Taste coding of heavy metal ion-induced avoidance in Drosophila

Increasing pollution of heavy metals poses great risks to animals globally. Their survival likely relies on an ability to detect and avoid harmful heavy metal ions (HMIs). Currently, little is known about the neural mechanisms of HMI detection. Here, we show that Drosophila and related species of Drosophilidae actively avoid toxic HMIs at micromolar concentrations. The high sensitivity to HMIs is biologically relevant. Particularly, their sensitivity to cadmium is as high as that to the most bitter substance, denatonium. Detection of HMIs in food requires Gr66a(+) gustatory neurons but is independent of bitter-taste receptors. In these neurons, the ionotropic receptors IR76b, IR25a, and IR7a are required for the perception of heavy metals. Furthermore, IR47a mediates the activation of a distinct group of non-Gr66a(+) gustatory neurons elicited by HMIs. Together, our findings reveal a surprising taste quality represented by noxious metal ions.