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Gustatory Receptors in Mosquito Olfaction and Host-Seeking Behavior

Abstract

Female mosquitoes have evolved multiple strategies to find hosts from a distance by their odor. Few compounds from the human odor blend are known that mediate these behaviors. One is carbon dioxide (CO2), which activates resting mosquitoes and triggers upwind flight. CpA neurons on the maxillary palps express three members of the gustatory receptor (GR) family and detect CO2.

I found that CO2-sensitive cpA neurons in both Aedes aegypti and Anopheles gambiae also detect components of the human odor blend. CpA responses to these odorants closely resemble its responses to CO2, and when CO2 and skin odorants are presented together, cpA responds more strongly to the combination than to either alone. CpA also detects the natural human odor blend. A novel long-term inhibitor of cpA was used to block cpA activity, and behavioral tests in cpA-off mosquitoes revealed specific deficits in behavioral activation in response to odor, even without a CO2 stimulus.

Genes for the receptor subunits Gr1, 2, and 3 were cloned and expressed in the Drosophila ab1C neuron. In mutants lacking Drosophila receptors, Gr2 and Gr3 form a functional receptor that is as sensitive to CO2 and more sensitive to other odorants than when Gr1 is added. Two inhibitors reduced CO2 responses in neurons expressing Gr2+3, and adding Gr1 modulated their activity in an odorant-specific manner. When mosquito GRs are expressed with Drosophila GRs, they form a CO2 receptor only when both mosquito Gr1+2 and Drosophila Gr63a are present, providing clues to the evolutionary history of protein interactions in this receptor class.

Mosquitoes use odor to discriminate between more and less preferred hosts. Human participants were ranked in attractiveness in wild type and mutant mosquitoes lacking function in cpA or other olfactory neurons. Mutants had altered preferences from wild type. Additional studies may elucidate the mechanisms by which these receptors contribute to preference.

The results of this study integrate molecular, physiological, and behavioral experiments to decode more of the links between a mosquito's chemical environment and her behavioral output. Better understanding the mechanisms driving host-seeking behavior will contribute to critically needed new strategies for combating mosquito-borne disease.

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