Habituation drives elevated antimicrobial resistance, functional, and compositional shifts in the black bear gut microbiome

Abstract

Wildlife habituation across the globe poses threats to human and animal safety and alters regular ecological function, yet the wildlife, environmental, and public health ramifications are poorly characterized. The gut microbiome is a valuable proxy for these factors as it is affected by anthropogenic exposure, influences host health, and may contribute to the environmental spread of virulence factors. Despite their importance, wildlife gut microbiomes are largely uncharacterized, both in composition and function. We characterized American black bear (Ursus americanus) gut microbiomes across a spectrum of lifestyles including wild (conflict-free), habituated (conflict-prone), and captive individuals. 16S rRNA gene sequencing was used for compositional analyses and whole genome short-read sequencing (WGS) was performed on a subset of bears to investigate microbiome function and virulence factors. We found that habituated, wild, and captive bears have unique gut microbiome compositions that are indicative of their respective lifestyles. In particular, captive bears are enriched in carnivory-associated gut microbiomes and habituated bears in inflammatory gut microbiomes. WGS reveals wild bears have increased fungi and soil-associated bacteria, as well as higher proportions of unclassified reads. Habituated bears have significantly increased levels of antimicrobial resistance genes, and captive bears are enriched in enterotoxins. We demonstrate that consequences of wildlife habituation corroborate a One Health framework, showing the interconnectedness of human, animal, plant, and environmental health. Graphical Abstract