Skin fungal assemblages of bats vary based on susceptibility to white-nose syndrome

Abstract

Microbial skin assemblages, including fungal communities, can influence host resistance to infectious diseases. The diversity-invasibility hypothesis predicts that high-diversity communities are less easily invaded than species-poor communities, and thus diverse microbial communities may prevent pathogens from colonizing a host. To explore the hypothesis that host fungal communities mediate resistance to infection by fungal pathogens, we investigated characteristics of bat skin fungal communities as they relate to susceptibility to the emerging disease white-nose syndrome (WNS). Using a culture-based approach, we compared skin fungal assemblage characteristics of 10 bat species that differ in susceptibility to WNS across 10 eastern U.S. states. The fungal assemblages on WNS-susceptible bat species had significantly lower alpha diversity and abundance compared to WNS-resistant species. Overall fungal assemblage structure did not vary based on WNS-susceptibility, but several yeast species were differentially abundant on WNS-resistant bat species. One yeast species inhibited Pseudogymnoascus destructans (Pd), the causative agent on WNS, in vitro under certain conditions, suggesting a possible role in host protection. Further exploration of interactions between Pd and constituents of skin fungal assemblages may prove useful for predicting susceptibility of bat populations to WNS and for developing effective mitigation strategies.

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Fig. 1: A map showing the distribution of sampling sites and the bat species sampled at each site.
Fig. 2: Fungal abundance and diversity on the skin of bats.
Fig. 3: Operational taxonomic units (OTUs) identified as differentially abundant (p < 0.05) among WNS-susceptibility groups in pairwise comparisons.

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Acknowledgements

We thank the many field biologists who coordinated sampling efforts and collected samples, including Anne Ballmann, Shelly Colatskie, Katie O’Connor, Tony Elliott, Kyle George, Lindsey Heffernan, Carl Herzog, Catherine Hoose, Daryl Howell, Jennifer Redell, Blake Sasse, Michael Scafini, Nick Sharp, Kirk Silas, Craig Stihler, Greg Turner, Paul White, Rebecca Williams, and Michelle Verant. We are most grateful to Rick Lankau for facilitating the culture-independent analysis, Doerte Doepfer and James Paterson for providing statistical advice, and Katie Schmidt and Daniel Taylor for providing technical assistance with laboratory work. We thank the University of Wisconsin Biotechnology Center DNA Sequencing Facility and Newcomb Imaging Center for providing next-generation sequencing and electron microscopy services, respectively. This work was funded by the U.S. Fish and Wildlife Service, the U.S. Geological Survey, and a Natural Sciences and Engineering Research Council of Canada postgraduate scholarship to KJV. Portions of this work were conducted by KJV and LJC while serving as volunteers at the U.S. Geological Survey. The use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the U.S. Government. Metadata associated with this publication is available in machine-readable format at https://doi.org/10.5066/P9Y54WW4 [90]. Scripts used in the analysis of this project are available from the GitHub repository URL https://github.com/zoolew/Bat-Wing-Mycobiomes.

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Vanderwolf, K.J., Campbell, L.J., Goldberg, T.L. et al. Skin fungal assemblages of bats vary based on susceptibility to white-nose syndrome. ISME J (2020). https://doi.org/10.1038/s41396-020-00821-w

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