Enrichment of beneficial bacteria in the skin microbiota of bats persisting with white-nose syndrome

Abstract Background Infectious diseases of wildlife are increasing worldwide with implications for conservation and human public health. The microbiota (i.e. microbial community living on or in a host) could influence wildlife disease resistance or tolerance. White-nose syndrome (WNS), caused by the...

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Main Authors: Virginie Lemieux-Labonté, Anouk Simard, Craig K. R. Willis, François-Joseph Lapointe
Format: Article
Language:English
Published: BMC 2017-09-01
Series:Microbiome
Subjects:
Online Access:http://link.springer.com/article/10.1186/s40168-017-0334-y
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spelling doaj-882de25d252d49059c575af9bbd725482020-11-24T21:48:00ZengBMCMicrobiome2049-26182017-09-015111410.1186/s40168-017-0334-yEnrichment of beneficial bacteria in the skin microbiota of bats persisting with white-nose syndromeVirginie Lemieux-Labonté0Anouk Simard1Craig K. R. Willis2François-Joseph Lapointe3Département de Sciences Biologiques, Université de MontréalDirection de l’expertise sur la faune terrestre, l’herpétofaune et l’avifaune, Ministère des Forêts, de la Faune et des ParcsDepartment of Biology and Centre for Forest Interdisciplinary Research, University of WinnipegDépartement de Sciences Biologiques, Université de MontréalAbstract Background Infectious diseases of wildlife are increasing worldwide with implications for conservation and human public health. The microbiota (i.e. microbial community living on or in a host) could influence wildlife disease resistance or tolerance. White-nose syndrome (WNS), caused by the fungus Pseudogymnoascus destructans (Pd), has killed millions of hibernating North American bats since 2007. We characterized the skin microbiota of naïve, pre-WNS little brown bats (Myotis lucifugus) from three WNS-negative hibernation sites and persisting, previously exposed bats from three WNS-positive sites to test the hypothesis that the skin microbiota of bats shifts following WNS invasion. Results Using high-throughput 16S rRNA gene sequencing on 66 bats and 11 environmental samples, we found that hibernation site strongly influenced the composition and diversity of the skin microbiota. Bats from WNS-positive and WNS-negative sites differed in alpha and beta diversity, as well as in microbiota composition. Alpha diversity was reduced in persisting, WNS-positive bats, and the microbiota profile was enriched with particular taxa such Janthinobacterium, Micrococcaceae, Pseudomonas, Ralstonia, and Rhodococcus. Some of these taxa are recognized for their antifungal activity, and specific strains of Rhodococcus and Pseudomonas are known to inhibit Pd growth. Composition of the microbial community in the hibernaculum environment and the community on bat skin was superficially similar but differed in relative abundance of some bacterial taxa. Conclusions Our results are consistent with the hypothesis that Pd invasion leads to a shift in the skin microbiota of surviving bats and suggest the possibility that the microbiota plays a protective role for bats facing WNS. The detection of what appears to be enrichment of beneficial bacteria in the skin microbiota of persisting bats is a promising discovery for species re-establishment. Our findings highlight not only the potential value of management actions that might encourage transmission, growth, and establishment of beneficial bacteria on bats, and within hibernacula, but also the potential risks of such management actions.http://link.springer.com/article/10.1186/s40168-017-0334-ySkin microbiotaWhite-nose syndromeMyotis lucifugusEndangered speciesConservation and management16S rRNA
collection DOAJ
language English
format Article
sources DOAJ
author Virginie Lemieux-Labonté
Anouk Simard
Craig K. R. Willis
François-Joseph Lapointe
spellingShingle Virginie Lemieux-Labonté
Anouk Simard
Craig K. R. Willis
François-Joseph Lapointe
Enrichment of beneficial bacteria in the skin microbiota of bats persisting with white-nose syndrome
Microbiome
Skin microbiota
White-nose syndrome
Myotis lucifugus
Endangered species
Conservation and management
16S rRNA
author_facet Virginie Lemieux-Labonté
Anouk Simard
Craig K. R. Willis
François-Joseph Lapointe
author_sort Virginie Lemieux-Labonté
title Enrichment of beneficial bacteria in the skin microbiota of bats persisting with white-nose syndrome
title_short Enrichment of beneficial bacteria in the skin microbiota of bats persisting with white-nose syndrome
title_full Enrichment of beneficial bacteria in the skin microbiota of bats persisting with white-nose syndrome
title_fullStr Enrichment of beneficial bacteria in the skin microbiota of bats persisting with white-nose syndrome
title_full_unstemmed Enrichment of beneficial bacteria in the skin microbiota of bats persisting with white-nose syndrome
title_sort enrichment of beneficial bacteria in the skin microbiota of bats persisting with white-nose syndrome
publisher BMC
series Microbiome
issn 2049-2618
publishDate 2017-09-01
description Abstract Background Infectious diseases of wildlife are increasing worldwide with implications for conservation and human public health. The microbiota (i.e. microbial community living on or in a host) could influence wildlife disease resistance or tolerance. White-nose syndrome (WNS), caused by the fungus Pseudogymnoascus destructans (Pd), has killed millions of hibernating North American bats since 2007. We characterized the skin microbiota of naïve, pre-WNS little brown bats (Myotis lucifugus) from three WNS-negative hibernation sites and persisting, previously exposed bats from three WNS-positive sites to test the hypothesis that the skin microbiota of bats shifts following WNS invasion. Results Using high-throughput 16S rRNA gene sequencing on 66 bats and 11 environmental samples, we found that hibernation site strongly influenced the composition and diversity of the skin microbiota. Bats from WNS-positive and WNS-negative sites differed in alpha and beta diversity, as well as in microbiota composition. Alpha diversity was reduced in persisting, WNS-positive bats, and the microbiota profile was enriched with particular taxa such Janthinobacterium, Micrococcaceae, Pseudomonas, Ralstonia, and Rhodococcus. Some of these taxa are recognized for their antifungal activity, and specific strains of Rhodococcus and Pseudomonas are known to inhibit Pd growth. Composition of the microbial community in the hibernaculum environment and the community on bat skin was superficially similar but differed in relative abundance of some bacterial taxa. Conclusions Our results are consistent with the hypothesis that Pd invasion leads to a shift in the skin microbiota of surviving bats and suggest the possibility that the microbiota plays a protective role for bats facing WNS. The detection of what appears to be enrichment of beneficial bacteria in the skin microbiota of persisting bats is a promising discovery for species re-establishment. Our findings highlight not only the potential value of management actions that might encourage transmission, growth, and establishment of beneficial bacteria on bats, and within hibernacula, but also the potential risks of such management actions.
topic Skin microbiota
White-nose syndrome
Myotis lucifugus
Endangered species
Conservation and management
16S rRNA
url http://link.springer.com/article/10.1186/s40168-017-0334-y
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