Pig gastrointestinal tracts harbor a heterogeneous and dynamic ecosystem populated with trillions of microbes, enhancing the ability of the host to harvest energy from dietary carbohydrates and contributing to host adipogenesis and fatness. However, the microbial community structure and related mechanisms responsible for the differences between the fatty phenotypes and the lean phenotypes of the pigs remained to be comprehensively elucidated. Herein, we first found significant differences in microbial composition and potential functional capacity among different gut locations in Jinhua pigs with distinct fatness phenotypes. Second, we identified that Jinhua pigs with lower fatness exhibited higher levels of short-chain fatty acids in the colon, highlighting their enhanced carbohydrate fermentation capacity. Third, we explored the differences in expressed carbohydrate-active enzyme (CAZyme) in pigs, indicating their involvement in modulating fat storage. Notably, Clostridium butyricum might be a representative bacterial species from Jinhua pigs with lower fatness, and a significantly higher percentage of its genome was dedicated to CAZyme glycoside hydrolase family 13 (GH13). Finally, a subsequent mouse intervention study substantiated the beneficial effects of C. butyricum isolated from experimental pigs, suggesting that it may possess characteristics that promote the utilization of carbohydrates and hinder fat accumulation. Remarkably, when Jinhua pigs were administered C. butyricum, similar alterations in the gut microbiome and host fatness traits were observed, further supporting the potential role of C. butyricum in modulating fatness. Taken together, our findings reveal previously overlooked links between C. butyricum and CAZyme function, providing insight into the basic mechanisms that connect gut microbiome functions to host fatness.

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