Seasonal Dietary Shifts Alter the Gut Microbiota of Avivorous Bats: Implication for Adaptation to Energy Harvest and Nutritional Utilization

The coevolution between the host and its gut microbes can promote an animal’s adaptation to its specific ecological niche and changes in energy and nutritional requirements. This study focused on an avivorous bat, the great evening bat (Ia io), to investigate how seasonal dietary shifts affect the gut microbial composition and function, thereby facilitating adaptation to an avian diet. ABSTRACT Plasticity in the microbial community composition and function can permit the host to adapt to ecological, environmental, and physiological changes. Much of the information on the gut microbiota-host relationship to date derives from studies of laboratory model organisms, while little is known concerning wild animals and their ecological relevance to gut microbes. It is also unclear how microbial community composition and activity adapt to changes in diet and energy, nutritional requirements, and utilization induced by dietary expansion from invertebrates to vertebrates. The great evening bat (Ia io) is both an insectivore and an avivore (that is, a bird-eater), and thus provides an opportunity to investigate the diet-host-microbiota-physiology relationship. Here, we investigated this relationship by using 16S rRNA amplicon sequencing and functional prediction in adult males of I. io. We found that gut microbial diversity was similar, while microbial community structures were significantly different between insectivorous and avivorous diets. Moreover, increases in the relative abundance of Firmicutes and the Firmicutes-to-Bacteroidetes ratio, changes in carbohydrate and nucleotide metabolism, and a decrease in Pseudomonas were associated with higher energy demands for hunting birds and with fat storage for entering hibernation and migration. These findings demonstrated that seasonal dietary shifts drive a significant change in the composition and function of gut microbiomes, thereby facilitating adaptation to the challenging avian dietary niche in bats. These results suggest that the gut microbial communities can constantly respond to alterations in diets, potentially facilitating the diversity of wild animal dietary niches, and enhance our understanding of the diet-host-microbiota-physiology relationship. IMPORTANCE The coevolution between the host and its gut microbes can promote an animal’s adaptation to its specific ecological niche and changes in energy and nutritional requirements. This study focused on an avivorous bat, the great evening bat (Ia io), to investigate how seasonal dietary shifts affect the gut microbial composition and function, thereby facilitating adaptation to an avian diet. We found that seasonal dietary shifts driving a significant change in the composition and function of gut microbiomes in I. io were associated with higher energy demands for hunting birds and fat storage for entering hibernation and migration. Our study provides novel insight into the role of gut bacteria in generating ecological diversity and flexibility in wild mammals. The results are valuable for clarifying the complicated host-microbiota-physiology relationship in a dietary niche expansion context.