Physiological Analysis and Transcriptome Analysis of Asian Honey Bee (Apis cerana cerana) in Response to Sublethal Neonicotinoid Imidacloprid

SIMPLE SUMMARY: In recent decades, there has been serious concern about the decline of honeybees in the world. One of the most debated factors contributing to bee population declines is exposure to pesticides, especially neonicotinoids. The most important Chinese indigenous species, Apis cerana presents a high risk on exposure to neonicotinoids, but few studies have explored the sublethal effects of neonicotinoids on Apis cerana. In this study, we highlight the molecular mechanism underlying the A. cerana toxicological characteristic against imidacloprid, the most commonly detected neonicotinoid in honey samples from Apis cerana. We not only investigated the physiological effects from sublethal doses of imidacloprid, but also identified several genes involved in a general stress response, including metabolism, catalytic activity, and structural molecule activity, response to stimulus, transporter activity, and signal transducer activity, as indicated by the GO analysis. In addition, genes related to the phenylalanine metabolism pathway, FoxO signaling pathway, and mTOR signaling pathway as indicated in the KEGG analysis were significantly up-related in the exposed bees. Overall, this study reveals the short-term sublethal effects of imidacloprid, which may be useful for accurately assessing the toxicity risk of Asian honeybees. ABSTRACT: Asian honey bee (Apis cerana) is the most important Chinese indigenous species, while its toxicological characteristic against neonicotinoids is poorly known. Here, we combined physiological experiments with a genome-wide transcriptome analysis to understand the molecular basis of genetic variation that responds to sublethal imidacloprid at different exposure durations in A. cerana. We found that LC(5) dose of imidacloprid had a negative impact on climbing ability and sucrose responsiveness in A. cerana. When bees were fed with LC(5) dose of imidacloprid, the enzyme activities of P450 and CarE were decreased, while the GSTs activity was not influenced by the pesticide exposure. The dynamic transcriptomic profiles of A. cerana workers exposed to LC(5) dose of imidacloprid for 1 h, 8 h, and 16 h were obtained by high-throughput RNA-sequencing. We performed the expression patterns of differentially expressed genes (DEGs) through trend analysis, and conducted the gene ontology analysis and KEGG pathway enrichment analysis with DEGs in up- and down-regulated pattern profiles. We observed that more genes involved in metabolism, catalytic activity, and structural molecule activity are down-regulated; while more up-regulated genes were enriched in terms associated with response to stimulus, transporter activity, and signal transducer activity. Additionally, genes related to the phenylalanine metabolism pathway, FoxO signaling pathway, and mTOR signaling pathway as indicated in the KEGG analysis were significantly up-related in the exposed bees. Our findings provide a comprehensive understanding of Asian honey bee in response to neonicotinoids sublethal toxicity, and could be used to further investigate the complex molecular mechanisms in Asian honey bee under pesticide stress.