RawData_Riptortus_SFA1_MEPdetox.xlsx

Insecticide resistance is one of the most serious problems in contemporary agriculture and public health. Although recent studies revealed that insect gut symbionts contribute to resistance, the symbiont-mediated detoxification process remains unclear. Here we report the <i>in vivo</i> detoxification process of an organophosphorus insecticide, fenitrothion, in the bean bug <i>Riptortus pedestris</i>. Using transcriptomics and reverse genetics, we reveal that gut symbiotic bacteria degrade this insecticide through a horizontally acquired insecticide-degrading enzyme into the non-insecticidal but bactericidal compound 3-methyl-4-nitrophenol, which is subsequently excreted by the host insect. This integrated “host-symbiont reciprocal detoxification relay” enables the simultaneous maintenance of symbiosis and efficient insecticide degradation. We also find that the symbiont-mediated detoxification process is analogous to the insect genome-encoded fenitrothion detoxification system present in other insects. Our findings highlight the capacity of symbiosis, combined with horizontal gene transfer in the environment, as a powerful strategy for an insect to instantly eliminate a toxic chemical compound, which could play a critical role in the human-pest arms race.

杀虫剂抗性是当代农业与公共卫生领域最为严峻的问题之一。尽管近期研究证实昆虫肠道共生菌可参与杀虫剂抗性的形成，但共生菌介导的解毒过程仍不明晰。本研究以点蜂缘蝽（*Riptortus pedestris*）为研究对象，报道了其体内（in vivo）有机磷杀虫剂杀螟硫磷（fenitrothion）的解毒过程。借助转录组学（transcriptomics）与反向遗传学（reverse genetics）技术，本研究发现肠道共生菌可通过水平转移获得的杀虫降解酶，将该杀虫剂降解为无杀虫活性但具杀菌活性的3-甲基-4-硝基苯酚（3-methyl-4-nitrophenol），随后由宿主昆虫排出体外。这种整合的"宿主-共生菌双向解毒接力"机制，可在维持共生关系的同时实现高效的杀虫剂降解。此外，本研究发现共生菌介导的解毒过程与其他昆虫体内由基因组编码的杀螟硫磷解毒系统具有相似性。本研究结果表明，共生作用结合环境中的水平基因转移（horizontal gene transfer），可使昆虫快速清除有毒化学物质，这一策略在人类与害虫的军备竞赛中可能发挥关键作用。