Characterization of Chemosensory Responses on the Labellum of the Malaria Vector Mosquito, Anopheles coluzzii

Abstract

Anopheles gambiae coluzzii (An. coluzzii) uses olfaction to modulate a range of critical behaviors that are essential for survival and reproduction; most notably, host preference and selection underlie its vectorial capacity for human malaria. As is the case for all mosquitoes, An. coluzzii has three specialized peripheral olfactory appendages—the antennae, maxillary palps and labella—which are used to detect and orient in response to a large variety of olfactory cues. Of these, neither the molecular nor the physiological significance of the labellum have been thoroughly characterized despite suggestions that labial-derived odorant reception is critical for close-range host attraction. Here we report global chemoreceptor transcriptome profiles together with a systematic electrophysiological analysis of labial T2 sensilla, and associated behavioral responses of female An. coluzzii. Single sensillum recordings of the T2 sensilla revealed robust responses to odorants previously associated with human sweat and oviposition sites and identified a 10-component blend that elicited attraction in a dual-choice landing bioassay designed to mimic host seeking in which non-blood fed females were significantly more attracted to the labial-responsive odorant blend as compared to gravid females. Taken together, these data suggest that, in An. coluzzii, olfactory responses derived from the labellum contribute to host-seeking.

An odorant receptor from Anopheles gambiae that demonstrates enantioselectivity to the plant volatile, linalool

“…Linalool is an interesting ligand due to its association with flowering plants and may therefore provide a chemical cue that helps to orient mosquitoes toward sources of nectar. AgamOr29 is most highly expressed in the labellar lobes of both sexes (Fig 3), which reinforces the hypothesis that this receptor is involved in short range chemical sensing and influences behavioral responses such as nectar feeding [40]. Linalool has also been identified as a component of human sweat and therefore may represent a multi-contextual odor cue that can act as a bloodmeal host attractant for Anophelines [48].…”

“…To better understand the expression profile of AgamOr29, we sought to determine the spatial expression of the transcript within sensory appendages of adult mosquitoes by analyzing published RNA sequencing data sets [38–40]. We have summarized available expressional data for the antennae, maxillary palps, labella, and whole bodies (Fig 3).…”

“…Transcriptional analysis of mosquito sensory appendages and bodies were derived from previously published studies [38–40]. Normalized transcript abundance values were reported as were available in the literature as either FPKM (Fragments per Kilobase per Million Reads) or RPKM (Reads per Kilobase per Million Reads).…”

Mutagenesis of the Orco Odorant Receptor Co-receptor Impairs Olfactory Function in the Malaria VectorAnopheles coluzzii

“…The oviposition preference assay was carried out for both wild-type and mutant mosquitoes in a dual-choice assay in a Bugdorm® insect rearing cage, as previously described (Saveer et al, 2018), with minor modifications. The oviposition blends were comprised of seven compounds (2-npropylphenol, 2-methylphenol, 4-methylphenol, 4-ethylphenol, nonanal, indole, and skatole) each at 10−8 M in ethanol (Choo et al, 2015(Choo et al, , 2018Himeidan et al, 2013;Hughes et al, 2010;Rinker et al, 2013;Zhu et al, 2013).…”

Species and sex-specific chemosensory gene expression in Anopheles coluzzii and An. quadriannulatus antennae

“…coluzzii and An. quadriannulatus female palps [21] and that all three are expressed in other olfactory organs as well [5,21,45], indicates their function extends beyond that.…”