Host Gender and Androgen Levels Regulate Gut Bacterial Taxa in Pigs Leading to Sex-Biased Serum Metabolite Profiles

Gut microbiota regulates host metabolism and immunity. The phylogenetic composition of gut microbiota is influenced by diverse factors that include host gender. In this study, the effects of gender on gut microbial composition and its subsequent influence on serum metabolites in pigs were evaluated. The bacterial composition of feces samples was determined by 16S rRNA sequencing in 293 pure-bred Duroc pigs (108 gilts and 185 entire boars) and 64 validated pigs from an eight-breed mosaic F6 population. Twenty-eight F6 boars were castrated at 80 days of age to evaluate the effects of androgen on gut microbial composition. Untargeted serum metabolite features were determined in 45 boars and 26 gilts by an ultra-performance liquid chromatography coupled with quadrupole time-of-flight mass spectrometry (UPLC-QTOF/MS). The study observed an obvious influence of host gender on the gut microbial composition and identified numerous sex-biased bacterial taxa. These included Veillonellaceae, Roseburia, Bulleidia and Escherichia which were of higher abundance in boars, and Treponema and Bacteroides which were over-represented in gilts. Castration significantly shifted the fecal microbiota composition of the boars towards that of gilts. The predicted functional pathways of the gut microbiome related to obesity and energy harvest were enriched in gilts, and positively associated with gilt-enriched bacteria. Functional pathways related to peptidases and carbohydrate metabolism were enriched in boars and positively associated with boar-enriched bacteria. Serum metabolites related to androgen and cresol metabolism were identified as sex-biased metabolites. Correlation analysis between serum metabolites and sex-biased bacteria identified that the serum concentration of androgen-related metabolites positively correlated with Bulleidia and Escherichia, but negatively associated with Treponema, suggesting a significant interaction between gut microbiota and host sex hormone metabolism. These results offer basic knowledge of how host gender and gut microbiota influence host metabolism.