White-nose syndrome restructures bat skin microbiomes

Abstract

The skin microbiome is an essential line of host defense against pathogens, yet our understanding of microbial communities and how they change when hosts become infected is limited. We investigated skin microbial composition in three North American bat species (Myotis lucifugus, Eptesicus fuscus, and Perimyotis subflavus) that have been impacted by the infectious disease, white-nose syndrome, caused by an invasive fungal pathogen, Pseudogymnoascus destructans. We compared bacterial and fungal composition from 154 skin swab samples and 70 environmental samples using a targeted 16S rRNA and ITS amplicon approach. We found that for M. lucifugus, a species that experiences high mortality from white-nose syndrome, bacterial microbiome diversity was dramatically lower when P. destructans is present. Key bacterial families-including those potentially involved in pathogen defense-significantly differed in abundance in bats infected with P. destructans compared to uninfected bats. However, skin bacterial diversity was not lower in E. fuscus or P. subflavus when P. destructans was present, despite populations of the latter species declining sharply from white-nose syndrome. The fungal species present on bats substantially overlapped with the fungal taxa present in the environment at the site where the bat was sampled, but fungal community composition was unaffected by the presence of P. destructans for any of the three bat species. This species-specific alteration in bat skin bacterial microbiomes after pathogen invasion may suggest a mechanism for the severity of WNS in M. lucifugus, but not for other bat species impacted by white-nose syndrome.

Antifungal Potential of the Skin Microbiota of Hibernating Big Brown Bats (Eptesicus fuscus) Infected With the Causal Agent of White-Nose Syndrome

“…We found mixed support for our first hypothesis that Pd inoculation would have little impact on the skin microbiota of this WNS-resistant species. No taxa were significantly more abundant on Pd-inoculated bats compared to controls, at the end of the experiment, and no difference was detected in diversity as observed in the wild for this species (Ange-Stark et al, 2019). Interestingly, the observed differences in beta diversity (weighted UniFrac distances) between bats assigned to our two experimental groups disappeared by the end of the experiment.…”

“…Introduced fungal pathogens such as Batrachochytrium dendrobatidis and Batrachochytrium salamandrivorans have caused global declines and even extinctions in amphibians ( Longcore et al, 1999 ; Martel et al, 2013 ). In recent decades, studies have highlighted the potential role of skin microbiota in patterns of resistance and susceptibility to these fungal pathogens and have pointed to potential management practices that might help conserve host populations ( Harris et al, 2009 ; Bletz et al, 2013 , 2017 ; Jani and Briggs, 2014 ; Woodhams et al, 2014 ; Bataille et al, 2016 ; Ange-Stark et al, 2019 ; Rebollar et al, 2019 ). However, despite this potential, management actions based on the skin microbiota have still not been widely applied in response to wildlife disease.…”

“…Therefore, E. fuscus represents a good model to study potential resistance mechanisms resulting from the skin microbiota in a controlled environment that accounts for variation in hibernation conditions. We tested two hypotheses about the skin microbiota of E. fuscus in the context of Pd infection: (1) that Pd inoculation is not a strong selective force on the skin microbiota of this species ( Ange-Stark et al, 2019 ) and would therefore not disrupt the microbial community, and (2) that microbial taxa with antifungal properties, which are common in the hibernation sites of bats persisting after WNS (e.g., Rhodococcus and Pseudomonas , Lemieux-Labonté et al, 2017 ), would be abundant both before and after infection with Pd in this resistant species.…”

No Change Detected in Culturable Fungal Assemblages on Cave Walls in Eastern Canada with the Introduction of Pseudogymnoascus destructans

“…However, while [37] found that bacterial diversity was higher on cave walls compared to bats, fungal diversity was similar. This difference in results may be due to differing methodologies, since the culture-independent methods used by [37] detects both viable and non-viable fungi. Fungi present on cave walls are likely introduced by air currents, percolating water, and cave fauna and fungi may also grow on the rock surface [3][4][5].…”

“…Fungal diversity on cave walls in China was also higher compared to other cave substrates, such as sediments and air [6]. However, while [37] found that bacterial diversity was higher on cave walls compared to bats, fungal diversity was similar. This difference in results may be due to differing methodologies, since the culture-independent methods used by [37] detects both viable and non-viable fungi.…”