Assessing the effects of imidacloprid exposure on the microbiota of Binodoxys communis (Hymenoptera: Braconidae) and gene expression

Imidacloprid is a potent neonicotinoid insecticide that exerts control over cotton aphids. Binodoxys communis is the predominant parasitic threat to cotton aphids, serving as a crucial biological means to control cotton aphids. Imidacloprid has been Sprayed to control cotton aphids, but it also causes toxic effects on the natural enemies of cotton aphids, such as parasitic wasps, Binodoxys communis. However, the sublethal impact of imidacloprid on parasitic antagonists has remained unclear. This study sought to investigate the sublethal effects of imidacloprid on B. communis at the biological phenotype and transcriptional level, as well as the impact of imidacloprid on the microbial composition in the B. communis. Our research indicated that the sublethal dosages of imidacloprid imparted significant biologic adverse impacts on B. communis, including extended larval and pupal stages, as well as reduced parasitism and emergence rates. Following treatment with imidacloprid, transcriptomic analysis identified 1263 significantly differentially expressed genes. These differentially expressed genes were predominantly annotated in metabolic routes, and the annotated genes mainly belong to the fatty acid metabolism pathway, the carbon metabolism pathway, and protein processing in the endoplasmic reticulum pathway. 16S rDNA sequencing results showed significant changes in the composition of the microbial community in B. communis after exposure to imidacloprid. A total of 14 bacteria exhibiting the highest abundance in parasitic wasps were found, and the microbiota abundance of Akkermansia, Bacteroides, Streptomyces, Helicobacter, and Prevotellaceae UCG_001 was noticeably reduced, while Lactobacillus, Escherichia Shigella, Ligilactobacillus, Lachnospiraceae, Rikenellaceae RC9_gut_group, Erysipelatoclostridium, Acinetobacter, Enterococcus, and Aquabacterium were significantly elevated. By evaluating the enrichment pathways of microbial functions, it was found that the microbial functions with significant changes in proportion were mainly annotated to the carbon, fatty acid, and amino acid (aa) metabolic pathways, which was consistent with the transcriptome sequencing results. This finding mirrored transcriptome analysis results. According to transcriptomics analysis and 16S rDNA sequencing data, imidacloprid limits changes in metabolic pathways of B. communis, including fatty acid metabolism, impacting the development and parasitic competence of B. communis. Accordingly, the gene expression linked to detoxification and the cytochrome P450 gene family was significantly elevated at 1 h and significantly declined after three days.