Variant Ionotropic Receptors in the Malaria Vector Mosquito Anopheles gambiae Tuned to Amines and Carboxylic Acids

R Jason Pitts,Zhiwei Zhang,Stephen L Derryberry,Laurence J Zwiebel

doi:10.1038/srep40297

Abstract

The principal Afrotropical human malaria vector mosquito, Anopheles gambiae, remains a significant threat to global health. A critical component in the transmission of malaria is the ability of An. gambiae females to detect and respond to human-derived chemical kairomones in their search for blood meal hosts. The basis for host odor responses resides in olfactory receptor neurons (ORNs) that express chemoreceptors encoded by large gene families, including the odorant receptors (ORs) and the variant ionotropic receptors (IRs). While ORs have been the focus of extensive investigation, functional IR complexes and the chemical compounds that activate them have not been identified in An. gambiae. Here we report the transcriptional profiles and functional characterization of three An. gambiae IR (AgIr) complexes that specifically respond to amines or carboxylic acids - two classes of semiochemicals that have been implicated in mediating host-seeking by adult females but are not known to activate An. gambiae ORs (AgOrs). Our results suggest that AgIrs play critical roles in the detection and behavioral responses to important classes of host odors that are underrepresented in the AgOr chemical space.

Highlights

With a single exception, the family of 46 variant ionotropic receptor genes identified in An. gambiae (AgIrs) have not been functionally characterized[16]
We previously reported the transcript abundances of the An. gambiae IR (AgIr) family in An. gambiae adult antennae and maxillary palps based on RNA sequencing[28]
RPKM values are reported for the co-receptors, AgIr8a, AgIr25a, and AgIr76b as well as for the tuning receptors AgIr41a, AgIr41c, and AgIr75k that have been functionally characterized in this study (Fig. 1; Supplemental Table S1)

Summary

Introduction

The family of 46 variant ionotropic receptor genes identified in An. gambiae (AgIrs) have not been functionally characterized[16]. We have observed that the AgIrs function independently of AgOrs at the larval stage where AgIr76b, a potential Ir coreceptor, is required for An. gambiae larval responses to butylamine[16], but virtually nothing is known about their relationships at the adult stage. This leads us to speculate that butylamine sensitivity in adult An. gambiae requires the expression of AgIr76b, plus the coreceptor AgIr25a and an as yet identified “tuning” AgIr. several of functional studies have been carried out on the AgOr family of chemoreceptors, very little is known about the roles of AgIrs in odor coding (the relationship between essential features of odor molecules and their transduction into patterns of neural activity) and function. Future studies will continue to illuminate the molecular foundations for host odor sensitivity, and the roles that AgIrs play in this process

Methods

Results

Conclusion