Thiamethoxam exposure deregulates short ORF gene expression in the honey bee and compromises immune response to bacteria

Pâmela Decio,Pinar Ustaoglu,Nigel Mongan,Osmar Malaspina,Kamila Derecka,Thaisa C. Roat,Ian C. W. Hardy,Matthias Soller,Reinhard Stöger

doi:10.1038/s41598-020-80620-7

Abstract

Maximizing crop yields relies on the use of agrochemicals to control insect pests. One of the most widely used classes of insecticides are neonicotinoids that interfere with signalling of the neurotransmitter acetylcholine, but these can also disrupt crop-pollination services provided by bees. Here, we analysed whether chronic low dose long-term exposure to the neonicotinoid thiamethoxam alters gene expression and alternative splicing in brains of Africanized honey bees, Apis mellifera, as adaptation to altered neuronal signalling. We find differentially regulated genes that show concentration-dependent responses to thiamethoxam, but no changes in alternative splicing. Most differentially expressed genes have no annotated function but encode short Open Reading Frames, a characteristic feature of anti-microbial peptides. As this suggested that immune responses may be compromised by thiamethoxam exposure, we tested the impact of thiamethoxam on bee immunity by injecting bacteria. We show that intrinsically sub-lethal thiamethoxam exposure makes bees more vulnerable to normally non-pathogenic bacteria. Our findings imply a synergistic mechanism for the observed bee population declines that concern agriculturists, conservation ecologists and the public.

Highlights

Maximizing crop yields relies on the use of agrochemicals to control insect pests
We have further demonstrated that sub-lethal exposure to thiamethoxam, another neonicotinoid, can cause impairment in the midgut and brain of the Africanized Apis mellifera, as well as contribute to a reduction in honey bee lifespan[9,42,43,44]
We found that thiamethoxam-exposed bees that were infected with bacteria had greatly decreased viability compared to infected but chemically unexposed bees

Summary

Introduction

Maximizing crop yields relies on the use of agrochemicals to control insect pests. One of the most widely used classes of insecticides are neonicotinoids that interfere with signalling of the neurotransmitter acetylcholine, but these can disrupt crop-pollination services provided by bees. We analysed whether chronic low dose long-term exposure to the neonicotinoid thiamethoxam alters gene expression and alternative splicing in brains of Africanized honey bees, Apis mellifera, as adaptation to altered neuronal signalling. Most differentially expressed genes have no annotated function but encode short Open Reading Frames, a characteristic feature of anti-microbial peptides As this suggested that immune responses may be compromised by thiamethoxam exposure, we tested the impact of thiamethoxam on bee immunity by injecting bacteria. The western honey bee Apis mellifera is highly beneficial for human societies Besides honey production, this semi-domesticated insect plays a critical role in sustaining global food security through the provision of managed pollination services that contribute to increased yields of many crops. Sub-lethal uptake of some neonicotinoids affects the honey bee brain, impairing foraging behaviour, flight, navigation, communication, learning and m emory[20,21,22,23,24,25]

Methods

Results

Conclusion