Natural sex reversal imparts permanent compositional changes to the swamp eel gonadal microbiome

Microbial communities are increasingly recognized for their essential roles in the reproductive system. However, the microbial communities in healthy gonads-neither in the ovary nor the testis-have not been extensively explored, particularly with respect to sex differentiation. Sex reversal is a unique mode of sex differentiation that is a well-documented phenomenon in various animal species, with the swamp eel (Monopterus albus) being a notable example of a hermaphroditic species that undergoes natural female-to-male sex reversal. Thus, swamp eel offers a robust system for exploring gonad microbial communities and their biological and functional significance.

Our study revealed a living microbial community in the gonads of healthy swamp eel, with microbial loads comparable to those found in three distinct niches: gut, skin, and blood. The gonad microbial communities shared > 55% of their diversity with those in the gut and blood. We focused on the niche-specific differences in microbial communities, particularly between the ovary and testis. After isolating and injecting the ovarian-dominant bacteria Bacillus, we observed significant microbial dysbiosis and metabolic responses in the ovary. These changes were primarily reflected in the altered abundance of the ovarian microbiota involved in amino acid and lipid metabolism, which may contribute to ovarian function in swamp eel. Additionally, Bacillus inhibited sperm motility, reduced sperm count, and induced inflammatory responses in the testes of male swamp eel. These findings highlight the crucial role of bacteria in the sexual transition from the ovary to the testis and in gametogenesis.

Characterizing the microbial composition and distribution in the gonads is crucial for understanding the role of the reproductive microbiome in hermaphroditic species and during sex reversal. Our findings first indicate that ovarian-dominant bacterial communities contribute to maintaining ovarian function while inhibiting testicular function in swamp eel, further suggesting that microbial communities are involved in the process of sex reversal. Video Abstract.