Microbiome variation correlates with the insecticide susceptibility in different geographic strains of a significant agricultural pest, Nilaparvata lugens

Microbiome variation correlates with the insecticide susceptibility in different geographic strains of a significant agricultural pest, Nilaparvata lugens

The brown planthopper, Nilaparvata lugens is currently one of the most destructive pests in rice production, and its overbreeding seriously restricts the safe, green, and high-quality production of rice in China. This pest also has serious resistance problems to multiple insecticides: the cumulative number of resistance events reported worldwide reached 453, ranking first among food crop pests (APRD, 2022). Having migrated from Southeast Asia to China and other countries every year, this insect is exposed to different insecticides, resulting in geographical differences in resistance profiles.

Before that, our group completed an ambitious task: we carried out decades of monitoring in central China and revealed the change process of resistance of brown planthopper to different insecticides. We started with metabolic resistance and found that insecticide resistance of N. lugens is dependent on the expression of cytochrome P450 (P450) genes, which include NlCYP6ER1, a key P450 gene that can mediate resistance to multiple insecticides including imidacloprid, nitenpyram, dinotefuran, thiamethoxam, clothianidin, and sulfoxaflor.

However, a growing number of studies suggest that symbiotic bacteria of N. lugens play a crucial role in many resistance problems. For example, previous research found that Wolbachia can affect the sensitivity of N. lugens to insecticide by regulating the expression of P450 detoxification enzyme genes. In addition, another important symbiotic bacterium Arsenophonus of N. lugens has the potential for the similar phenomenon, but the mechanism has not been clarified.

This time, we explore the correlation between host genetics background, microbiome composition, gene expression, and insecticide resistance profiles of nine N. lugens field strains collected from different geographical locations and identify significant environmental abiotic factors that may predict these differences.

Our results reveal insecticide susceptibility phenotypes are poorly dependent on host genetics background but associated with multiple bacteria and corresponding detoxifying gene expressions of N. lugens. We further demonstrate that several environmental abiotic factors correlated with the variation in abundance of these key microbes. We expect there would be variations across years that justify our future work to sample multiple years. Nevertheless, our findings provide new insights into the heterogeneity of insecticide resistance in field insect populations in the context of potential microbiome-host-environment relationships. As a forward-looking work, this study provides many potential research objects, like Acinetobacter soli, Arsenophonus, and Staphylococcus sciuri. More studies focusing on these symbiotic bacteria of N. lugens from our group are on the way to address resistance questions to insecticides.

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