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. 2019 Jan 24:12:533.
doi: 10.3389/fncel.2018.00533. eCollection 2018.

Supersensitive Odorant Receptor Underscores Pleiotropic Roles of Indoles in Mosquito Ecology

Affiliations

Supersensitive Odorant Receptor Underscores Pleiotropic Roles of Indoles in Mosquito Ecology

David M Ruel et al. Front Cell Neurosci. .

Erratum in

Abstract

Mosquitoes exhibit highly diverse and fast evolving odorant receptors (ORs). The indole-sensitive OR gene clade, comprised of Or2 and Or10 is a notable exception on account of its conservation in both mosquito subfamilies. This group of paralogous genes exhibits a complex developmental expression pattern in Aedes aegypti: AaegOr2 is expressed in both adults and larvae, AaegOr10 is adult-specific and a third member named AaegOr9 is larva-specific. OR2 and OR10 have been deorphanized and are selectively activated by indole and skatole, respectively. Using the two-electrode voltage clamp of Xenopus oocytes expressing Ae. aegypti ORs, we show that AaegOR9 is supersensitive and narrowly tuned to skatole. Our findings suggest that Ae. aegypti has evolved two distinct molecular strategies to detect skatole in aquatic and terrestrial environments, highlighting the central ecological roles of indolic compounds in the evolutionary and life histories of these insects.

Keywords: Aedes aegypti; indole; mosquito; odorant receptor; skatole.

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Figures

Figure 1
Figure 1
Aedes aegypti OR9 (AaegOR9) is narrowly tuned to skatole. Indole-tuning curve of AaegOR9 to an odor panel comprised of 31 indole derivatives (kurtosis value: 17.75). Skatole is five times more potent than indole (t-test: ****p < 0.0001; n = 10; 100% and 500% response thresholds shown as dotted lines), which is inversely correlated with their respective water solubility (inset). Error bars of average responses indicate standard errors.
Figure 2
Figure 2
Aedes aegypti OR9 (AaegOR9) is a supersensitive skatole receptor. (A) Based on their respective EC50 values (yellow dots), AaegOR9 is significantly (one-way ANOVA followed by Tukey’s post test; p < 0.0001) more sensitive to skatole than to indole or to indole-3-carboxaldehyde (I3C). The concentration (500 nM) to which the tuning curve is based on is indicated by "TC." (B) AaegOR9 is a more sensitive skatole receptor than AaegOR10 (t-test; p < 0.01). (C) Sensitivity ranking (according to EC50 values of cognate receptor-semiochemical interactions) of pheromone and kairomone receptors (Supplementary Table 2).
Figure 3
Figure 3
Or9 is a Culicinae-specific gene expansion. (A) DNA sequence identity, substitution rates, intron locations and odorant ligands (deorphanized receptors are labeled with a black dot, see Supplementary Table 2) suggest that Or9 is a Culicinae-specific gene expansion while Or2 and Or10 are present in both Culicinae (red branches) and Anophelinae (blue branches). Intron locations are color-coded and numbered from 1 to 6 (i1–i6). Missing introns are indicated by a crossed intron with a dotted lines underneath. Bootstrap values (%) are based on 5,000 replicates. Numbered circles on branch points indicate lineage splits in million years (MY). (B) Indolergic receptors are located on the q arm of chromosome 2 and on the R arm of chromosome 3 in Ae. aegypti and An. gambiae, respectively. Transcript numbers are shown for An. gambiae (AGAP#) and Ae. aegypti (AAEL#).
Figure 4
Figure 4
Proposed evolution and ecological roles of Aedes aegypti indolergic receptors. (A) The Or2, 9 and 10 gene clade derives from two successive gene duplication events followed by neofunctionalization (yellow highlights) consisting of modifications of ligand selectivity, sensitivity and developmental expression patterns. The most parsimonious hypothesis is that the most recent common ancestors (MRCAs) of Or2 and Or10 derived from a gene duplication event prior to the Anophelinae-Culicinae split. This event lead to neofunctionalization by means of selective detection of indole derivatives. The second duplication event arose in the Culicinae subfamily (e.g., Ae. aegypti) leading to the emergence of a low [X] and high [x] sensitivity skatole receptor, each expressed in a distinct developmental stage. (B) Putative ecological roles of indole and skatole in adults and larvae. Adults may detect both indole compounds to identify suitable hosts and oviposition sites while larvae may use these compounds to locate food sources, including dead larvae, decomposing organic matter and microbes.

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