Gut Microbiota-Bile Acid Crosstalk Contributes to Meat Quality and Carcass Traits of Tan and Dorper Sheep

Tan sheep outperform Dorper sheep in meat-quality traits, including muscle fiber characteristics and fatty acid composition, while Dorper sheep excel in carcass weight. However, the molecular mechanisms underlying these breed-specific traits, especially gut microbiota-bile acid (BA) interactions, remain poorly understood. As host-microbiota co-metabolites, BAs are converted by colonic microbiota via bile salt hydrolase (BSH) and dehydroxylases into secondary BAs, which activate BA receptors to regulate host lipid and glucose metabolism. This study analyzed colonic BA profiles in 8-month-old Tan and Dorper sheep, integrating microbiome and longissimus dorsi muscle transcriptome data to investigate the gut-muscle axis in meat-quality and carcass trait regulation. Results showed that Tan sheep had 1.6-fold higher secondary BA deoxycholic acid (DHCA) levels than Dorper sheep (<i>p</i> < 0.05), whereas Dorper sheep accumulated conjugated primary BAs glycocholic acid (GCA) and tauro-α-muricholic acid (<i>p</i> < 0.05). Tan sheep exhibited downregulated hepatic BA synthesis genes, including cholesterol 7α-hydroxylase (<i>CYP7A1</i>) and 27-hydroxylase (<i>CYP27A1</i>), alongside upregulated transport genes such as bile salt export pump (<i>BSEP</i>), sodium taurocholate cotransporting polypeptide (<i>NTCP</i>), and ATP-binding cassette subfamily B member 4 (<i>ABCB4</i>), with elevated gut BSH activity (<i>p</i> < 0.05). DHCA was strongly correlated with <i>g_Ruminococcaceae_UCG-014</i>, <i>ENSOARG00000001393</i>, and <i>ENSOARG00000016726</i>, muscle fiber density, diameter, and linoleic acid (C18:2n6t) (|r| > 0.5, <i>p</i> < 0.05). In contrast, GCA was significantly associated with <i>g_Lachnoclostridium_10</i>, <i>g_Rikenellaceae_RC9_gut_group</i>, <i>ENSOARG0000001232</i>, carcass weight, and net meat weight (|r| > 0.5, <i>p</i> < 0.05). In conclusion, breed-specific colonic BA profiles were shaped by host-microbiota interactions, with DHCA potentially promoting meat quality in Tan sheep via regulation of muscle fiber development and fatty acid deposition, and GCA influencing carcass traits in Dorper sheep. This study provides novel insights into the gut microbiota-bile acid axis in modulating ruminant phenotypic traits.