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

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Abstract

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.

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (31871991), the Natural Science Foundation of Hubei Province (2019CFB471) and the Fundamental Research Funds for the Central Universities (2662018JC049).

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HW, JHL and SH conceived and designed the experiments. TT, YHZ and TWC conducted the experiments. XQD, CYL and JML analyzed the data. HW, TT and YHZ wrote the manuscript. All authors read, corrected, and approved the manuscript.

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Correspondence to Hu Wan.

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The authors declare that they have no conflict of interest.

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This article does not contain any studies with human participants or animals performed by any of the authors.

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Communicated by Emmanouil Roditakis.

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Tang, T., Zhang, Y., Cai, T. et al. Antibiotics increased host insecticide susceptibility via collapsed bacterial symbionts reducing detoxification metabolism in the brown planthopper, Nilaparvata lugens. J Pest Sci 94, 757–767 (2021). https://doi.org/10.1007/s10340-020-01294-8

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  • DOI: https://doi.org/10.1007/s10340-020-01294-8

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