Gut microbiota in a leaf beetle enhance the toxicity of insecticide Dursban to host

Chemical insecticide application is the most effective strategy for pest control, and the development of highly effective and environment-friendly insecticides and more appropriate application methods has become the focus of research. Insect gut bacteria play a pivotal role in the host's physiological processes and have the potential to cooperate with insecticides to expedite host mortality, although such cases are less frequently reported. Here, we investigated the survival difference between conventionally-reared (CR), which possess gut microbiota, and germ-free (GF) larvae of the leaf beetle Plagiodera versicolora treated with the organophosphorus insecticide Dursban. Results showed gut bacteria accelerated the mortality of P. versicolora larvae. Dursban treatment caused a dynamic change in the gut microbiota of P. versicolora with a significant reduction in bacterial diversity, a significant increase in the relative abundance of Pantoea and Pseudomonas, and the entry of gut bacteria into the hemocoel. The reintroduction of gut bacterial isolates Pseudomonas aeruginosa and Pantoea anthophila to GF larvae further enhanced mortality upon Dursban exposure. Transcriptome analysis indicated that gut bacteria significantly influenced the gene expression profiles of P. versicolora larvae upon Dursban exposure. Further RT-qPCR results showed that the expression levels of immune gene Toll in CR larvae were upregulated compared to GF larvae under Dursban exposure, but the transcript levels of PPO and PGRP1 were downregulated, indicating that the disruption of the immune system in Dursban-treated CR larvae was involved in the acceleration of mortality. The findings will enhance our understanding of insect gut bacterial function and provide insights for pest control strategies combining gut bacteria with chemical insecticides. •Gut microbiota accelerated the mortality of Plagiodera versicolora upon Dursban exposure.•Dursban treatment caused a dynamic change in the gut microbiota of P. versicolora.•Reintroducing pathogenic gut bacteria to GF larvae enhanced mortality upon Dursban exposure.•The disruption of the immune system in Dursban-treated CR larvae was involved in accelerating mortality.