Rumen microbiome carbohydrate metabolism is associated with host lipid metabolic differences between Wagyu and Nanyang cattle

The rumen microbiome plays an important role in converting dietary carbohydrates into metabolites associated with host physiology, yet the relationships between microbial carbohydrate metabolism and host lipid metabolism remain incompletely understood. Here, we compared Japanese Wagyu and Nanyang cattle to investigate microbiota–metabolite–host associations in relation to breed-associated differences in intramuscular fat (IMF) deposition. Metagenomic analysis revealed differences in rumen microbial community composition and functional profiles between breeds, including differential abundances of carbohydrate-active enzyme (CAZyme) families associated with polysaccharide degradation. Wagyu cattle exhibited higher abundances of glycoside hydrolase (GH) families GH5 (cellulose degradation) and GH92 (alpha-mannan degradation), whereas GH13 (starch degradation) and GH43 (arabinoxylan and arabinan degradation) were enriched in Nanyang cattle, together with differences in carbohydrate-degrading genera, including Prevotella , Fibrobacter , and Butyrivibrio . These microbial functional differences were accompanied by distinct fermentation profiles, with higher ruminal acetate and butyrate concentrations in Wagyu cattle and higher propionate concentrations in Nanyang cattle. Proteomic analysis of the longissimus dorsi muscle identified breed-associated differences in proteins involved in lipid synthesis, lipid storage, and energy metabolism, including FABP4, FASN, PLIN1, ACSS2, and IDH1, which showed higher abundances in Wagyu cattle. Correlation analyses identified associations among microbial taxa, CAZyme families, fermentation metabolites, and host proteins related to lipid metabolism and IMF deposition. Overall, these findings reveal coordinated breed-associated differences in rumen microbial functions, fermentation characteristics, and host lipid metabolic profiles, providing insights into microbiota–host metabolic associations related to IMF deposition in cattle. Keypoints • Rumen carbohydrate-active enzyme (CAZyme) profiles differ between Wagyu and Nanyang cattle. • Wagyu cattle show higher acetate and butyrate levels. • Microbiota–volatile fatty acids (VFAs)–proteome axis is linked to intramuscular fat (IMF) deposition