External bacterial diversity on bats in the southwestern United States: Changes in bacterial community structure above and below ground

Abstract

Microorganisms that reside on and in mammals, such as bats, have the potential to influence their host's health and to provide potential defenses against invading pathogens. However, we have little to no understanding of the external bacterial microbiome on bats, or factors that influence the structure of these communities. The southwestern United States offers excellent sites for the study of external bat bacterial microbiomes due to the diversity of bat species, the variety of abiotic and biotic factors that may govern bat bacterial microbiome communities, and the lack of white-nose syndrome (a newly emergent fungal disease of bats) presence in the Southwest. We studied the extent to which changes in distributions of bacteria on external bat surfaces are a function of geographic location and ecoregion, and whether the sampled bats were caught in caves or surface-netted. To test these variables we used 16S rRNA gene 454 pyrosequencing from swabs of external skin and fur surfaces from 186 bats from 14 species sampled across southeastern New Mexico to northwestern Arizona. Community similarity patterns and random forest models, and generalized linear mixed-effects models show that factors such as location (e.g. cave-caught vs. surface-netted) and ecoregion are major contributors to the structure of bacterial communities on bats. Bats caught in caves had a distinct microbial community compared to those that were netted on the surface. Our results provide a first insight into the distribution of external bat bacteria in a WNS-free environment and provide a baseline of bat external microbiomes that can be explored for potential natural defenses against pathogens.

Western Bats as a Reservoir of Novel Streptomyces Species with Antifungal Activity

“…It is possible that some of these bat-associated actinobacteria have the potential to be used as a probiotic in the control of WNS, with the additional environmental advantage that these microorganisms are already natural inhabitants of cave ecosystems (31). Western caves are currently free of WNS, and therefore, it is unknown if the bacteria present on the bats and cave walls are antagonistic to the fungus in vivo; however, the present study, together with that of Winter et al, provide a preinfection baseline and serve as a valuable resource to help assess differences in response if the bats in these caves become affected by the disease (11).…”

“…It is possible that the high abundance of actinobacteria recovered from bat skin is a result of inoculation from cave walls in which they are abundant (16,18,42). For example, Winter et al reported that cave-caught bats possess a different external microbiome with respect to bats caught outside the caves (11), showing the potential influence of collection site on bat microbiota. Alternatively, actinobacteria are likely an active part of the bat microbiome, as they have been reported to be one of the most common skin habitants in multiple vertebrates, including humans (14), fish (10), amphibians (9), and bats (11).…”

“…For example, Winter et al reported that cave-caught bats possess a different external microbiome with respect to bats caught outside the caves (11), showing the potential influence of collection site on bat microbiota. Alternatively, actinobacteria are likely an active part of the bat microbiome, as they have been reported to be one of the most common skin habitants in multiple vertebrates, including humans (14), fish (10), amphibians (9), and bats (11). In humans, actinobacteria are prevalent and represent up to 50% of the human skin microbiome (6).…”

“…They are also one of the most dominant groups on the skin of different amphibian species (9), fish (10), and bats (11). Actinobacteria are well adapted to survive long periods and grow well in nutrientdepleted environments, such as caves (12).…”

Enrichment of beneficial bacteria in the skin microbiota of bats persisting with white-nose syndrome

“…Due to its direct exposure to the local environment, the skin microbiota is more dynamic and should be more strongly influenced by the environment, than the gut microbiota [ 39 ]. Environment and host species are strong predictors of variation in the skin microbiota among bats [ 40 – 42 ]. However, one study [ 43 ] found a strong influence of site and habitat type on the skin microbiota of 13 bat species in the western USA but was not able to detect an influence of host species or sex.…”