Age-related succession of the gut microbiome drives ovarian function decline in laying hens

The precipitous decline in egg production and the deterioration of egg quality induced by aging in laying hens pose significant challenges to the poultry industry; however, the underlying systemic mechanisms remain incompletely elucidated. This study aimed to comprehensively delineate the trajectory of ovarian function decline during the aging of laying hens and to explore the underlying mechanisms involving age-related intestinal injury and the succession of the intestinal microbiome. Laying hens at the peak, mid, and late laying periods were utilized as the experimental models. The results showed that with the increase of age, the production performance of laying hens decreased significantly, the follicle reserve was exhausted, and the secretion of reproductive hormones was significantly reduced, and the expression of key steroid synthases and hormone receptors was significantly down-regulated. Furthermore, severe oxidative stress and inflammatory responses were observed in the ovaries during the late laying period, which subsequently triggered ovarian cell apoptosis. Concurrently, the normal intestinal architecture and physical barrier function were compromised in aging hens, evidenced by a significant downregulation of tight junction proteins and accompanied by marked intestinal dysbiosis. Moreover, aging induced profound alterations in the intestinal microbial community. The late laying period was characterized by a reduced abundance of beneficial bacteria, including Parabacteroides and Lactobacillus, alongside a substantial enrichment of pathogenic taxa such as Helicobacter. In order to verify whether intestinal microbes are involved in regulating ovarian function, a fecal microbiota transplantation (FMT) experiment was conducted in this study. The FMT results indicated that receiving fecal microbiota from peak-laying donors effectively ameliorated the ovarian condition and alleviated ovarian functional decline in aged recipient hens, thereby confirming the regulatory role of the gut microbiota. In conclusion, by delineating ovarian functional degradation, systematically evaluating age-related intestinal tissue damage and microbiota succession, and revealing the potential link between age-associated gut microbes and core indicators of reproductive decline, this study provides comprehensive insights into hen aging. Importantly, the FMT trial substantiates the regulatory effect of the gut microbiota on ovarian aging, offering a crucial theoretical basis for targeting gut microecology to delay reproductive senescence and prolong the laying cycle in poultry.