Glutaminolysis Mediated by the Gut-Muscle Axis Facilitates Collagen Cross-Linking to Regulate Muscle Texture Traits in Tilapia

The potential involvement of gut microbiota and associated metabolites in regulating the muscle texture traits of farmed animals remains largely unexplored. Herein, a cohort of 74 tilapia was enrolled and subjected to a prolonged fava bean-based diet. Texture profile analysis revealed significant interindividual variability in muscle texture properties. Tilapia with higher muscle hardness were characterized by elevated collagen cross-linking levels. Transplantation of gut microbiota from high-hardness tilapia increased the expression of collagen cross-linking enzymes in gnotobiotic zebrafish. Serum metabolomics analysis identified L-glutamine as a prominent differentially abundant metabolite, which exhibited a strong positive correlation with muscle hardness and collagen pyridinoline contents. High-hardness tilapia showed enhanced L-glutamine catabolism. Moreover, glutaminolysis-derived α-ketoglutarate (αKG) supported the expression of collagen cross-linking enzymes in the fish fibroblast. Dietary αKG supplementation enhanced muscle collagen cross-linking and improved the texture properties of the tilapia. These findings established a microbiota-L-glutamine-αKG axis that mediated the gut-muscle crosstalk, offering a potential strategy for improving texture traits in animal production.