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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.

SUBMITTER: Meteyer CU

PROVIDER: S-EPMC9176227 | biostudies-literature | 2022 Dec

REPOSITORIES: biostudies-literature

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

Meteyer Carol Uphoff CU Dutheil Julien Y JY Keel M Kevin MK Boyles Justin G JG Stukenbrock Eva H EH

Virulence 20221201 1

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 mechanis ...[more]

PMID: 35635339

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Project description:1. Fungal diseases are an emerging global problem affecting human health, food security and biodiversity. Ability of many fungal pathogens to persist within environmental reservoirs can increase extinction risks for host species and presents challenges for disease control. Understanding factors that regulate pathogen spread and persistence in these reservoirs is critical for effective disease management. 2. White-nose syndrome (WNS) is a disease of hibernating bats caused by Pseudogymnoascus destructans (Pd), a fungus that establishes persistent environmental reservoirs within bat hibernacula, which contribute to seasonal disease transmission dynamics in bats. However, host and environmental factors influencing distribution of Pd within these reservoirs are unknown. 3. We used model selection on longitudinally collected field data to test multiple hypotheses describing presence-absence and abundance of Pd in environmental substrates and on bats within hibernacula at different stages of WNS. 4. First detection of Pd in the environment lagged up to one year after first detection on bats within that hibernaculum. Once detected, the probability of detecting Pd within environmental samples from a hibernaculum increased over time and was higher in sediment compared to wall surfaces. Temperature had marginal effects on the distribution of Pd. For bats, prevalence and abundance of Pd were highest on Myotis lucifugus and on bats with visible signs of WNS. 5. Synthesis and applications. Our results indicate that distribution of Pseudogymnoascus destructans (Pd) within a hibernaculum is driven primarily by bats with delayed establishment of environmental reservoirs. Thus, collection of samples from Myotis lucifugus, or from sediment if bats cannot be sampled, should be prioritized to improve detection probabilities for Pd surveillance. Long-term persistence of Pd in sediment suggests that disease management for white-nose syndrome should address risks of sustained transmission from environmental reservoirs.

Dataset Information

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

Publications

Plant pathogens provide clues to the potential origin of bat white-nose syndrome <i>Pseudogymnoascus destructans</i>.

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