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

François-Joseph Lapointe,Virginie Lemieux-Labonté,Anouk Simard,Craig K R Willis

doi:10.1186/s40168-017-0334-y

François-Joseph Lapointe, Virginie Lemieux-Labonté + Show 2 more

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https://doi.org/10.1186/s40168-017-0334-y

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Abstract

BackgroundInfectious 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.ResultsUsing 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.ConclusionsOur 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.

Highlights

Infectious diseases of wildlife are increasing worldwide with implications for conservation and human public health
The principal coordinates analysis (PCoA), based on unweighted UniFrac, revealed a clear separation between White-nose syndrome (WNS)-positive sites in Québec and WNS-negative sites in Manitoba, and grouped samples from within the same hibernaculum (Fig. 2a). This pattern was not observed with weighted UniFrac (Fig. 2b), which implies that accounting for differential abundances, and not just the presence/absence of bacterial operational taxonomic units (OTUs) between samples, affected our results
Bat skin samples and local environmental samples were by no means identical in their compositional profiles, indicating that microbial communities on the skin of hibernating bats are probably not regulated in the same way as in the Conclusions This study highlights the role of skin microbiota for wildlife population health, conservation, and management in the face of emerging infectious diseases

Summary

Introduction

Infectious diseases of wildlife are increasing worldwide with implications for conservation and human public health. White-nose syndrome (WNS), caused by the fungus Pseudogymnoascus destructans (Pd), has killed millions of hibernating North American bats since 2007. A number of ecologically important species are threatened by white-nose syndrome (WNS). This skin disease, caused by the fungus Pseudogymnoascus destructans (Pd) [6, 7], has killed millions of North American bats since 2006 [8]. White-nose syndrome involves invasion of exposed skin by Pd, and the disease is defined by cup-shaped erosions and ulcerations on the tissue of the flight membranes (wings and tail), ears, and muzzle [9]. The immune system is downregulated during hibernation [19,20,21] which, in turn, facilitates infection

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