Meat quality is a complex trait that exhibits significant variation across pig breeds, and the regulatory mechanisms governing pork meat quality are not fully elucidated. We compared the transcriptomics and metabolomics of the longissimus dorsi (LD) muscle between the Songliao Black Pig (SBP) and Large White × Landrace Pig (LWLDP) to investigate breed-specific differences in meat quality and underlying regulatory pathways. The results showed that SBP meat had a higher marbling score and backfat thickness, a richer color, a lower shear force, and reduced drip loss. Fatty acid (FA) analysis identified 15 significant FAs in the LWLDP, with docosahexaenoic acid (DHA) in the SBP, while amino acid (AA) analysis revealed no breed-based differences. Transcriptome analysis identified 134 upregulated and 362 downregulated genes in the SBP. Protein–protein interaction (PPI) network analysis found 25 key genes, which are associated with muscle development, fat deposition, and overall meat quality, while genes in the insulin signaling pathway, such as PPP1R3B, PPARGC1A, SOCS1, EIF4E, PRKAR2A, PRKAG2, and FASN, play a crucial role in balancing fat metabolism and catabolism. Metabolomic analysis identified 89 upregulated and 10 downregulated metabolites in the SBP, primarily involved in fructose and mannose metabolism, amino acid biosynthesis, nucleotide sugar metabolism, and glucagon signaling pathways. Gene–metabolite association analysis found that the PPP1R3B gene had a strong association with Thr-Leu, Maltol, D-myo-Inositol-4-phosphate, and Fructose-6-phosphate, while MYOG correlated with Mannose-6-phosphate, Fructose-1-phosphate, Mannose-1-phosphate, and Glucose-6-phosphate. In contrast, NR4A3 and PPARGC1A showed a strong negative correlation with most upregulated metabolites. In conclusion, this study identified functional genes, elucidated the mechanisms associated with meat quality traits, and identified gene–metabolite associations involved in energy metabolism, muscle development, and fat deposition, providing valuable insights into the molecular mechanisms that regulate meat quality between pig breeds.

The gut microbiota plays a pivotal role in host metabolism, influencing the production of small metabolites from non-digestible compounds, which can accumulate in tissues and play important role in fatty acids synthesis for improving the meat quality. We investigate the breed-specific differences in longissimus dorsi (LD) muscle fatty acid profile, gut microbiota, and metabolites across the cecum, ileum, and rectum in Chinese Songliao Black pigs (SBP) and commercial Large White × Landrace crossbred pigs (LWLDP) and interactions. Significant correlations highlighting potential microbiota-metabolite interactions that contribute to muscle fatty acid composition. LWLDP pigs exhibited a higher number of significant fatty acids and maintained higher operational taxonomic units (OTUs) in the cecum and rectum, with no differences observed in the ileum between breeds. Firmicutes, Bacteroidetes, Proteobacteria, and Spirochaetes were the predominant phyla across both breeds. Differentially expressed metabolites (DEMs) were more abundant in the cecum and ileum of LWLDP, while rectum showed higher expression in SBP. Integrative analysis identified significant correlations between fatty acids, metabolites, and microbial taxa. DHA was linked to cecal metabolites and rectal microbial families, while saturated and unsaturated fatty acids were associated with different microbes and metabolites. This study demonstrates distinct breed-specific interactions between gut microbiota, metabolites, and fatty acid composition, offering insights into potential microbial interventions to enhance pork quality through fatty acid modulation.