Environmental exposure to cadmium induces olfactory neurotoxicity in fire ants and the molecular basis

Cadmium (Cd) exhibits widely olfactory toxicity to animals. We previously reported that Cd exposure induces the transcriptional dysregulation of olfactory marker proteins (OMPs) of the red imported fire ant Solenopsis invicta. However, it is still unclear how environmental Cd exposure-induced deregulation of OMPs affects the olfactory signal transduction and olfaction-driven social behavior of S. invicta. Here, we showed that S. invicta displayed dull sensory perception on bait in Cd-contaminated areas and dietary Cd ingestion by S. invicta reduced the bait search efficiency. We hypothesize that deregulation of OMPs by Cd exposure blocks the olfactory signal transduction in fire ants. Our results indicated the odor binding protein 14 (SiOBP14) was consistently inhibited in antennal sensilla of fire ants across Cd exposure at 0.5, 5 and 50 mg/kg. Function analysis in vitro and in vivo demonstrated that SiOBP14 is essential in perception of S. invicta to bait odorants. Cd-exposed fire ants showed weak odorant receptor neurons (ORNs) chemosensory signaling and electroantennogram (EAG) response. Moreover, Cd exposure repeals the preference of S. invicta to the active bait odorants, including 2-methyltetrahydrofuran-3-one, 2-methyl-3-furanthiol and 4,5-dimethylthiazole, and even triggers a behavioral transition from preference to repellence. These results indicate that Cd exposure inhibits the specific OMP expression and disrupts olfactory signal transduction, thereby inducing dull sensory perception of S. invicta to bait odorants. The findings provide new implications for monitoring and control of agricultural insect pests in heavy metal polluted areas.