The previous studies have reported that the mammalian gut microbiota is a physiological consequence; nonetheless, the factors influencing its composition and function remain unclear. In this study, to evaluate the contributions of the host and environment to the gut microbiota, we conducted a sequencing analysis of 16S rDNA and shotgun metagenomic DNA from plateau pikas and yaks, two sympatric herbivorous mammals, and further compared the sequences in summer and winter. The results revealed that both pikas and yaks harboured considerably more distinct communities between summer and winter. We detected the over-representation of Verrucomicrobia and Proteobacteria in pikas, and Archaea and Bacteroidetes in yaks. Firmicutes and Actinobacteria, associated with energy-efficient acquisition, significantly enriched in winter. The diversity of the microbial community was determined by the interactive effects between the host and season. Metagenomic analysis revealed that methane-metabolism-related pathway of yaks was significantly enriched in summer, while some pathogenic pathways were more abundant in pikas. Both pikas and yaks had a higher capacity for lipid degradation in winter. Pika and yak shared more OTUs when food shortage occurred in winter, and this caused a convergence in gut microbial composition and function. From winter to summer, the network module number increased from one to five in pikas, which was different in yaks. Our study demonstrates that the host is a dominant factor in shaping the microbial communities and that seasonality promotes divergence or convergence based on dietary quality across host species identity.

Interactions between species provide the basis for understanding coexisting mechanisms. The plateau pika (Ochotona curzoniae) and the yak (Bos grunniens) are considered competitors because they have shared habitats and consumed similar food on the Qinghai–Tibetan Plateau for more than 1 million years. Interestingly, the population density of plateau pikas increases with yak population expansion and subsequent overgrazing. To reveal the underlying mechanism, we sequenced the fecal microbial 16S rDNA from both sympatric and allopatric pikas and yaks. Our results indicated that sympatry increased both gut microbial diversity and similarity between pikas and yaks. The abundance of Firmicutes, Proteobacteria, Cyanobacteria, and Tenericutes decreased, while that of Verrucomicrobia increased in sympatric pikas. As for sympatric yaks, Firmicutes, Bacteroidetes, and Spirochaetes significantly increased, while Cyanobacteria, Euryarchaeota, and Verrucomicrobia significantly decreased. In sympatry, plateau pikas acquired 2692 OTUs from yaks, and yaks obtained 453 OTUs from pikas. The predominant horizontally transmitted bacteria were Firmicutes, Bacteroidetes, Verrucomicrobia, and Proteobacteria. These bacteria enhanced the enrichment of pathways related to prebiotics and immunity for pikas, such as heparin sulfate, heparin, chitin disaccharide, chondroitin-sulfate-ABC, and chondroitin-AC degradation pathways. In yaks, the horizontally transmitted bacteria enhanced pathways related to hepatoprotection, xenobiotic biodegradation, and detoxification. Our results suggest that horizontal transmission is a process of selection, and pikas and yaks tend to develop reciprocity through the horizontal transmission of gut microbiota.

Animal gut microbiomes can be clustered into “enterotypes” characterized by an abundance of signature genera. The characteristic determinants, stability, and resilience of these community clusters remain poorly understood. We used plateau pika (Ochotona curzoniae) as a model and identified three enterotypes by 16S rDNA sequencing. Among the top 15 genera, 13 showed significantly different levels of abundance between the enterotypes combined with different microbial functions and distinct fecal short-chain fatty acids. We monitored changes in the microbial community associated with the transfer of plateau pikas from field to laboratory and observed that feeding them a single diet reduced microbial diversity, resulting in a single enterotype with an altered composition of the dominant bacteria. However, microbial diversity, an abundance of some changed dominant genera, and enterotypes were partially restored after adding swainsonine (a plant secondary compound found in the natural diet of plateau pikas) to the feed. These results provide strong evidence that gut microbial diversity and enterotypes are directly related to specific diet, thereby indicating that the formation of different enterotypes can help animals adapt to complex food conditions. Additionally, natural plant secondary compounds can maintain dominant bacteria and inter-individual differences of gut microbiota and promote the resilience of enterotypes in small herbivorous mammals.