Unravelling the molecular determinants of bee sensitivity to neonicotinoid insecticides

A - Papers appearing in refereed journals

Manjon, C., Troczka, B. J., Zaworra, M., Beadle, K., Randall, E., Hertlein, G., Singh, K. S., Zimmer, C. T., Homem, R. A., Lueke, B., Reid, R., Kor, L., Kohler, M., Benting, J., Williamson, M. S., Davies, T. G. E., Field, L. M., Bass, C. and Nauen, R. 2018. Unravelling the molecular determinants of bee sensitivity to neonicotinoid insecticides. Current Biology. 27 (7), p. 1137–1143. https://doi.org/10.1016/j.cub.2018.02.045

AuthorsManjon, C., Troczka, B. J., Zaworra, M., Beadle, K., Randall, E., Hertlein, G., Singh, K. S., Zimmer, C. T., Homem, R. A., Lueke, B., Reid, R., Kor, L., Kohler, M., Benting, J., Williamson, M. S., Davies, T. G. E., Field, L. M., Bass, C. and Nauen, R.
Abstract

The impact of neonicotinoid insecticides on the health of bee pollinators is a topic of intensive research and considerable current debate. As insecticides, certain neonicotinoids, i.e., N-nitroguanidine compounds such as imidacloprid and thiamethoxam, are as intrinsically toxic to bees as to the insect pests they target. However, this is not the case for all neonicotinoids, with honeybees orders of magnitude less sensitive to N-cyanoamidine compounds such as thiacloprid. Although previous work has suggested that this is due to rapid metabolism of these compounds, the specific gene(s) or enzyme(s) involved remain unknown. Here, we show that the sensitivity of the two most economically important bee species to neonicotinoids is determined by cytochrome P450s of the CYP9Q subfamily. Radioligand binding and inhibitor assays showed that variation in honeybee sensitivity to N-nitroguanidine and N-cyanoamidine neonicotinoids does not reside in differences in their affinity for the receptor but rather in divergent metabolism by P450s. Functional expression of the entire CYP3 clade of P450s from honeybees identified a single P450, CYP9Q3, that metabolizes thiacloprid with high efficiency but has little activity against imidacloprid.We demonstrate that bumble bees also exhibit profound differences in their sensitivity to different neonicotinoids, and we identify CYP9Q4 as a functional ortholog of honeybee CYP9Q3 and a key metabolic determinant of neonicotinoid sensitivity in this species. Our results demonstrate that bee pollinators are equipped with biochemical defense systems that define their sensitivity to insecticides and this knowledge can be leveraged to safeguard bee health.

Year of Publication2018
JournalCurrent Biology
Journal citation27 (7), p. 1137–1143
Digital Object Identifier (DOI)https://doi.org/10.1016/j.cub.2018.02.045
PubMed ID29576476
Web address (URL)http://www.cell.com/current-biology/fulltext/S0960-9822(18)30230-6
Open accessPublished as ‘gold’ (paid) open access
FunderBayer Crop Science
Funder project or codeBBSRC Strategic Programme in Smart Crop Protection
Publisher's version
Accepted author manuscript
Output statusPublished
Publication dates
Online22 Mar 2018
Publication process dates
Accepted16 Feb 2018
PublisherCell Press
Copyright licenseCC BY
ISSN0960-9822

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