Discrete roles of Ir76b ionotropic coreceptor impact olfaction, blood feeding, and mating in the malaria vector mosquito Anopheles coluzzii

Abstract

Anopheline mosquitoes rely on their highly sensitive chemosensory apparatus to detect diverse chemical stimuli that drive the host-seeking and blood-feeding behaviors required to vector pathogens for malaria and other diseases. This process incorporates a variety of chemosensory receptors and transduction pathways. We used advanced in vivo gene-editing and -labeling approaches to localize and functionally characterize the ionotropic coreceptor AcIr76b in the malaria mosquito Anopheles coluzzii, where it impacts both olfactory and gustatory systems. AcIr76b has a broad expression pattern in female adult antennal grooved pegs, coeloconic sensilla, and T1 and T2 sensilla on the labellum, stylets, and tarsi, as well as the larval sensory peg. AcIr76b is colocalized with the Orco odorant receptor (OR) coreceptor in a subset of cells across the female antennae and labella. In contrast to Orco and Ir8a, chemosensory coreceptors that appear essential for the activity of their respective sets of chemosensory neurons in mosquitoes, AcIr76b−/− mutants maintain wild-type peripheral responses to volatile amines on the adult palps, labellum, and larval sensory cone. Interestingly, AcIr76b−/− mutants display significantly increased responses to amines in antennal grooved peg sensilla, while coeloconic sensilla reveal significant deficits in responses to several acids and amines. Behaviorally, AcIr76b mutants manifest significantly female-specific insemination deficits, and although AcIr76b−/− mutant females can locate, alight on, and probe artificial blood hosts, they are incapable of blood feeding successfully. Taken together, our findings reveal a multidimensional functionality of Ir76b in anopheline olfactory and gustatory pathways that directly impacts the vectorial capacity of these mosquitoes.