Temporal and geographic distribution of gut microbial enterotypes associated with host thermogenesis characteristics in plateau pikas

Abstract

ABSTRACT Differentiation of the gut microbiota between individuals within a species can be identified by enterotypes. However, whether different enterotypes are associated with host-related physiological status and adaptation to specific habitats is still poorly understood. In this study, we collected 308 cecal samples from plateau pikas during varying seasons and altitudes. We identified three bacterial and two fungal enterotypes. The proportion of Rikenellaceae_RC9_gut_group - and Prevotella -predominated enterotype 3 was higher than that of the other two enterotypes in all samples. Enterotype 1, distinguished by norank Muribaculaceae , was mainly detected during the warm season and at high altitudes, whereas enterotype 2, which is unclassified Lachnospiraceae , was mainly detected during the cold season. Plateau pikas with bacterial enterotypes 2 and 3 showed significantly higher alpha diversity than those with enterotype 1, while pikas with fungal enterotype 1 displayed higher diversity than those with enterotype 2. Functional pathways of lipid metabolism were enriched in bacterial enterotype 1, carbohydrate and amino acid metabolism were enriched in enterotype 2, and energy metabolism was enriched in enterotype 3. The neutral process was more important in bacterial enterotype 3 than in enterotypes 1 and 2. The body temperature and resting metabolic rate of pikas with bacterial enterotypes 1 and 3 were significantly higher than those with enterotype 2. Pikas with unclassified Sporormiaceae - and Sporormiella -dominated fungal enterotypes may engage more frequently in coprophagy. Overall, this study revealed that both gut bacterial and fungal communities in pikas can be clustered into enterotypes, and individuals with different enterotypes showed significant differences in thermogenesis. IMPORTANCE The gut microbiotas of small mammals play an important role in host energy homeostasis. However, it is still unknown whether small mammals with different enterotypes show differences in thermogenesis characteristics. Our study confirmed that plateau pikas with different bacterial enterotypes harbored distinct thermogenesis capabilities and employed various strategies against cold environments. Additionally, we also found that pikas with different fungal enterotypes may display differences in coprophagy.