The evolutionarily conserved indolergic receptors of the non-hematophagous elephant mosquito Toxorhynchites amboinensis

Abstract

The conservation of the mosquito indolergic receptors across the Culicinae and Anophelinae mosquito lineages, which spans 200 million years of evolution, is a testament to the central role of indolic compounds in the biology of these insects. Indole and skatole have been associated with the detection of oviposition sites and animal hosts. To evaluate the potential ecological role of these two compounds, we have used a pharmacological approach to characterize homologs of the indolergic receptors Or2 and Or10 in the nonhematophagous elephant mosquito Toxorhynchites amboinensis. We provide evidence that both receptors are narrowly tuned to indole and skatole like their counterparts from hematophagous mosquitoes. These findings indicate that indole and skatole are operating in a non-animal-host seeking context in Toxorhynchites and underscore the importance of understanding their roles in hematophagous mosquitoes.

Mosquito indolergic receptors belong to an ancient and functionally conserved Dipteran gene lineage

“…In this study, we propose that the brachyceran OR30a is an indolOR by virtue of its ligand selectivity, nanomolar sensitivity towards 3-methylindole, and gene structure. Until now, IndolORs were considered to be a Culicidae-specific expansion due to their ligand-binding characteristics [13,24,[34][35][36][37][38][39][40] and amino-acid sequence conservation (50-70%) [12]. Candidate indolORs outside the Culicidae family display an amino-acid sequence identity significantly lower than within mosquitoes.…”

“…Furthermore, these heterocyclic compounds contribute to floral scent [20,21] and are preferred by A. aegypti in the context of plant-host attraction [22]. The complex developmental expression patterns [12] and evolution of mosquito indolORs [13,23,24], in terrestrial adults and aquatic larvae, suggest that these two compounds play key roles in regulating inter-specific interactions in addition to their stage-specific functions. Mosquito species belonging to the subfamilies, Anophelinae and Culicinae, express both an indole-selective (OR2) and a skatole-selective (OR10) receptor.…”

“…Mosquito species belonging to the subfamilies, Anophelinae and Culicinae, express both an indole-selective (OR2) and a skatole-selective (OR10) receptor. In Culicine mosquitoes, including members of the genera Aedes, a third paralog named OR9 operates as a supersensitive skatole receptor during the aquatic stage [24]. The expression of indolORs in aquatic larvae [12] and in terrestrial blood-and nectar-feeding adults of different sex and species [23,25] suggests that indolic compounds may have the intriguing property of influencing mosquito 4 behaviors in multiple ecological contexts, including larval foraging, animal-and plant-host seeking, and oviposition site selection [19].…”

The Emergence of Insect Odorant Receptor-Based Biosensors

“…The first large-scale deorphanization efforts of mosquito ORs [135,136] led to the identification of the indole receptor named OR2. The closely related paralog OR10 is a skatole receptor in several mosquito species [57,137,138]. OR9, a third member of this gene subgroup [133] was also shown to act as a skatole receptor [55].…”

Toxorhynchites Species: A Review of Current Knowledge

“…amboinensis and Ae. aegypti share a number of chemosensory and olfactory genes [84], including functional orthologs of odorant receptors, such as indolergic receptors, OR2 and OR10 [85], (R)-1-octen-3-ol receptor, OR8 [86], and sulcatone receptor, OR4 [87]. Sulcatone has previously been suggested to be involved in human host sensing through OR4 in Ae.…”