Molecular basis of ancestral vertebrate electroreception

Elasmobranch fishes, including sharks, rays, and skates, use specialized electrosensory organs called ampullae of Lorenzini to detect extremely small changes in environmental electric fields. Electrosensory cells within these ampullae can discriminate and respond to minute changes in environmental voltage gradients through an unknown mechanism. Here we show that the voltage-gated calcium channel CaV1.3 and the big conductance calcium-activated potassium (BK) channel are preferentially expressed by electrosensory cells in little skate (Leucoraja erinacea) and functionally couple to mediate electrosensory cell membrane voltage oscillations, which are important for the detection of specific, weak electrical signals. Both channels exhibit unique properties compared with their mammalian orthologues that support electrosensory functions: structural adaptations in CaV1.3 mediate a low-voltage threshold for activation, and alterations in BK support specifically tuned voltage oscillations. These findings reveal a molecular basis of electroreception and demonstrate how discrete evolutionary changes in ion channel structure facilitate sensory adaptation. Detection of weak electrical signals by skates relies on functional coupling of specific calcium and potassium channels, which mediates oscillations in electrosensory cell membrane voltage. Cartilaginous fish, such as sharks, rays and skates, can detect tiny changes in electric fields, thanks to specialized electrosensory organs, but the biophysical mechanism has remained unknown. Now David Julius and colleagues show that the voltage-gated calcium channel CaV1.3 and the calcium-activated potassium channel BK work together in electrosensory cells in little skate to mediate voltage oscillations across the cell membrane, allowing the detection of weak electrical signals in the environment. The work dissects the structural adaptations that distinguish both channels from their mammalian orthologues and enable a low-voltage threshold for activation and tuned voltage oscillations.