Exploring the mechanisms by which the microbiome influences muscle development during early growth in pigs through holo-omics analyses

Abstract

The gut microbiota is intricately linked to host phenotypes, yet its influence on host early growth and development, especially regarding the development of meat quality traits remains poorly understood. Here, we applied integrative multi-omics analyses of the gut microbiome, metabolome, and transcriptomes of muscle and colon tissues in Jinhua pigs during the rapid growth stage. At 90 days of age, Jinhua pigs exhibited a marked increase in microbial diversity, accompanied by enhanced microbial carbohydrate utilization and butyrate metabolism. To dissect host-microbe interactions, we integrated microbiome quantitative trait locus mapping with host whole-genome sequencing. Blautia wexlerae ( B. wexlerae ) emerged as a key microbial species genetically associated with multiple muscle related and meat quality traits. Colocalization and Mendelian randomization analyses implicated CPSF3 as a putative host gene potentially mediating the association of B. wexlerae on phenotypes such as loin muscle depth and lean meat percentage. Functional validation in mouse models showed that B. wexlerae supplementation was associated with improved muscle development, increased markers of type I muscle fibers, and attenuation of dexamethasone-induced muscle atrophy. B. wexlerae was associated with increased Ppargc1a expression in skeletal muscle, suggesting a potential role in muscle metabolism and fiber type specification. Overall, this study not only provides a promising avenue for enhancing pork quality through microbial interventions but also offers valuable insights for developing microbiota-based therapeutic treatments for human muscle related conditions such as sarcopenia and muscle atrophy.