Convergent evolution of noxious heat sensing by TRPA5, a novel class of heat sensor in Rhodnius prolixus

Abstract

As ectotherms, insects need a multifaceted repertoire of heat-sensitive receptors to monitor environmental temperatures and finely control behavioral thermoregulation. Here, we show that TRPA5 genes, a class of ankyrin transient receptor potential channels lost in genomes of model fruit flies or mosquitoes, are widespread across insect orders, and encode a previously uncharacterized type of heat receptors. We demonstrate that RpTRPA5B, a TRPA5 channel of the triatomine bug Rhodnius prolixus (Insect: Hemiptera), primary vector of Chagas disease, forms a homo-tetrameric channel displaying a uniquely high thermosensitivity. The channel biophysical determinants include a large channel activation enthalpy change (72 kcal/mol), a high temperature coefficient (Q10 = 25), and temperature-induced currents from 53 {degrees}C to 68 {degrees}C (T0.5= 58.6 {degrees}C) in vitro, similar to mammalian noxious TRPV heat receptors. Monomeric and tetrameric predictions of the ion channel architecture show reliable and conserved structural parallels with fruit fly dTRPA1, albeit depicting structural uniqueness from dTRPA, Painless and Pyrexia in the ankyrin repeat domain and the channel selectivity filter, potential modulator regions of functional characteristics of TRPs. The channel activation response, structural features and ubiquitous sensory tissue expression delineate a potential thermosensitive physiological niche close to that of Pyrexia genes, lost during the evolution of true bugs. Overall, the finding of TRPA5 genes as a class of temperature-activated receptor illustrates the dynamic evolution of a large family of insect molecular heat detectors, with TRPs as promising multimodal sensory targets for triatomine vector control.