Variation and assembly mechanisms of Rhinolophus ferrumequinum skin and cave environmental fungal communities during hibernation periods

Microbiol Spectr. 2025 Jan 23:e0223324. doi: 10.1128/spectrum.02233-24. Online ahead of print.

Abstract

Animal skin acts as the barrier against invasion by pathogens and microbial colonizers. Environmental microbiota plays a significant role in shaping these microbial communities, which, in turn, have profound implications for host health. Previous research has focused on characterizing microorganisms on bats' skin and in their roosting environments, particularly bacterial communities. The emergence of white-nose syndrome, caused by the fungal-pathogen Pseudogymnoascus destructans, highlights the importance of understanding fungal dynamics in cave ecosystems and on bats' skin. In this study, we employed ITS amplicon sequencing to investigate the fungal community associated with the skin of Rhinolophus ferrumequinum and surfaces within hibernacula. In addition, we utilized neutral community and null models to assess the relative importance of stochastic and deterministic processes in fungal community assembly. The infection status of P. destructans did not significantly impact fungal community composition either on bat skin or cave environments. However, fungal diversity was significantly higher in cave environments compared to bat skin. Notably, potentially inhibitory genera of fungal pathogens were present in both bats and cave environments during hibernation. Furthermore, the composition and structure of fungal communities on both bat skin and cave environments varied across hibernation periods. Our findings suggest neutral processes primarily drive the assembly of fungal communities associated with hibernating R. ferrumequinum and cave environments, with dispersal limitation exerting a significant influence. This study provides insights into the fungal communities associated with hibernating R. ferrumequinum and cave environments.IMPORTANCEAnimal habitats provide sources and reservoirs for host microorganisms, making it critical to understand changes in microbial communities between habitats and hosts. While most studies have focused on bacterial microorganisms, research on fungal communities is lacking. This study investigated how community dynamics and assembly processes differ between the skin of hibernating Rhinolophus ferrumequinum and the cave environments under pathogen stress. We found significant differences in the composition and structure of the fungal communities between bat skin and roosting cave environments. Fungal genera with potential inhibitory effects on pathogens were found in all bat skin and cave environments. In addition, dispersal limitations during stochastic processes were a key factor in the formation of environmental fungal communities on bat skin and in caves. These findings offer new insights for exploring pathogen-host-environment-microbe interactions.

Keywords: Pseudogymnoascus destructans; dynamic change; environmental reservoir; fungal community; hibernation.