Integrative metabolic and lipidomic analysis reveals microbiota-associated mechanisms of thigh meat quality variation in spent laying hens from different rearing systems.

This study aims to elucidate the differences in poultry meat quality between cage-rearing (CR) and free-range (FR) rearing systems and to dissect the underlying microbiota-mediated mechanisms. A total of 200 Jianghan laying hens (50-week-old) were equally assigned to either FR or CR group. At 56 w, 10 hens from each group were selected and underwent integrated analyses of gut microbial metagenomes, muscle nutrient composition, amino acid, and lipid profiles. The results showed that the FR group had lower abdominal fat yield but higher leg muscle yield (P < 0.01). Leg muscle of FR hens exhibited lower crude fat content, drip loss, malondialdehyde levels, but higher pH24h, glutathione peroxidase (GSH-Px) activity and DPPH radical-scavenging rate (P < 0.05). Additionally, the FR group showed significant increases in glutamic acid, alanine, isoleucine, tyrosine, phenylalanine, histidine, arginine and total flavor amino acids (FAA, P < 0.05). Lipidomic profiling identified 38 differentially abundant lipids and an elevation in total fatty acyls in FR muscles. Subsequent fatty acids composition analysis revealed higher proportions of C20:4 and total polyunsaturated fatty acids (PUFA) in the FR group (P < 0.05). Cecal microbiota analysis indicated FR rearing increased the relative abundances of Ligilactobacillus aviarius, Enterococcus faecium, Corynebacterium stationis, C.glutamicum, and C.casei (P < 0.05). Correlation analyses demonstrated that L. aviarius was positively correlated with FAA content, while the three Corynebacterium species were positively correlated with GSH-Px activity, pH24h, FAA, and PUFA, and negatively with drip loss (|r| > 0.6, P < 0.05). Collectively, free-range rearing improves meat quality and nutritional traits, which may be linked to changes in the gut microbial community.