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 Nelson, Martin S. Williamson, T. G.Emyr Davies, Linda M. Field, Ralf Nauen, Chris Bass

Research output: Contribution to journalArticle

3 Citations (Scopus)

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 languageEnglish (US)
Article numbere1007903
JournalPLoS genetics
Volume15
Issue number2
DOIs
StatePublished - Feb 1 2019

Fingerprint

Osmia rufa
solitary bees
neonicotinoid insecticides
Bees
bee
genomics
pesticides
thiacloprid
Pesticides
Apoidea
pollinating insects
pesticide
enzymes
enzyme
detoxification
pollinator
cholinergic receptors
Insecticides
insecticide
Apidae

All Science Journal Classification (ASJC) codes

  • Ecology, Evolution, Behavior and Systematics
  • Molecular Biology
  • Genetics
  • Genetics(clinical)
  • Cancer Research

Cite this

Beadle, K., Singh, K. S., Troczka, B. J., Randall, E., Zaworra, M., Zimmer, C. T., ... Bass, C. (2019). Genomic insights into neonicotinoid sensitivity in the solitary bee Osmia bicornis. PLoS genetics, 15(2), [e1007903]. https://doi.org/10.1371/journal.pgen.1007903

Genomic insights into neonicotinoid sensitivity in the solitary bee Osmia bicornis. / Beadle, Katherine; Singh, Kumar Saurabh; Troczka, Bartlomiej J.; Randall, Emma; Zaworra, Marion; Zimmer, Christoph T.; Hayward, Angela; Reid, Rebecca; Kor, Laura; Kohler, Maxie; Buer, Benjamin; Nelson, David; Williamson, Martin S.; Davies, T. G.Emyr; Field, Linda M.; Nauen, Ralf; Bass, Chris.

In: PLoS genetics, Vol. 15, No. 2, e1007903, 01.02.2019.

Research output: Contribution to journalArticle

Beadle, K, Singh, KS, Troczka, BJ, Randall, E, Zaworra, M, Zimmer, CT, Hayward, A, Reid, R, Kor, L, Kohler, M, Buer, B, Nelson, D, Williamson, MS, Davies, TGE, Field, LM, Nauen, R & Bass, C 2019, 'Genomic insights into neonicotinoid sensitivity in the solitary bee Osmia bicornis', PLoS genetics, vol. 15, no. 2, e1007903. https://doi.org/10.1371/journal.pgen.1007903
Beadle K, Singh KS, Troczka BJ, Randall E, Zaworra M, Zimmer CT et al. Genomic insights into neonicotinoid sensitivity in the solitary bee Osmia bicornis. PLoS genetics. 2019 Feb 1;15(2). e1007903. https://doi.org/10.1371/journal.pgen.1007903
Beadle, Katherine ; Singh, Kumar Saurabh ; Troczka, Bartlomiej J. ; Randall, Emma ; Zaworra, Marion ; Zimmer, Christoph T. ; Hayward, Angela ; Reid, Rebecca ; Kor, Laura ; Kohler, Maxie ; Buer, Benjamin ; Nelson, David ; Williamson, Martin S. ; Davies, T. G.Emyr ; Field, Linda M. ; Nauen, Ralf ; Bass, Chris. / Genomic insights into neonicotinoid sensitivity in the solitary bee Osmia bicornis. In: PLoS genetics. 2019 ; Vol. 15, No. 2.
@article{79f39190b7bc4172a0ebb4b8e7f8d53c,
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 David Nelson and Williamson, {Martin S.} and Davies, {T. G.Emyr} and Field, {Linda M.} and Ralf Nauen and Chris Bass",
year = "2019",
month = "2",
day = "1",
doi = "10.1371/journal.pgen.1007903",
language = "English (US)",
volume = "15",
journal = "PLoS Genetics",
issn = "1553-7390",
publisher = "Public Library of Science",
number = "2",

}

TY - JOUR

T1 - Genomic insights into neonicotinoid sensitivity in the solitary bee Osmia bicornis

AU - Beadle, Katherine

AU - Singh, Kumar Saurabh

AU - Troczka, Bartlomiej J.

AU - Randall, Emma

AU - Zaworra, Marion

AU - Zimmer, Christoph T.

AU - Hayward, Angela

AU - Reid, Rebecca

AU - Kor, Laura

AU - Kohler, Maxie

AU - Buer, Benjamin

AU - Nelson, David

AU - Williamson, Martin S.

AU - Davies, T. G.Emyr

AU - Field, Linda M.

AU - Nauen, Ralf

AU - Bass, Chris

PY - 2019/2/1

Y1 - 2019/2/1

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.

AB - 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.

UR - http://www.scopus.com/inward/record.url?scp=85061562980&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85061562980&partnerID=8YFLogxK

U2 - 10.1371/journal.pgen.1007903

DO - 10.1371/journal.pgen.1007903

M3 - Article

C2 - 30716069

AN - SCOPUS:85061562980

VL - 15

JO - PLoS Genetics

JF - PLoS Genetics

SN - 1553-7390

IS - 2

M1 - e1007903

ER -