Genomic insights into neonicotinoid sensitivity in the solitary bee Osmia bicornis

Katherine Beadle; Kumar Saurabh Singh; Bartlomiej J. Troczka; Emma Randall; Marion Zaworra; Christoph T. Zimmer; Angela Hayward; Rebecca Reid; Laura Kor; Maxie Kohler; Benjamin Buer; David R. Nelson; Martin S. Williamson; T. G.Emyr Davies; Linda M. Field; Ralf Nauen; Chris Bass

doi:10.1371/journal.pgen.1007903

Genomic insights into neonicotinoid sensitivity in the solitary bee Osmia bicornis

Katherine Beadle, Kumar Saurabh Singh, Bartlomiej J. Troczka, Emma Randall, Marion Zaworra, Christoph T. Zimmer, Angela Hayward, Rebecca Reid, Laura Kor, Maxie Kohler, Benjamin Buer, David R. Nelson, Martin S. Williamson, T. G.Emyr Davies, Linda M. Field, Ralf Nauen, Chris Bass^*

^*Corresponding author for this work

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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.

Original language	English
Article number	e1007903
Journal	PLoS Genetics
Volume	15
Issue number	2
DOIs	https://doi.org/10.1371/journal.pgen.1007903
Publication status	Published - Feb 2019

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10.1371/journal.pgen.1007903

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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., & Bass, C. (2019). Genomic insights into neonicotinoid sensitivity in the solitary bee Osmia bicornis. PLoS Genetics, 15(2), Article e1007903. https://doi.org/10.1371/journal.pgen.1007903

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title = "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.",

author = "Katherine Beadle and Singh, {Kumar Saurabh} and Troczka, {Bartlomiej J.} and Emma Randall and Marion Zaworra and Zimmer, {Christoph T.} and Angela Hayward and Rebecca Reid and Laura Kor and Maxie Kohler and Benjamin Buer and Nelson, {David R.} and Williamson, {Martin S.} and Davies, {T. G.Emyr} and Field, {Linda M.} and Ralf Nauen and Chris Bass",

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AU - Zimmer, Christoph T.

AU - Hayward, Angela

AU - Reid, Rebecca

AU - Kor, Laura

AU - Kohler, Maxie

AU - Buer, Benjamin

AU - Nelson, David R.

AU - Williamson, Martin S.

AU - Davies, T. G.Emyr

AU - Field, Linda M.

AU - Nauen, Ralf

AU - Bass, Chris

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N2 - 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.

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Genomic insights into neonicotinoid sensitivity in the solitary bee Osmia bicornis

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