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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 compounds1,2,3,4. 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 avoidance5, 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.

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Figure 1: The E409-Gal4 enhancer trap labels taste peg neurons that project to the taste region of the fly brain.
Figure 2: Neurons labelled by E409 respond to carbonation.
Figure 3: E409 neurons are necessary for behavioural preference for sodium bicarbonate, pH 6.5, and sufficient to trigger taste acceptance behaviour.
Figure 4: Segregation of CO 2 detection by the taste and olfactory systems.

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Acknowledgements

We thank U. Heberlein and her laboratory for generating and providing the Gal4 enhancer trap library containing the E409-Gal4 transgenic flies; Z. Wang for generation of the Gr5a-GFP-IRES-GFP-IRES-GFP transgenic flies; S. Asgarian for technical assistance in the anatomy screen; and G. Agarwaal for assistance with Matlab. We also thank L. Vosshall, C. Zuker and members of the Scott laboratory for providing comments on the manuscript. This work was supported by a grant from the NIH (NIDCD), a Burroughs Wellcome Fund Career Award, a McKnight Scholar Award and a John Merck Award to K.S.

Author Contributions W.F. performed the majority of G-CaMP imaging experiments, developed the behavioural assay, performed behavioural experiments and co-wrote the manuscript. P.K. performed the anatomy screen leading to the identification of E409-Gal4. S.M. performed the G-CaMP imaging experiments of capsaicin-induced responses in E409-Gal4, UAS-GCaMP, UAS-VR1E600K flies, sequenced the Gal4 insertion site in the E409-Gal4 flies and participated in initial characterization of the E409 neurons. K.S. assisted P.K. in the anatomy screen and W.F. in the G-CaMP imaging and behavioural studies, co-wrote the manuscript and supervised the project.

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Correspondence to Kristin Scott.

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This file contains Supplementary Figure 1 with Legend. The Supplemental Figure provides a schematic of fly taste anatomy and the expression pattern of E409 in the fly brain. (PDF 161 kb)

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Fischler, W., Kong, P., Marella, S. et al. The detection of carbonation by the Drosophila gustatory system. Nature 448, 1054–1057 (2007). https://doi.org/10.1038/nature06101

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