Abstract

Insecticides are thought to be among the major factors contributing to current declines in bee populations. However, detoxification mechanisms in healthy, unstressed honey bees are poorly characterised. Alkaloids are naturally encountered in pollen and nectar, and we used nicotine as a model compound to identify the mechanisms involved in detoxification processes in honey bees. Nicotine and neonicotinoids have similar modes of action in insects. Our metabolomic and proteomic analyses show active detoxification of nicotine in bees, associated with increased energetic investment and also antioxidant and heat shock responses. The increased energetic investment is significant in view of the interactions of pesticides with diseases such as Nosema spp which cause energetic stress and possible malnutrition. Understanding how healthy honey bees process dietary toxins under unstressed conditions will help clarify how pesticides, alone or in synergy with other stress factors, lead to declines in bee vitality.

Highlights

  • The honey bee Apis mellifera is an ecologically and economically important pollinator species worldwide

  • Our analysis indicated an increase in phase I and phase II detoxification processes accompanied by an increase in energy metabolism, glutathione anabolism, lipid metabolism and protein synthesis, as well as increased abundance of proteins that function as part of the cellular heat shock and oxidative stress responses

  • Consumed nicotine is oxidised to less toxic metabolites, cotinine and cotinine N-oxide, by phase I detoxification enzymes, most likely constitutively expressed CYP6 or CYP9 enzymes; followed by phase II conjugation with glutathione catalysed by glutathione S-transferase Delta isoform 1 (GSTD1)

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Summary

Introduction

The honey bee Apis mellifera is an ecologically and economically important pollinator species worldwide. Most acute and chronic toxicity studies have been performed under laboratory conditions as semi-field and field studies assessing toxicity are challenging (controlled multifactor experiments at the landscape scale are very hard to conduct)[5,6] As a result it is not yet clear how much neonicotinoid-containing nectar and pollen is collected and stored in bee hives[7], or how much can be tolerated on a colony level[4,5]. Several studies have demonstrated the involvement of the P450-, GST- or COE-enzyme families in pesticide and secondary metabolite detoxification in honey bees[13,14,15,16,17,18]. Even though we are able to link specific enzymes or enzyme families to honeybee detoxification processes, the overall protection mechanisms that allow these insects to tolerate the variety of potentially toxic secondary metabolites and pesticides encountered in floral nectars and pollen remain largely unknown

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