Olfactory responses in a gustatory organ of the malaria vector mosquito Anopheles gambiae

Abstract

The proboscis is an important head appendage in insects that has primarily been thought to process gustatory information during food intake. Indeed, in Drosophila and other insects in which they have been identified, most gustatory receptors are expressed in proboscis neurons. Our previous characterization of the expression of AgOR7, a highly conserved odorant receptor (OR) of the Afrotropical malaria vector mosquito Anopheles gambiae in the labellum at the tip of the proboscis was suggestive of a potential olfactory function in this mosquito appendage. To test this hypothesis, we used electrophysiological recording and neuronal tracing, and carried out a molecular characterization of candidate OR expression in the labellum of A. gambiae. These studies have uncovered a set of labial olfactory responses to a small spectrum of human-related odorants, such as isovaleric acid, butylamine, and several ketones and oxocarboxylic acids. Molecular analyses indicated that at least 24 conventional OR genes are expressed throughout the proboscis. Furthermore, to more fully examine AgOR expression within this tissue, we characterized the AgOR profile within a single labial olfactory sensillum. This study provides compelling data to support the hypothesis that a cryptic set of olfactory neurons that respond to a small set of odorants are present in the mouth parts of hematophagous mosquitoes. This result is consistent with an important role for the labellum in the close-range discrimination of bloodmeal hosts that directly impacts the ability of A. gambiae to transmit malaria and other diseases.olfaction ͉ proboscis ͉ insect ͉ olfactory receptor neuron

Olfaction in vector-host interactions

“…Here at least one sensillum that is reminiscent of the Cs. inornata T2 sensilla harbours at least two ORNs and responds to butylamine, aliphatic acids and several ketone compounds including acetophenone (Kwon et al 2006). The presence of this cryptic olfactory capacity in the primary gustatory organ of An.…”

“…Recent electrophysiological studies, however, demonstrated that the labellum of An. gambiae is also sensitive to odorant stimuli including butylamine and several aliphatic carboxylic acids (Kwon et al 2006). Here at least one sensillum that is reminiscent of the Cs.…”

“…This functionality has been repeatedly validated with An. gambiae , Hallem et al 2004a, Kwon et al 2006, Sato et al 2008, Xia et al 2008, Bombyx mori Linnaeus (Nakagawa et al 2005, Syed et al 2006, Heliothis virescens (Fabricius) (Grosse-Wilde et al 2007) and Apis mellifera Linnaeus ORs (Wanner et al 2007). Not surprisingly, these data indicate that the expression of a given Or gene in insect ORNs determines their functional specificity (Dobritsa et al 2003, Hallem et al 2004a, Hallem et al 2004b, Jones et al 2005.…”

“…In An. gambiae detailed transcription profiles of the proboscis, the maxillary palp and the larval antenna have been established (Kwon et al 2006, Xia et al 2008, while the precise expression profile of olfactory genes in the adult antenna has yet to be fully elucidated.…”

“…Furthermore, the odorants that elicit responses from labellar sensilla have relatively low volatility compared to other known mosquito attractants, raising the suggestion that the labellum of An. gambiae might be involved in the close-range odour detection at the penultimate stages of host-seeking or oviposition behaviour (Kwon et al 2006).…”