Molecular and cellular basis of acid taste sensation in Drosophila

Tingwei Mi,John O Mack,Christopher M Lee,Yali V Zhang

doi:10.1038/s41467-021-23490-5

Tingwei Mi, John O Mack + Show 2 more

Open Access

https://doi.org/10.1038/s41467-021-23490-5

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Abstract

Acid taste, evoked mainly by protons (H+), is a core taste modality for many organisms. The hedonic valence of acid taste is bidirectional: animals prefer slightly but avoid highly acidic foods. However, how animals discriminate low from high acidity remains poorly understood. To explore the taste perception of acid, we use the fruit fly as a model organism. We find that flies employ two competing taste sensory pathways to detect low and high acidity, and the relative degree of activation of each determines either attractive or aversive responses. Moreover, we establish one member of the fly Otopetrin family, Otopetrin-like a (OtopLa), as a proton channel dedicated to the gustatory detection of acid. OtopLa defines a unique subset of gustatory receptor neurons and is selectively required for attractive rather than aversive taste responses. Loss of otopla causes flies to reject normally attractive low-acid foods. Therefore, the identification of OtopLa as a low-acid sensor firmly supports our competition model of acid taste sensation. Altogether, we have discovered a binary acid-sensing mechanism that may be evolutionarily conserved between insects and mammals.

Highlights

Acid taste, evoked mainly by protons (H+), is a core taste modality for many organisms
We employed the fly as a model organism to decipher the taste sensation of acid, given that it has been used successfully over the past 20 years to identify taste receptors, sensory cells, and neuronal circuits involved in taste perception[17,18,19]
Consistent with the results obtained through the two-way feeding assay, we found that the wild-type fly exhibits strong proboscis extension reflex (PER) responses when low concentrations of hydrochloric acid (HCl) are applied to the proboscis, indicating an attractive feeding response

Summary

Introduction

Acid taste, evoked mainly by protons (H+), is a core taste modality for many organisms. We report that the fly mainly uses two different subsets of gustatory receptor neurons (GRNs) to selectively sense low or high concentrations of acids. One of the Otop family members, Otop[1], is essential for sour-taste transduction[15,16] Despite this significant finding, the exact role played by Otop[1] in discriminating low- from high-acid foods remained unclear. We discovered that one of the fly Otop orthologues, Otopetrin-like a (OtopLa), acts as a proton channel and is selectively required for attractive taste sensation of acids in Drosophila. By establishing OtopLa as a bona fide taste receptor for acid in flies, our work overturns the long-standing view that insects and mammals use fundamentally different gustatory receptors

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