Odorant-receptor-mediated regulation of chemosensory gene expression in the malaria mosquito Anopheles gambiae

Mosquitoes locate and approach humans based on the activity of odorant receptors (ORs) expressed on olfactory receptor neurons (ORNs). Olfactogenetic experiments in Anopheles gambiae mosquitoes revealed that the ectopic expression of an AgOR (AgOR2) in ORNs dampened the activity of the expressing neuron. This contrasts with studies in Drosophila melanogaster in which the ectopic expression of non-native ORs in ORNs confers ectopic neuronal responses without interfering with native olfactory physiology. RNA-seq analyses comparing wild-type antennae to those ectopically expressing AgOR2 in ORNs indicated that nearly all AgOR transcripts were significantly downregulated (except for AgOR2). Additional experiments suggest that AgOR2 protein rather than mRNA mediates this downregulation. Using in situ hybridization, we find that AgOR gene choice is active into adulthood and that AgOR2 expression inhibits AgORs from turning on at this late stage. Our study shows that the ORNs of Anopheles mosquitoes (in contrast to Drosophila) are sensitive to a currently unexplored mechanism of AgOR regulation. [Display omitted] •Ectopic OR expression disrupts mosquito olfactory neuron activity•Expression of an OR in mosquitoes reduces endogenous OR expression•Onset of mosquito OR expression extends into adult stages•Mosquitoes host seek despite the lack of OR neuron function Maguire et al. discover that the ectopic expression of an olfactory receptor can downregulate the transcription of endogenous odorant receptors in mosquito olfactory neurons. The onset of mosquito odorant-receptor expression by an olfactory neuron continues into adult stages, and is particularly sensitive to exogenous olfactory reception expression.