The neonicotinoid thiacloprid causes transcriptional alteration of genes associated with mitochondria at environmental concentrations in honey bees

Karl Fent,Michael Schmid,Timm Hettich,Simon Schmid

doi:10.1016/j.envpol.2020.115297

Abstract

Thiacloprid is widely used in agriculture and may affect pollinators. However, its molecular effects are poorly known. Here, we report the global gene expression profile in the brain of honey bee foragers assessed by RNA-sequencing. Bees were exposed for 72 h to nominal concentrations of 25 and 250 ng/bee via sucrose solution. Determined residue concentrations by LC-MS/MS were 0.59 and 5.49 ng/bee, respectively. Thiacloprid exposure led to 5 and 71 differentially expressed genes (DEGs), respectively. Nuclear genes encoding mitochondrial ribosomal proteins and enzymes involved in oxidative phosphorylation, as well as metabolism enzymes and transporters were altered at 5.49 ng/bee. Kyoto Encylopedia of Genes and Genomes (KEGG) analysis revealed that mitochondrial ribosome proteins, mitochondrial oxidative phosphorylation, pyrimidine, nicotinate and nicotinamide metabolism and additional metabolic pathways were altered. Among 21 genes assessed by RT-qPCR, the transcript of farnesol dehydrogenase involved in juvenile hormone III synthesis was significantly down-regulated. Transcripts of cyp6a14-like and apolipophorin-II like protein, cytochrome oxidase (cox17) and the non-coding RNA (LOC102654625) were significantly up-regulated at 5.49 ng/bee. Our findings indicate that thiacloprid causes transcriptional changes of genes prominently associated with mitochondria, particularly oxidative phosphorylation. This highlight potential effects of this neonicotinoid on energy metabolism, which may compromise bee foraging and thriving populations at environmentally relevant concentrations.

Highlights

The documented decline of insects (Hallmann et al, 2017) and arthropods biomass and diversity (Seibold et al, 2019) are of major concern, which holds for bees (Lee et al, 2015; Ollerton et al, 2014)
Bee decline compromises pollination (Cameron et al, 2011; Goulson et al, 2015; Grab et al, 2019) and has many causes (Goulson et al, 2015) including loss of plant biodiversity associated with intensified farming, impacts of pathogens and pesticides
Insects are exposed to numerous agricultural pesticides (David et al, 2016) including neonicotinoids (Mullin et al, 2010; Sanchez-Bayo and Goka, 2014)

Summary

Introduction

The documented decline of insects (Hallmann et al, 2017) and arthropods biomass and diversity (Seibold et al, 2019) are of major concern, which holds for bees (Lee et al, 2015; Ollerton et al, 2014). Direct exposure of bees may cause acute toxicity and chronic effects to the nervous system (Decourtye et al, 2004), immune system (Di Prisco et al, 2013) or on energy allocation (Christen et al, 2019a). Their neurotoxicity may compromise memory and orientation as demonstrated for thiacloprid that reduced homing success of honey bees (Tison et al, 2016). Neonicotinoid insecticides may harm bee populations (Henry et al, 2012; Rundlo€f et al, 2015; Tsvetkov et al, 2017)

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