Antibiotics increased host insecticide susceptibility via collapsed bacterial symbionts reducing detoxification metabolism in the brown planthopper, Nilaparvata lugens

Symbionts participate in various physiological activities of their insect hosts, including detoxification metabolism. Emerging evidence has revealed that the bacterial symbiont Arsenophonus is involved in insecticide detoxification metabolism of Nilaparvata lugens, which harbors diverse symbionts. However, it is still unknown whether other bacterial symbionts have a functional role in this process. This study showed that pretreatment with antibiotics significantly increased N. lugens susceptibility to imidacloprid, chlorpyrifos, and clothianidin, and the detoxifying enzyme activities of the cytochrome P450 enzyme (P450) and glutathione S-transferase (GST) were significantly inhibited. Notably, the P450 genes NlCYP6ER1 and NlCYP4CE1, which are related to imidacloprid metabolism, were dramatically downregulated in ciprofloxacin- and tetracycline-pretreated N. lugens, respectively. Furthermore, the expression levels of various detoxifying genes (GSTs and P450s) were significantly positively correlated with Wolbachia, Arsenophonus, Acinetobacter, and Staphylococcus. These results indicated that bacterial symbionts may affect insecticide metabolism by regulating the expression of the insect host’s GST and P450 genes, and provide a foundation for further study on the mechanism of symbiont-mediated host detoxification metabolism in insect pests.