A TASTE FOR WATER

Abstract

Whether we like sweet wine, salty tomato juice or bitter lemon depends on our individual preferences: each to his own. Regardless of which flavour of beverage we prefer, from a chemical point of view it is more or less the same as they are all composed primarily of water. But do we also have a taste for water? Although water is essential for us, astonishingly little is known about how we sense it and regulate its uptake. However, we can learn how we may taste water from studying insects, as there is a general agreement among scientists that these little creatures have a taste for water. A research team from the University of California-Berkeley led by Kirstin Scott have now published an exciting study in Nature providing new insights into the molecular basis of water taste in Drosophila.Drosophila and other insects have a unique set of gustatory sensory neurons in their mouthparts that participate in the detection of various tastes. Among them are also neurons known to respond to water, but by an unknown mechanism. In order to identify the neurons' water receptor, Peter Cameron, a graduate student in Scott's lab, compared gene expression in the mouthparts between control flies and mutant flies lacking all taste neurons. One of the genes, whose expression was significantly decreased in the mutant flies, was pickpocket 28 (ppk28), a gene encoding an ion channel of the degenerin/epithelial sodium channel (ENaC) family. PPK28 was a promising candidate for the wanted water receptor, as ion channels are known to be involved in the detection of different tastes. Indeed, when Peter Cameron tested which gustatory neurons actually make PPK28, he could not detect it in neurons known to sense sweet or bitter tastes, but he found it in neurons known to participate in water sensing.Next, he monitored neuronal activity in response to different taste solutions by using a genetically encoded fluorescent Ca2+ sensor expressed in the water-sensing neurons of living flies. He found higher neuronal activity when he stimulated the flies' mouthparts with pure water and lower activity when he applied solutions containing salts, sugars, acids or bitter substances. The higher the concentration of the added substance, the lower the resulting neuronal activity, suggesting that the water receptor responds to changes in the relative water content and hence is an osmosensitive receptor. Then Peter Cameron's colleague Makoto Hiroi recorded electrical signals from gustatory neurons of the taste-sensing organs (sensilla), comparing control and mutant flies lacking a functional PPK28 channel. The sensilla of the mutant flies failed to respond to water, in contrast to the control flies, which did. Moreover, the mutant flies also changed their behaviour as they drank significantly less water. Finally, to determine whether PPK28 is directly involved in water sensing, the team genetically manipulated bitter-sensing neurons as well as human embryonic kidney cells, which do not have any taste receptors, to make them produce PPK28, and again recorded Ca2+ signals to monitor whether they could detect water. They successfully converted the bitter-sensing neurons into water-sensing ones, and even conferred this type of responsiveness on human embryonic kidney cells, which lack the taste response.Scott and her colleagues have provided solid evidence that a sodium channel of the degenerin/ENaC family functions as a water receptor by sensing differences in the solution's osmolarity. The PKK28 receptor may therefore serve as a framework for studying water sensing and osmosensing in other animals and even humans. Whether the identified receptor type could also be involved in central osmosensation, which is essential to control the osmolarity of our extracellular body fluids, remains unclear, as this would require extreme sensitivity to minute osmolarity changes.