Pseudogymnoascus destructans invasion stage impacts the skin microbial functions of highly vulnerable Myotis lucifugus

Abstract

The role of the skin microbiome in resistance and susceptibility of wildlife to fungal pathogens has been examined from a taxonomic perspective but skin microbial function, in the context of fungal infection, has yet to be studied. Our objective was to understand effects of a bat fungal pathogen site infection status and course of invasion on skin microbial function. We sampled seven hibernating colonies of Myotis lucifugus covering three-time points over the course of Pseudogymnoascus destructans (Pd) invasion and white nose syndrome (pre-invasion, epidemic, and established). Our results support three new hypotheses about Pd and skin functional microbiome: (1) there is an important effect of Pd invasion stage, especially at the epidemic stage; (2) disruption by the fungus at the epidemic stage could decrease anti-fungal functions with potential negative effects on the microbiome and bat health; (3) the collection site might have a larger influence on microbiomes at the pre-invasion stage rather than at epidemic and established stages. Future studies with larger sample sizes and using meta-omics approaches will help confirm these hypotheses, and determine the influence of the microbiome on wildlife survival to fungal disease.

Keywords: Myotis lucifugus; Pseudogymnoascus destructans; little brown bats; microbial function assemblage; shotgun metagenomic; skin microbiome; white-nose syndrome.

Figure 1.

Functional Shannon diversity of skin microbiome samples transformed at the COG2 level according to (A) site Pd status and (B) invasion stage. Pairwise comparisons among invasion stages are significantly different for pre-invasion vs. established, and epidemic vs. established (Table 2).

Figure 2.

Principal component analysis of Aitchison skin microbiome functional profiles according to invasion stage and sites for (A) the COG2 level and (B) the COG3 level. Each point represents 5 bats.

Figure 3.

Count abundance of functions detected as significantly divergent by ANCOM according to invasion stages at 0.8 thresholds (Table S4 for W statistics). Asterisks indicate significant differences between corresponding groups.

Figure 4.

Bipartite graph associating samples pooled by sites and collection years with the more abundant functions at the COG3 level (>1%). Only the nine functions with the higher species specificity index are presented (for other functions see Table S5). The four different modules identified in the complete bipartite graph are highlighted to illustrate the relationships with the corresponding functions. Wider links indicate functions with higher relative abundance in a sample.