Superior ability of dietary fiber utilization in obese breed pigs linked to gut microbial hydrogenotrophy

Dietary fiber is widely recognized for its benefits to human health. Individual variations in the ability to degrade dietary fiber are influenced by the gut microbiome that may be associated with the host's metabolic phenotype and genetic diversity. This is exemplified by the distinct fiber digestibility observed in obese (e.g. Meishan) and lean-breed (e.g. Yorkshire) pigs. However, the underlying mechanisms remain unclear. The present study found that with the same diet under the same environment, the obese-type Meishan pigs showed greater dietary fiber digestibility and harbored higher abundances of polysaccharide-degrading bacteria (<i>Bacteroides</i>, <i>Treponema</i>, and <i>Paraprevotella</i>) compared to lean-type Yorkshire pigs. Metatranscriptomic profiling revealed that the elevated presence of <i>Bacteroides</i> contributed to the enrichment of carbohydrate-active enzymes, particularly those degrading arabinoxylan, indicating a preference for arabinoxylan as a substrate in Meishan pigs. Further enzymatic-product measurements, combined with microbial enzyme profiles, validated greater microbial conversion of xylose into short-chain fatty acids (SCFAs) in Meishan pigs. Additionally, higher abundances of hydrogenotrophic microbes (<i>Methanobrevibacter</i> and <i>Blautia</i>) were detected in the Meishan gut, along with the enrichment of methanogenesis and acetogenesis pathways. To determine whether methanogenesis drives inter-breed variation in arabinoxylan degradation, an <i>in vitro</i> experiment using the methanogen inhibitor, 2-bromoethanesulfonate (BES) was performed. The results confirmed that Meishan gut microbiome effectively reduced hydrogen accumulation through methanogenesis, promoting arabinoxylan degradation. Conversely, inhibiting methanogenesis by BES led to hydrogen accumulation, reduced SCFAs, β-xylosidase activity, and <i>Bacteroides</i> abundances. These findings demonstrate that the Meishan pigs have a superior ability of dietary fiber utilization with greater microbial conversion to more SCFAs, which is linked to stronger hydrogenotrophic methanogenesis. This study reinforces the role of gut microbial hydrogenotrophy in dietary fiber utilization in pigs.