Fungicides chlorothanolin, azoxystrobin and folpet induce transcriptional alterations in genes encoding enzymes involved in oxidative phosphorylation and metabolism in honey bees (Apis mellifera) at sublethal concentrations

Abstract

Fungicides are highly used for plant protection but their molecular and chronic effects are poorly known. Here, we analyse transcriptional effects in the brain of honey bees of three frequently applied fungicides, azoxystrobin, chlorothanolin and folpet, after oral exposure for 24, 48 and 72 h. Among transcripts assessed were genes encoding proteins for immune and hormone system regulation, oxidative phosphorylation, metabolism, and acetylcholine receptor alpha 1. Azoxystrobin and folpet induced minor alterations, including down-regulation of hbg-3 by azoxystrobin and induction of ndufb-7 by folpet. Chlorothanolin induced strong transcriptional down-regulation of genes encoding enzymes related to oxidative phosphorylation and metabolism, including cyp9q1, cyp9q2 and cyp9q3, acetylcholine receptor alpha 1 and hbg-3 and ilp-1, which are linked to hormonal regulation and behavioural transition of honey bees. Exposures to chlorothanolin in different seasonal times showed different responsiveness; responses were faster and often stronger in April than in June. Chlorothanolin caused the strongest effects and affected transcriptional abundance of genes related to energy production, metabolism and the endocrine system. Disturbed energy production may reduce foraging activity and hormonal dysregulation, such as the transition of nurse bees to foragers. Further analyses are needed to further substantiate potential adverse effects of chlorothanolin in bees on the physiological level.