A multiomics analysis of antioxidant and neurotransmitter disorder in honey bees caused by the bioinsecticide, Spinosad.

The natural origin and biodegradable nature of bioinsecticides endow them with promising application potential. Spinosad, a major microbial bioinsecticide, has been detected in nectar source plants. However, the impact of bioinsecticides on honey bee gut health has not been sufficiently evaluated. This study comprehensively assessed the effects of three Spinosad concentrations (0.1, 0.25, and 0.5 mg/L) on the apparent gut health of 7-day-old adult honey bee workers (Apis cerana Fabricius). Following two weeks of oral exposure to Spinosad, there was no significant decline in honey bee survival or sucrose consumption, nor were there significant alterations in the composition of the midgut microbiota. However, transcriptomic, metabolomic, and their integrated analyses revealed significantly elevated oxiglutatione levels (direct product of glutathione after oxidation). Genes that redirect glutathione into alternative metabolites (LOC107999471 (Anpepl1)), and not into oxiglutatione and LOC133665765 (glutathione hydrolase light chain 1-like, GGTLC1) were significantly up-regulated. Spinosad significantly reduced the antioxidant, uric acid, and the neurotransmitter, histamine. Correlation analysis between metabolites and gut microbiota indicated that the beneficial Gilliamella and Bombella preserved stability under Spinosad exposure. This study comprehensively evaluated the toxicity of Spinosad to honey bees from a gut health, key microbe, metabolites, and genes perspective, and provides insights for protecting non-target insects such as honey bees.