Abstract
The interactions between insects and their bacterial symbionts are shaped by a variety of abiotic factors, including temperature. As global temperatures continue to break high records, a great deal of uncertainty surrounds how agriculturally important insect pests and their symbionts may be affected by elevated temperatures, and its implications for future pest management. In this study, we examine the role of bacterial symbionts in the brown planthopper Nilaparvata lugens response to insecticide (imidacloprid) under different temperature scenarios. Our results reveal that the bacterial symbionts orchestrate host detoxification metabolism via the CncC pathway to promote host insecticide resistance, whereby the symbiont-inducible CncC pathway acts as a signaling conduit between exogenous abiotic stimuli and host metabolism. However, this insect-bacterial partnership function is vulnerable to high temperature, which causes a significant decline in host-bacterial content. In particular, we have identified the temperature-sensitive Wolbachia as a candidate player in N. lugens detoxification metabolism. Wolbachia-dependent insecticide resistance was confirmed through a series of insecticide assays and experiments comparing Wolbachia-free and Wolbachia-infected N. lugens and also Drosophila melanogaster. Together, our research reveals elevated temperatures negatively impact insect-bacterial symbiosis, triggering adverse consequences on host response to insecticide (imidacloprid) and potentially other xenobiotics.
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Acknowledgements
This work was supported by the National Natural Science Foundation of China (31871991 and 32072462), the National Key Research and Development Program of China (2016YFD0200500), the Natural Science Foundation of Hubei Province (2019CFB471), and the Fundamental Research Funds for the Central Universities (2662018JC049). We would like to thank Prof. Xiaoyue Hong from Nanjing Agricultural University, Nanjing for providing Wolbachia-infected (WI) and Wolbachia-free (WU) N. lugens. We would like to thank Prof. Yufeng Wang from Central China Normal University for providing Wolbachia-infected (Dmel wMel) and Wolbachia-free (Dmel wMel T) D. melanogaster. We also would like to acknowledge Dr. Jing Zhao and Dr. Kangsheng Ma for critical reading and suggestions for improvement of the manuscript.
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H.W. and Y.Z. designed the experiments. Y.Z., T.C., Z.R., Y.L., M.Y., and Y.C. performed the experiments. Y.Z., C.Y., S.H., and J.L. analyzed the data and generated figures. Y.Z., A.W., and H.W. wrote the paper. All authors read and approved the final manuscript.
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Zhang, Y., Cai, T., Ren, Z. et al. Decline in symbiont-dependent host detoxification metabolism contributes to increased insecticide susceptibility of insects under high temperature. ISME J 15, 3693–3703 (2021). https://doi.org/10.1038/s41396-021-01046-1
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DOI: https://doi.org/10.1038/s41396-021-01046-1
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