Genomic insight into neonicotinoid sensitivity in the solitary bee Osmia bicornis

A - Papers appearing in refereed journals

Beadle, K., Singh, K. S., Troczka, B. J., Randall, E., Zaworra, M., Zimmer, C. T., Hayward, A., Reid, R., Kor, L., Kohler, M., Buer, B., Nelson, D. R., Williamson, M. S., Davies, T. G. E., Field, L. M., Nauen, R. and Bass, C. 2019. Genomic insight into neonicotinoid sensitivity in the solitary bee Osmia bicornis. PLOS Genetics. 15 (2), p. e1007903.

AuthorsBeadle, K., Singh, K. S., Troczka, B. J., Randall, E., Zaworra, M., Zimmer, C. T., Hayward, A., Reid, R., Kor, L., Kohler, M., Buer, B., Nelson, D. R., Williamson, M. S., Davies, T. G. E., Field, L. M., Nauen, R. and Bass, C.
Abstract

The impact of pesticides on the health of bee pollinators is determined in part by the capacity of bee detoxification systems to convert these compounds to less toxic forms. For example, recent work has shown that cytochrome P450s of the CYP9Q subfamily are critically important in defining the sensitivity of honey bees and bumblebees to pesticides, including neonicotinoid insecticides. However, it is currently unclear if solitary bees have functional equivalents of these enzymes with potentially serious implications in relation to their capacity to metabolise certain insecticides. To address this question, we sequenced the genome of the red mason bee, Osmia bicornis, the most abundant and economically important solitary bee species in Central Europe. We show that O. bicornis lacks the CYP9Q subfamily of P450s but, despite this, exhibits low acute toxicity to the N-cyanoamidine neonicotinoid thiacloprid. Functional studies revealed that variation in the sensitivity of O. bicornis to N-cyanoamidine and N-nitroguanidine neonicotinoids does not reside in differences in their affinity for the nicotinic acetylcholine receptor or speed of cuticular penetration. Rather, a P450 within the CYP9BU subfamily, with recent shared ancestry to the Apidae CYP9Q subfamily, metabolises thiacloprid in vitro and confers tolerance in vivo. Our data reveal conserved detoxification pathways in model solitary and eusocial bees despite key differences in the evolution of specific pesticide-metabolising enzymes in the two species groups. The discovery that P450 enzymes of solitary bees can act as metabolic defence systems against certain pesticides can be leveraged to avoid negative pesticide impacts on these important pollinators.

Year of Publication2019
JournalPLOS Genetics
Journal citation15 (2), p. e1007903
Digital Object Identifier (DOI)doi:10.1371/journal.pgen.1007903
PubMed ID30716069
PubMed Central IDPMC6375640
Web address (URL)https://doi.org/10.1371/journal.pgen.1007903
Open accessPublished as ‘gold’ (paid) open access
FunderBayer Crop Science
BBSRC Industrial Strategy Challenge
Biotechnology and Biological Sciences Research Council
European Research Council
Funder project or codeBBSRC Strategic Programme in Smart Crop Protection
Publisher's version
Output statusPublished
Publication dates
Online04 Feb 2019
Publication process dates
Accepted17 Dec 2018
Copyright licenseCC BY
PublisherPublic Library of Science (PLOS)
ISSN1553-7404

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