Genomic insights into neonicotinoid sensitivity in the solitary bee Osmia bicornis

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.

Are honeybees suitable surrogates for use in pesticide risk assessment for non‐Apisbees?

“…pyrethroids, N ‐cyanoamidine neonicotinoids, organophosphorus compounds) and plant toxins such as flavonoids, with solitary species ( Osmia spp.) using analogues from a related CYP family (CYP9BU) . It has also been established that receptor composition is pivotal in determining the binding strength and consequently the toxicity of certain compounds.…”

“…using analogues from a related CYP family (CYP9BU). 40 It has also been established that receptor composition is pivotal in determining the binding strength and consequently the toxicity of certain compounds. This has been put forward as a likely explanation for why insects are much more susceptible than mammals to neonicotinoids.…”

Extrapolating acute bee sensitivity to insecticides using a phylogenetically informed interspecies scaling framework

“…In addition to this physiological explanation there is some genomic evidence suggesting that A. mellifera, and by extension likely additional members of the Apis genus, lack some substantial detoxifying enzymes (including glutathione-Stransferases, cytochrome P450 monooxygenases and carboxyl/cholinesterases) which are essential for detoxifying a range of xenobiotics including insecticides [53]. This line of evidence is supported by recent findings which pinpoint members of the P450 family as key determinates of bee sensitivity to different insecticides [22,35,36].…”

“…All reported substance specific LD50 were categorized according to their mode of action (MoA [30]) and the four currently most commonly used insecticides were selected for further analysis [31][32][33][34]. The neonicotinoids were split between cyano-(c-) and nitro-(n-) substituted neonicotinoids, as it is known that bee species' responses can drastically differ between these two classes [22,35,36]. This resulted in five insecticide classes for analysis: acetylcholinesterase inhibitors (AChE-inhibitors), pyrethroids, cand n-substituted neonicotinoids and organochlorines.…”

Transcriptome analysis reveals nutrition‐ and age‐related patterns of gene expression in the fat body of pre‐overwintering bumble bee queens

“…One of the best‐studied functions of cytochrome P450 monooxygenases in insects is their role in meeting the challenge of pesticide exposure, as they can metabolize nearly all insecticides that have been examined thus far (Bergé, Feyereisen, & Amichot, ; Scott, ). Previous studies suggest P450 genes have generalized functions in detoxification in insects, including bees, such that they can directly detoxify xenobiotics/insecticides and are also key detoxification enzymes that mediate synergistic interactions between acaricides/insecticides and fungicides (Beadle et al, ; Berenbaum & Johnson, ; Manjon et al, ; Mao, Schuler, & Berenbaum, ). Bumble bees have a functional set of P450 enzymes, although they are depauperate relative to most other insects with full genome sequences available (Sadd et al, ; Xu, Strange, Welker, & James, ).…”