Plant pathogens provide clues to the potential origin of bat white-nose syndrome Pseudogymnoascus destructans

ABSTRACT

White-nose syndrome has killed millions of bats, yet both the origins and infection strategy of the causative fungus, Pseudogymnoascus destructans, remain elusive. We provide evidence for a novel hypothesis that P. destructans emerged from plant-associated fungi and retained invasion strategies affiliated with fungal pathogens of plants. We demonstrate that P. destructans invades bat skin in successive biotrophic and necrotrophic stages (hemibiotrophic infection), a mechanism previously only described in plant fungal pathogens. Further, the convergence of hyphae at hair follicles suggests nutrient tropism. Tropism, biotrophy, and necrotrophy are often associated with structures termed appressoria in plant fungal pathogens; the penetrating hyphae produced by P. destructans resemble appressoria. Finally, we conducted a phylogenomic analysis of a taxonomically diverse collection of fungi. Despite gaps in genetic sampling of prehistoric and contemporary fungal species, we estimate an 88% probability the ancestral state of the clade containing P. destructans was a plant-associated fungus.

KEYWORDS:

• Dermatophyte
• fungal pathogens
• hemibiotrophy
• hibernation
• pathogen emergence
• pathogen evolution

Acknowledgements

We would like to thank the many field biologists from State, Regional, and Federal organizations that documented progression as P. destructans spread across the United States of America and affected regions in Canada. Special thanks to Kathryn Wesenberg for help with references and others at the National Wildlife Health Center for supporting the effort to define white-nose syndrome, and to Emmanuel Paradis for helping with the use of the R ‘ace’ function. EHS is grateful for support from the Canadian Institute for Advanced Research (CIFAR). Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the U.S. Government.

Disclosure statement

No potential conflict of interest was reported by the authors.

Author contributions

CUM conceived the study, performed analyses, wrote the original draft, performed histopathology, photography and visualization of images

JYD Formal analysis, investigation, resources, visualization and writing – review and editing

MKK Investigation, resources, visualization of the data and writing – review and editing

JGB Conceptualization and writing – review and editing

EHS Formal analysis, investigation, writing – review and editing

Data availability statement

The data that support the findings of this study are openly available in Zenodo at DOI reference number 10.5281/zenodo. 5939906 at https://zenodo.org/record/5939906#.YjpiN-rMKUk.

Supplementary material

Supplemental data for this article can be accessed online at https://doi.org/10.1080/21505594.2022.2082139

Additional information

Funding

The authors reported there is no funding associated with the work featured in this article.