Chronic exposure of bumblebees to neonicotinoid imidacloprid suppresses the entire mevalonate pathway and fatty acid synthesis

Tomas Erban; Bruno Sopko; Pavel Talacko; Karel Harant; Klara Kadlikova; Tatana Halesova; Katerina Riddellova; Apostolos Pekas

doi:10.1016/j.jprot.2018.12.022

Chronic exposure of bumblebees to neonicotinoid imidacloprid suppresses the entire mevalonate pathway and fatty acid synthesis

J Proteomics. 2019 Mar 30:196:69-80. doi: 10.1016/j.jprot.2018.12.022. Epub 2018 Dec 21.

Authors

Tomas Erban¹, Bruno Sopko², Pavel Talacko³, Karel Harant³, Klara Kadlikova⁴, Tatana Halesova⁵, Katerina Riddellova⁵, Apostolos Pekas⁶

Affiliations

¹ Crop Research Institute, Drnovska 507/73, Prague CZ-161 06, Czechia. Electronic address: arachnid@centrum.cz.
² Crop Research Institute, Drnovska 507/73, Prague CZ-161 06, Czechia; Department of Medical Chemistry and Clinical Biochemistry, Faculty of Medicine, Charles University and Motol University Hospital, V Uvalu 84/1, Prague CZ-150 06, Czechia.
³ Proteomics Core Facility, Faculty of Science, Charles University, Prague, Czechia.
⁴ Crop Research Institute, Drnovska 507/73, Prague CZ-161 06, Czechia; Department of Plant Protection, Faculty of Agrobiology, Food and Natural Resources, Czech University of Life Sciences Prague, Kamycka 129, Prague 6, Suchdol CZ-165 00, Czechia.
⁵ ALS Limited, ALS Czech Republic, Na Harfe 336/9, Prague CZ-190 00, Czechia.
⁶ R&D Department, Biobest Group, Ilse Velden 18, Westerlo B-2260, Belgium.

PMID: 30583045
DOI: 10.1016/j.jprot.2018.12.022

Abstract

Determining the side effects of pesticides on pollinators is an important topic due to the increasing loss of pollinators. We aimed to determine the effects of chronic sublethal exposure of the neonicotinoid pesticide imidacloprid on the bumblebee Bombus terrestris under laboratory conditions. The analytical standard of imidacloprid in sugar solution was used for the treatment. Verification of pesticides using UHPLC-QqQ-MS/MS in the experimental bumblebees showed the presence of only two compounds, imidacloprid and imidacloprid-olefin, which were found in quantities of 0.57 ± 0.22 and 1.95 ± 0.43 ng/g, respectively. Thus, the level of the dangerous metabolite imidacloprid-olefin was 3.4-fold higher than that of imidacloprid. Label-free nanoLC-MS/MS quantitative proteomics of bumblebee heads enabled quantitative comparison of 2883 proteins, and 206 proteins were significantly influenced by the imidacloprid treatment. The next analysis revealed that the highly downregulated markers are members of the terpenoid backbone biosynthesis pathway (KEGG: bter00900) and that imidacloprid treatment suppressed the entire mevalonate pathway, fatty acid synthesis and associated markers. The proteomics results indicate that the consequences of imidacloprid treatment are complex, and the marker changes are associated with metabolic and neurological diseases and olfaction disruption. This study provides important markers and can help to explain the widely held assumptions from biological observations. SIGNIFICANCE: The major finding is that all markers of the mevalonate pathway were substantially downregulated due to the chronic imidacloprid exposure. The disbalance of mevalonate pathway has many important consequences. We suggest the mechanism associated with the novel toxicogenic effect of imidacloprid. The results are helpful to explain that imidacloprid impairs the cognitive functions and possesses the delayed and time cumulative effect.

Keywords: Bombus terrestris; Endocrine disruptor; Imidacloprid-olefin; Pesticide exposure; Proteomics; Terpenoid backbone biosynthesis pathway.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Animals
Bees / metabolism*
Fatty Acids / biosynthesis*
Insecticides / pharmacology*
Mevalonic Acid / metabolism*
Neonicotinoids / pharmacology*
Nitro Compounds / pharmacology*

Substances

Fatty Acids
Insecticides
Neonicotinoids
Nitro Compounds
imidacloprid
Mevalonic Acid