Honey bee (Apis mellifera) gut microbiota promotes host endogenous detoxification capability via regulation of P450 gene expression in the digestive tract

Authors: WU, YUQI - Zhejiang University; ZHENG, YUFEI - Zhejiang University; CHEN, YANAN - Zhejiang University; WANG, SHUAI - Zhejiang University; Chen, Yanping - Judy; HU, FU-LIANG - Zhejiang University; ZHENG, HUOQING - Zhejiang University

Submitted to: mBio
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/4/2020
Publication Date: 5/5/2020
Citation: Wu, Y., Zheng, Y., Chen, Y., Wang, S., Chen, Y., Hu, F., Zheng, H. 2020. Honey bee (Apis mellifera) gut microbiota promotes host endogenous detoxification capability via regulation of P450 gene expression in the digestive tract. mBio. 13(4):1201-1212. https://doi.org/10.1111/1751-7915.13579.
DOI: https://doi.org/10.1111/1751-7915.13579

Interpretive Summary: There is growing evidence that gut microbiota comprising different beneficial bacteria species affect honeybee health in many ways. However, the functional role of gut microbiota in honeybees’ responses and detoxification ability against environmental chemicals such as insecticides has yet to be investigated. In the present study, we compared the expression of the genes encoding enzymes involved in pesticide detoxification between the gut-microbiota-deficient worker bees and gut-microbiota-normal worker bees. Our results demonstrated that gut microbiota contribute to bee health through the optimization of detoxification pathways and have a pronounced positive impact on the ability of honeybees to detoxify pesticides. The results from this provide critical insights into the host-microbiome interactions in honeybees and should be of interest to researchers, graduate students, apiary inspectors, and beekeepers worldwide.

Technical Abstract: Gut microbiota affects host physiology in many ways. There are a growing number of studies demonstrating a close relationship between insect gut microbiota and insecticide resistance. However, the contribution of honey bee gut microbiota to host detoxification ability has yet to be investigated. In order to address this question, we compared the expression of the cytochrome P450s (CYPs) genes including CYP6AS1, CYP6AS3, CYP6AS4, CYP6AS10, CYP9Q1, CYP9Q2 and CYP9Q3 that plays an important role in detoxification of chemicals in the midgut and hindgut between gut microbiota deficient (GD) workers and conventional gut community (CV) workers. We measured and compared the mortality rates and the pesticide residue levels of GD and CV workers treated with sublethal dose of thiacloprid or tau-fluvalinate. Our results showed that gut microbiota could promote the expression of cytochrome P450 enzymes (P450s) in the midgut. When treated with pesticide, the mortality rate and the pesticide residue levels of GD workers are significantly higher than those of CV workers. In addition, comparisons between antibiotic-treated workers and un-treated workers demonstrated that antibiotic-induced gut demage leads to attenuated expression of P450s in the midgut. The co-treatment of antibiotics and pesticides leads to reduced survival rate and significantly more pesticide residues in honey bees. Taken together, our results demonstrated that honey bee gut symbiont contributes to bee health through the modification of the host xenobiotic detoxification pathways and revealed a potential negative impact of antibiotics to honey bee health. These findings provided new insights into the host-microbiome interactions and xenobiotic detoxification in honey bees.