The detection of carbonation by the Drosophila gustatory system

Abstract

There are five known taste modalities in humans: sweet, bitter, sour, salty and umami (the taste of monosodium glutamate). Although the fruitfly Drosophila melanogaster tastes sugars, salts and noxious chemicals, the nature and number of taste modalities in this organism is not clear. Previous studies have identified one taste cell population marked by the gustatory receptor gene Gr5a that detects sugars, and a second population marked by Gr66a that detects bitter compounds. Here we identify a novel taste modality in this insect: the taste of carbonated water. We use a combination of anatomical, calcium imaging and behavioural approaches to identify a population of taste neurons that detects CO2 and mediates taste acceptance behaviour. The taste of carbonation may allow Drosophila to detect and obtain nutrients from growing microorganisms. Whereas CO2 detection by the olfactory system mediates avoidance, CO2 detection by the gustatory system mediates acceptance behaviour, demonstrating that the context of CO2 determines appropriate behaviour. This work opens up the possibility that the taste of carbonation may also exist in other organisms.

Oviposition preference for and positional avoidance of acetic acid provide a model for competing behavioral drives in Drosophila

“…However, when needing to lay eggs, the attraction for AA overrides this positional repulsion, thereby allowing females to deposit their eggs on AA-containing food. Other studies have revealed opposing behavioral responses to a single compound; when detected as carbonation by the gustatory system, CO 2 is attractive (27), but when detected as an odorant, it is aversive (28). However, our experimental setup is unique in that opposing behavioral responses to a single stimulus (AA) are concurrently induced and assayed, affording direct observation of the competition between the 2 behavioral drives.…”

Flying the Fly: Long-range Flight Behavior of Drosophila melanogaster to Attractive Odors

“…Water has earlier been reported to be critically important for attraction to traps baited with synthetic fruit odors (Zhu et al 2003). Drosophila melanogaster sense water with gustatory receptor neurons on the proboscis, projecting into a specific region of the suboesophagal ganglion, and with hygrosensory neurons located on the antennae, projecting into the antennal mechanosensory centre (Fischler et al 2007;Liu et al 2007;Inoshita and Tanimura 2008). It is remarkable that stimuli from outside the antennal lobe, the olfactory center, generate or contribute to an upwind flight response in D. melanogaster.…”

Tuning the chemosensory window

“…Antennal perception of carbon dioxide is interpreted as an alarm signal and generates an avoidance response, 29 whereas the perception of carbon dioxide via taste receptors on the proboscis is interpreted as the presence of a fermenting food source and elicits an attractant response. 30 These observations and behavioral responses to pheromones would suggest that inputs from specialized chemosensory systems are processed via distinct specialized neural pathways. Nevertheless, one cannot exclude that input from olfactory receptors and gustatory receptors might often be integrated, a notion that is supported by covariant transcriptional modules that contain both Gr and Or transcripts.…”