Identification of the trail-following pheromone receptor in termites

Chemical communication is the cornerstone of eusocial insect societies since it mediates the social hierarchy, division of labor, and concerted activities of colony members. The chemistry of social insect pheromones received considerable attention in both major groups of social insects, the eusocial Hymenoptera and termites. By contrast, current knowledge on molecular mechanisms of social insect pheromone detection by odorant receptors (ORs) is limited to hymenopteran social insects and no OR was yet functionally characterized in termites, the oldest eusocial insect clade. Here, we present the first OR deorphanization in termites. Using the data from antennal transcriptome and genome of the termiteProrhinotermes simplex(Rhinotermitidae), we selected 4 candidate OR sequences, expressed them in Empty NeuronDrosophila, and functionally characterized using single sensillum recording (SSR) and a panel of termite semiochemicals. In one of the selected ORs, PsimOR14, we succeeded in obtaining strong and reliable responses to the main component ofP. simplextrail-following pheromone, the monocyclic diterpene neocembrene. PsimOR14 showed a narrow tuning to neocembrene; only one additional compound out of 72 tested (geranylgeraniol) generated non-negligible responses. Subsequently, we used SSR andP. simplexworkers to identify the olfactory sensillum specifically responding to neocembrene, thus likely expressingPsimOR14. We report on homology-based modelling of neocembrene binding by PsimOR14 and show how different ligands impact the receptor dynamicity using molecular dynamics simulations. Finally, we demonstrate thatPsimOR14is significantly more expressed in workers than in soldiers, which correlates with higher sensitivity of workers to neocembrene.