Multi-omics analysis reveals host-microbe interactions driving divergent energy allocation strategies in Tibetan sheep under cold-season feeding regimes

Abstract Background As an indigenous livestock species on the Tibetan Plateau, Tibetan sheep exhibit remarkable adaptability to low temperatures and nutrient-scarce environments. During the cold season, Tibetan sheep are typically managed under two feeding regimes: barn feeding (BF) and traditional grazing (TG). However, the molecular mechanisms underlying their adaptation to these distinct management strategies remain unclear. This study aimed to investigate the adaptive strategies of rumen function in Tibetan sheep to cold-season feeding regimes by integrating analyses of rumen morphology, microbiome, metabolome, and transcriptome. Twelve healthy Tibetan sheep with similar body weights were assigned into two groups (BF vs. TG). At the end of the experiment, rumen tissues were subjected to histological observation. Multi-omics techniques were employed to evaluate the effects of cold-season feeding regimes on rumen function in Tibetan sheep. Results The ruminal papilla height, width, and muscular thickness were significantly higher in BF group. The relative abundances of Actinobacteria and Succiniclasticum were significantly elevated in the rumen of BF group, whereas Rikenellaceae, Gracilibacteria, and Lachnospiraceae showed higher abundances in the TG group. Metabolomic analysis identified 19 differential metabolites between the two groups, including upregulated compounds in BF group (fumaric acid, maltose, L-phenylalanine, and L-alanine) and TG group (e.g., phenylacetic acid, salicyluric acid and ferulic acid). These metabolites were predominantly enriched in phenylalanine metabolism, alanine, aspartate and glutamate metabolism, and phenylalanine, tyrosine and tryptophan biosynthesis pathways. Additionally, 210 differentially expressed genes (DEGs) were identified in rumen epithelium: 100 upregulated DEGs in the BF group were enriched in nutrient metabolism-related pathways (e.g., fatty acid degradation and PPAR signaling pathway), while 110 upregulated DEGs in the TG group were associated with immune-related pathways (e.g., p53 signaling pathway and glutathione metabolism). Conclusions Among these, we observed distinct rumen functional responses to different cold-season feeding regimes in Tibetan sheep and revealed energy allocation strategies mediated by host-microbe interactions. In the BF group, Tibetan sheep adopted a "metabolic efficiency-priority" strategy, driving rumen microbiota to maximize energy capture from high-nutrient diets to support host growth. In contrast, the TG group exhibited an "environmental adaptation-priority" strategy, where rumen microbiota prioritized cellulose degradation and anti-inflammatory functions, reallocating energy toward homeostasis maintenance at the expense of rumen development and growth performance.