Gut microbiota play a role in boosting the mating competitiveness of male Cydia pomonella by mitigating the DNA damage induced by X-ray irradiation

X-ray irradiation is extensively utilized in the sterile insect technique (SIT) program for generating sterile insects. However, irradiation leads to DNA damage, induces random mutations in genes associated with fertility, and disrupts the composition of gut microbiota. Despite achieving sterility at 200 Gy, X-ray irradiation results in reduced mating competitiveness, thereby affecting the efficacy of SIT applications. However, the precise mechanism underlying radiation-induced sterility and decreased mating competitiveness in insects remains ambiguous. In this study, we investigated the effects of X-ray irradiation on DNA damage and repair, as well as the diversity of gut microbiota in Cydia pomonella , managed through X-ray irradiation-based SIT. Upon exposure to 200 Gy, the genomic template stability (GTS) of sterile male C. pomonella decreased significantly to approximately 86.57% of the non-irradiated control, with GTS failing to recover to control levels. Additionally, irradiation triggered the up-regulation of genes involved in DNA damage response and repair. Analysis using 16S rRNA-seq confirmed alterations in the gut microbiota composition following 200 Gy X-ray treatment at the family and genus levels. Notably, replenishing Stenotrophomonas , a prominent constituent of the gut microbiota, demonstrated a notable capacity to elevate the expression levels of crucial damage response genes and repair genes in irradiated individuals compared to the control group, enhancing mating competitiveness of sterilized males. This study shed light on the understanding of the mechanisms underlying sterility induced by X-ray irradiation and underscores the crucial role of gut microbes in aiding hosts in coping with DNA damage and repair resulting from radiation-induced stress. • X-ray cause DNA damage of C.pomonella ; • X-ray activated genes for damage response and repair in the C.pomonella; • X-ray impact gut microbiota structure; • Stenotrophomonas enhances the mating competitiveness of C.pomonella to X-ray irradiation.