Chemosensation in the Common Bed Bug, Cimex lectularius

Abstract

As an ectoparasite on human beings and other animals, the common bed bug, Cimex lectulatius, has been resurgent worldwide and is of concern by both governments and general public for their biting nuisance and potential risk of disease transmission. The host-seeking or risk-avoiding behavior of bed bugs is mediated by their olfaction system in detecting attractive odorants or chemical repellents. Although the constituents of human emanations and chemical insect repellents have been thoroughly elucidated, we know little about which constituents are sensed and how they are recognized by the bed bug’s olfactory system, such as olfactory receptor neurons (ORNs) or odorant receptors (ORs). In order to reveal the mechanisms involved in the chemoreception of bed bugs, the current study investigated the responses from olfactory receptor neurons and odorant receptor to both human odorants and chemical insect repellents, especially DEET. Different types of olfactory sensilla were found to produce distinctive response profiles to human odorants and chemical insect repellents. Particularly, D types of olfactory sensilla possess the widest spectrum in detecting these odorants; E sensilla respond to very few odorants with low firing frequencies and C sensilla were only found to be sensitive to amines and several heterocyclics. Among all different chemical categories of stimuli, bed bug showed bias in detecting the aldehydes /ketones and alcohols and terpene-derived repellents but not the carboxylic acids and non-terpen-derived repellents. In addition, the dosages of odorants were shown to be an important factor in determining the firing frequency and temporal dynamics of neuronal response in bed bugs. To further decipher the molecular basis of neuronal responses to these odorants, bed bug ORs expressed in the Xenopus oocyte were challenged by odorants from both human being and chemical insect repellents. Each odorant receptor displayed variant tuning curves in response to these odorants and each odorant was encoded by multiple odorant receptors. Aldehydes/ketones, alcohols, heterocyclics and terpenes/terpenoides were more likely to activate bed bug ORs than carboxylic acids, which was consistent with the neuronal response bias. Moreover, dosage and chemical structure of odorants were two critical factors in influencing the responses of ORs. DEET, one of the most successful synthetic insect repellents, showed very significant repulsive effects to the common bed bug. Dual roles of DEET (activating effect and interfering effect) on the olfactory responses of bed bugs were revealed in this study. ORNs housed in two types of olfactory sensilla (Dα and Dβ sensilla) and at least three bed bug ORs (OR20, OR36 and OR37) were identified to be activated directly by DEET. Meanwhile, it was also proven that DEET could block or mask the neuronal responses of bed bugs to certain odorants by interfering with the function of specific odorant receptors in response to certain odorants. Interestingly, those three DEET-sensitive odorant receptors were found to be even more sensitive to the terpenes/terpenoids, which were originally isolated from plants. Behavior bioassays further indicated that these terpenes/terpenoids were much more effective in repelling bed bugs compared to DEET, suggesting that DEET targeted on the bed bug receptors that were naturally sensitive to terpenes/terpenoids. Thus our finding provided a novel mechanism for DEET’s function on insect olfactory systems. Taken together, my study presented a global picture about the chemoreception of the bed bug to both human odorants and chemical insect repellents, which gave insight to mechanisms of odorant recognition in the bed bug peripheral olfactory system. Particularly, we clarified both the activating and interfering effect of DEET in repelling the common bed bug, which should benefit the development of new repellents in bed bug control.