Genomic variant features of gut microbes among distinct pig populations and identification of microbial variants associated with fatness traits

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The gut microbiota is involved in host metabolism, immunity, and energy homeostasis. Stressors, such as diets and environments, can cause changes in microbial compositions and genomic variations. Here, we performed a population genomic analysis to reveal the genetic landscape of the pig gut microbiome and identified microbial single-nucleotide variants (SNVs) associated with host fatness traits. We characterized genomic variant features of gut microbiota across three pig populations having distinct genetics background and raised in dramatically different environments: wild boars (free-range and natural diets), Tibetan pigs (semi-free, high-altitude, and hypoxic environment), and Duroc pigs (intensive farming, and commercial diets). At the population level, gut microbiome of wild boars harbored the lowest SNV density, but the highest pN/pS ratios, in contrast to the elevated SNV density and recombination rates observed in Duroc and Tibetan pigs. Functional profiles of genes under selection in microbial genomes also differed across populations: purifying selected genes were enriched in the pathway of simple sugar metabolism in Duroc pigs, but secondary bile acid biosynthesis in wild boars, with Tibetan pigs exhibiting an intermediate pattern that included additional flavonoid metabolism pathways. Positively selected genes were involved in carbohydrate metabolism and proteolysis in Duroc pigs, adhesion in wild boars, and mucin-binding functions in Tibetan pigs. To further investigate whether microbial SNVs affected pig fatness traits, we performed an association analysis in well-phenotyped F 6 pigs from a designed mosaic pig population. We identified 11 microbial SNVs in Lactobacillus amylovorus , Limosilactobacillus reuteri , Streptococcus faecavium , and CAG-177 sp003514385 that were significantly associated with pig fatness-related traits. These SNVs were predicted to be involved in energy metabolic enzymes and epigenetic modification. All associations were independent of bacterial abundance, highlighting the value of SNV-based analyses beyond traditional abundance approaches. Our findings revealed distinct genomic signatures of gut microbiota across three pig populations and established a framework for linking microbial genetic variation to host phenotypes, moving beyond taxonomic composition.

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