UC Riverside

The taste system is essential to determine the palatability of a potential food sources. Insects use gustatory receptors (Gr) to detect both appetitive and aversive compounds. In D. melanogaster, sweet neurons express eight Grs belonging to a highly conserved clade in insects. Currently, it is unknown how these receptors detect sweet tastants. A system that can functionally express single Grs to study ligand recognition is necessary to fill a critical gap in the field. Using the CO2-sensing olfactory neuron as a unique in vivo decoder, we expressed each receptor of the sweet clade individually and recorded the neural activity to a panel of sweet tastants. We also expressed Gr43a, an internal fructose sensor found outside of the sweet clade, and its mosquito ortholog, AgGr 25, in the CO2 olfactory neuron. Each receptor conferred sensitivity to two or more sweet tastants and each sweet tastant was detected by more than one sweet Gr, indicating direct roles in ligand detection for all sweet receptors. Moreover, sweet Grs play a role in bitter tastant detection. Bitter compounds can directly suppress sugar induced activity of sweet taste neurons in the absence of bitter neurons yet the mechanism is unknown. We found that receptors of the sweet clade can be directly inhibited by bitter tastants and each receptor is inhibited by a unique subset of compounds. This property is a distinguishing feature of sweet clade since neither Gr43a nor its mosquito ortholog AgGr25 are inhibited by bitter compounds.

Many features of sweet Grs are evolutionarily conserved in mosquitoes. We discovered that labellar sweet neurons from both A. gambiae and A. aegypti can detect sweet tastants and be directly inhibited by bitter tastants.. Furthermore using the CO2 neuron, we discovered that every receptor of the A. gambiae sweet clade is involved in ligand recognition of at least one sweet tastant and one sweet AgGr can be inhibited by bitter tastants, suggesting the sweet clade has evolved to become dual sensor of sweet and bitter tastants. This work set the platform to study ligand recognition of Grs in other insects, expanding our understanding of insect taste detection.