Molecular Basis of Odorant Reception in the Asian Tiger Mosquito, Aedes albopictus
Abstract
As a major vector of multiple mosquito-borne diseases, the Asian tiger mosquito Aedes albopictus relies heavily on its olfactory system to detect attractive or aversive chemical cues during host seeking and habitat selection. However, the molecular mechanisms underlying odorant reception in Ae. albopictus remain largely elusive. In this study, we mapped the spatial distribution of odorant receptors (ORs) in the mosquito antenna using ultra-low input single-flagellomere RNA sequencing and the Q-binary reporter system. We identified a distinct spatial organization of ORs along the antenna: some ORs were uniformly expressed across flagellomeres (termed Uniform ORs), whereas others were preferentially enriched in the distal or proximal regions (termed Distal or Proximal ORs, respectively), thereby transcriptionally partitioning the antenna into distinct proximal and distal domains. We then successfully deorphanized 33 out of 68 annotated antennal tuning AalbORs, including 15 Distal, 10 Proximal, and 8 Uniform AalbORs, via the Drosophila “empty” neuron system, which exhibited robust responses to at least one compound from a comprehensive odorant panel spanning various chemical categories. Particularly, several narrowly tuned receptors were found to specialize in detecting ecologically relevant odorants, such as human-associated volatiles and plant-derived repellents. Moreover, Ae. albopictus ORs displayed significantly higher discriminability for ketones, alcohols, esters, aromatics, terpenoids, and heterocyclics compared with aldehydes and carboxylic acids, the latter of which were more likely recognized by ionotropic receptors. Notably, human-associated volatiles (e.g., alcohols, ketones, aromatics, and heterocyclics) were broadly recognized by ORs across all distribution patterns, whereas some terpenoids, previously reported as mosquito repellents, were preferentially detected by distally distributed ORs, suggesting potentially functional compartmentalization in the perception of aversive compounds. Collectively, this work provides novel insights into the chemosensory biology of Ae. albopictus, and may inform the development of innovative olfaction-based strategies for mosquito control.
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