Microbiota contribute to regulation of the gut-testis axis in seasonal spermatogenesis.

Seasonal breeding is an important adaptive strategy for animals. Recent studies have highlighted the potential role of the gut microbiota in reproductive health. However, the relationship between the gut microbiota and reproduction in seasonal breeders remains unclear. In this study, we selected a unique single food source animal, the flying squirrel (Trogopterus xanthipes), as a model organism for studying seasonal breeding. By integrating transcriptomic, metabolomic, and microbiome data, we comprehensively investigated the regulation of the gut-metabolism-testis axis in seasonal breeding. Here, we demonstrated a significant spermatogenic phenotype and highly active spermatogenic transcriptional characteristics in the testes of flying squirrels during the breeding season, which were associated with increased polyamine metabolism, primarily involving spermine and γ-amino butyric acid. Moreover, an enrichment of Ruminococcus was observed in the large intestine during the breeding season and may contribute to enhanced methionine biosynthesis in the gut. Similar changes in Ruminococcus abundance were also observed in several other seasonal breeders. These findings innovatively revealed that reshaping the gut microbiota regulates spermatogenesis in seasonal breeders through polyamine metabolism, highlighting the great potential of the gut-testis axis in livestock animal breeding and human health management.