require an approach that circumvents host mechanisms maintaining equilibrium in microbial communities.
format article
author Denise Küng
Laurent Bigler
Leyla R Davis
Brian Gratwicke
Edgardo Griffith
Douglas C Woodhams
author_facet Denise Küng
Laurent Bigler
Leyla R Davis
Brian Gratwicke
Edgardo Griffith
Douglas C Woodhams
author_sort Denise Küng
title Stability of microbiota facilitated by host immune regulation: informing probiotic strategies to manage amphibian disease.
title_short Stability of microbiota facilitated by host immune regulation: informing probiotic strategies to manage amphibian disease.
title_full Stability of microbiota facilitated by host immune regulation: informing probiotic strategies to manage amphibian disease.
title_fullStr Stability of microbiota facilitated by host immune regulation: informing probiotic strategies to manage amphibian disease.
title_full_unstemmed Stability of microbiota facilitated by host immune regulation: informing probiotic strategies to manage amphibian disease.
title_sort stability of microbiota facilitated by host immune regulation: informing probiotic strategies to manage amphibian disease.
publisher Public Library of Science (PLoS)
publishDate 2014
url https://doaj.org/article/badf098a2ccb47848af2d3df3cf8f119
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