Pharyngeal neuronal mechanisms governing sour taste perception in Drosophila melanogaster

Bhanu Shrestha, Jiun Sang, Suman Rimal, Youngseok Lee

Posted on: 23 September 2024

Preprint posted on 30 July 2024

Sour taste perception in fruit flies: neurons in the pharynx, not the external mouthparts, trigger attraction to sour foods.

Selected by Matthew Davies

Categories: animal behavior and cognition, cell biology, neuroscience

Imagine a margarita. It’s refreshing and vibrant. And enjoyably sour – that’s the lime juice. Alone though, lime juice kicks like a mule with an unpleasant, unbearably sour slap.

This is because in great amounts, sourness, indicating acidity, serves as a warning against corrosive tissue damage and often reflects spoilt food. Because of that, the sensation of sourness is a necessary evolutionary development apparent far and wide in the animal kingdom.

Insects, for instance, are also able to detect sourness in food – lower concentrations are perceived as attractive whereas greater concentrations are repulsive (Shrestha and Lee 2021; Rimal et al. 2019). To ‘taste’ chemicals in their environment, the common fruit fly, Drosophila melanogaster, employs tasting organs in its mouthparts, legs and wings. In the external mouthparts, organs termed the ‘labella’ house highly specific neurons which harbour receptors for individual chemicals e.g. sugars and metals (Dahanukar et al. 2007; Li et al. 2023), or less specific receptors for varieties of chemicals e.g. carboxylic acids (Shrestha and Lee 2021).

Once ingested, the food is then additionally assessed by neurons in the pharynx. However, the involvement of these neurons in perceiving a sour taste is largely unexplored. Bhanu Shrestha and colleagues, of Kookmin University, South Korea, sought to address this gap in knowledge, aiming to shed light on the intricate mechanisms underlying taste in insects.

First, the preprint authors attempted to identify the receptor responsible specifically for attractive sourness.

How though can the ability of a fly to discern sourness be measured? Well, two foods are prepared for the flies – one containing sugar only which is coloured red, and the other containing sugar plus a small amount of carboxylic acid which is coloured blue. A starved fly then makes a decision – do I prefer the red food or the blue food? After feasting, the colour of its belly is checked – is it red, blue, or purple? The colour of its gut therefore betrays which food the fly favoured.

After diligently assessing over 30 different taste receptors, Shrestha found that flies lacking receptors IR51b, IR94a or IR94h had a lower preference for the ‘sour’ food. These therefore might be receptors specific for sourness.

The authors also assessed the ability of the labella in mutant flies that lack these proposed sour taste receptors to respond to sourness. To do this, their electrical activity needed to be tested in the same manner as how an ECG reveals the electrical activity of the heart. Electrodes placed at the labella, however, revealed no difference in electrical activity in mutant flies, meaning that although these receptors are essential for perceiving sourness, they don’t function in the external mouthparts. Instead, further experimentation revealed that these receptors are found internally in the pharynx (Fig. 1).

Figure 1. Location of pharynx neurons that display IR94a and IR94h sour-sensing receptors within the fly head. IR94a is exclusively found in the ventral cibarial sense organs (VCSO), while IR94h is found in both the VCSO and labral sense organs (LSO). The VCSO and LSO make up part of the pharynx.

Finally, Shristha and colleagues wanted to confirm that activating the pharynx neurons that harbour these receptors causes attraction to sourness. To do so, the team introduced the receptor TrpV1 into the same neurons. TrpV1 is sensitive to capsaicin – the chemical that makes chillies so hot. Fascinatingly, when flies in which the specific pharynx neurons were activated were given the choice between normal food and food containing capsaicin, they devoured the spicy food. This therefore means that those pharynx neurons, when activated, mediate attraction.

So, rather than with its mouthparts, flies only perceive attractive levels of sourness once they have already ingested the food using specific sour-sensing neurons in the pharynx. As such, Shrestha and colleagues have revealed a previously unknown layer of complexity in the perception of sourness. How these neurons function, however, in the complex taste network as a whole remains to be determined. Ultimately, as this research proves, when it comes to sourness, it’s what’s on the inside that counts.

Why I chose this preprint:

I also work on Drosophila neurobiology however on an entirely different topic. I am always interested in research that reveals behaviour in flies that is similar to humans despite the two being so different. Prior to finding this paper, I was unaware that flies have different taste modalities, but of course that makes sense from an evolutionary perspective. I found that particularly intriguing.

Questions for the authors:

What is the reason for flies having multiple taste organs in the mouthparts, legs and wings?
Flies are able to vomit. Is this ever a response to repulsion from certain food? Or does this serve another purpose independent of taste?
If a food has high acidity but also a sufficiently high sugar content, can that outweigh a repulsive sour response?
Are the same receptors responsible for taste also present in olfactory organs? Or are these entirely different receptors?

References

Dahanukar, Anupama, Ya-Ting Lei, Jae Young Kwon, and John R. Carlson. 2007. “Two Gr Genes Underlie Sugar Reception in Drosophila.” Neuron 56 (3): 503–16.

Li, Xiaonan, Yuanjie Sun, Shan Gao, Yan Li, Li Liu, and Yan Zhu. 2023. “Taste Coding of Heavy Metal Ion-Induced Avoidance in Drosophila.” iScience 26 (5): 106607.

Rimal, Suman, Jiun Sang, Seeta Poudel, Dhananjay Thakur, Craig Montell, and Youngseok Lee. 2019. “Mechanism of Acetic Acid Gustatory Repulsion in Drosophila.” Cell Reports 26 (6): 1432–42.e4.

Shrestha, Bhanu, and Youngseok Lee. 2021. “Mechanisms of Carboxylic Acid Attraction in Drosophila Melanogaster.” Molecules and Cells 44 (12): 900–910.

Tags: behaviour, circuit, probscis

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