Integrative analysis of rumen microbiota and host multi-organ interactions underlying feed conversion efficiency in Hu sheep

BACKGROUND: Rumen microbiota drive fermentation and contribute to variation in feed efficiency among ruminants, yet the underlying host-microbe mechanisms remain poorly understood. This study explores how rumen microbes shape feed conversion efficiency (FCR) through integrated interactions with multiple host organs. RESULTS: We applied a multi-omics strategy-combining rumen metagenomics and host multi-organ transcriptomics-in Hu sheep with divergent FCR. From a uniform cohort of 150 weaned male Hu lambs, 13 low-FCR (LFCR) and 13 high-FCR (HFCR) individuals were selected for integrated analyses. LFCR sheep exhibited greater growth performance and higher ruminal propionate concentrations compared with HFCR animals. The ruminal microbiomes were enriched in Saccharofermentans and Succinivibrionaceae_UBA2804, and showed functional convergence on amino acid biosynthesis, central carbon metabolism, and propionate-oriented fermentation in LFCR sheep. Carbohydrate-active enzyme profiles indicated that LFCR animals favored fiber- and starch-associated modules (GH126, CBM27, EPS-GT), whereas HFCR animals were enriched in host-glycan and uronic acid-degrading families (CE14, GH89, PL15). Hydrogen metabolism highlighted a clear dichotomy: LFCR animals redirected H₂ toward propionate and sulfate reduction, while HFCR animals retained greater butyrate-producing and methanogenic capacity. Transcriptomic profiling across rumen epithelium, liver, and muscle identified tissue-specific regulatory modules. Only the liver showed strong enrichment of carbohydrate metabolism, with a complete glycogen turnover and glucose export system (GYS2, PYGL, PGM2, G6PC1) and pathways linking microbial short-chain fatty acids to gluconeogenesis. In contrast, muscle efficiency modules were dominated by contractile and cytoskeletal genes (e.g., MYL2, TNNC1, TPM3), reflecting optimized energy expenditure rather than substrate metabolism. No efficiency-associated modules were detected in the rumen epithelium, consistent with its role in propionate absorption rather than metabolism. CONCLUSIONS: The rumen microbiota of LFCR sheep possess highly efficient capacities for volatile fatty acid and amino acid synthesis, thereby enhancing energy utilization at its source. The resulting propionate further promotes hepatic gluconeogenesis, directly supplying energy for muscle cell growth and ultimately improving FCR. Thus, co-metabolism between rumen microbiota and the liver provides energy for muscle cell growth and is a key determinant of improved feed efficiency.