Bacterial-Fungal Co-Occurrence in the Porcine Gut Microbiome Is Associated with Distinctive Meat Flavor Profiles in Indigenous Congjiang Xiang Pigs.

Meat flavor significantly influences consumer preference and market value, particularly for indigenous pig breeds renowned for distinctive sensory characteristics. While traditional research has focused on genetic factors and feeding regimens, emerging evidence suggests that gut microbiota plays a crucial role in meat quality attributes. However, the specific contribution of bacterial-fungal co-occurrence to meat flavor formation remains largely unexplored. This study aimed to characterize the associations between intestinal bacterial-fungal co-occurrence networks and the muscle flavor-related metabolite profiles of CX pigs, using an integrated multi-omics approach. Twenty male pigs (10 CX and 10 LAN, 12 months old) were subjected to comprehensive analyses, including meat quality evaluation, electronic nose analysis, 16S and 18S rRNA sequencing, and untargeted metabolomics. CX pigs exhibited significantly superior meat quality characteristics, including higher moisture content (p < 0.001), fat content (p = 0.008), and meat color scores (p < 0.001). Electronic nose analysis revealed significantly higher response values across all ten aroma sensors in CX pigs (p < 0.001), with the most pronounced differences observed in sensors detecting sulfur compounds and organic compounds. Untargeted metabolomics identified 40 differential metabolites, with 27 up-regulated in CX pigs, including key flavor compounds such as glycocholic acid, isorhamnetin, and pantothenic acid. Microbiome analysis demonstrated significantly higher bacterial alpha diversity in CX pigs (p < 0.05), with enrichment of beneficial bacteria, including Rikenellaceae_RC9_gut_group, Prevotellaceae_UCG_003, and Phascolarctobacterium, while fungal communities showed enrichment of Candida_Lodderomyces_clade. Correlation network analysis revealed that Rikenellaceae_RC9_gut_group demonstrated strong positive correlations with flavor compounds (r = 0.575 for isorhamnetin, r = 0.535 for pantothenic acid, p < 0.001) and all electronic nose responses (r = 0.434-0.691, p < 0.001). Bacterial-fungal co-occurrence networks showed synergistic relationships, with Rikenellaceae_RC9_gut_group positively correlated with Candida_Lodderomyces_clade (r = 0.711, p < 0.001) while exhibiting antagonistic relationships with Piromyces (r = -0.714, p < 0.001). These findings offer novel insights for developing microbiome-targeted strategies to enhance meat quality in pig production systems.