Character of sour taste receptor: when mammals hate intense sour taste how birds can snack it on its plate; whether preference or tolerance

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Tapas Kumar Goswami

Department of Microbiology, Institute of Veterinary Science and Animal Husbandry, Siksha “O”Anusandhan (Deemed to be University), Bhubaneswar-751030, Odisha, India

Corresponding Author Email: goswami.tapas@gmail.com

DOI : https://doi.org/10.51470/AMSR.2025.04.02.04

Abstract

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Introduction

Taste is essential for life, and human beings prefer tasty food. The sense of taste acts as a dominant controller and motorist of feeding behavior in living creatures. Sense of taste has been viewed as a nutritional quality control device. Mammals can perceive taste using taste receptors present on the tongue and palate, whereas flies can sense through gustatory receptor neurons (GRNs), distributed over the head, body, and legs {1}. Gustation is one of the chemosensory systems arbitrated by taste receptors present in the oral cavity of avian species. These receptors are strategically present on taste buds (sensory organs). Except for hagfish, all other vertebrates carry taste buds. The taste system has evolved to descry applicable composites, including amino acids and peptides, carbohydrates, lipids, calcium, salts, and toxic or antinutritional compounds present in food. Taste is also vital for life, and it sends a distressing signal for toxic substances. Tastes of foods are perceived under five categories those are sweet, sour, bitter, salty, and umami.  Each of these is recognised by a specific receptor. Additionally, a few other “secondary” tastes such as fat taste, metallic taste, astringency and kokum are also perceived by sensory taste receptors {2}. Generally, a slight touch of sour is pleasant, but deep sour is repulsive for humans. Neonatal babies can identify the sour taste and pucker their lips. Conceivably this repulsive behaviour towards extreme sour taste is an inbuilt safeguard machinery that warns against stale and putrefied food which becomes sour due to bacterial growth, like rancid milk {3}. Earlier, we described why cat prefer fish but decline sweet dishes {4}. During the elaboration of sour taste, the subject of acidity in terms of pH (potential of hydrogen) needs a brief content. Credit goes to a Danish scientist, S.P.L. Sørensen, who introduced the pH scale (0 to 14) in 1909, and a pH detecting equipment in the form pH meter was introduced in 1934 by Arnold Beckman, which facilitated the study of sour taste. The test of pure chemicals revealed that the taste of hydrochloric acid (HCl) is sour and a little bitter, and astringent {5}. Likewise, organic acids including citric, tartaric, and malic acids, with a sour taste proportional to their pH were also noted. This has handed the first signal that protons are required to elicit the sour taste. The sourness of a substance doesn’t depend only on the concentration of hydrogen ions (pH); there are a few more factors at play, so weak (organic) acids taste much sour. {6}. Aristotle, in his work On Sense and the Sensible, wrote that “all animals are nourished by the sweet” (panta ta zōiatrephetaitōglykōi). By “sweet,” he meant substances that were nutritive and energy-providing—what we now recognize as calorie-rich sugars and carbohydrates. {1}. Humans have a liking towards fruits with a sweet taste, and mammals are aversive towards sour taste, whereas numerous birds happily consume highly acidic fruits like zesty lemons to unripe honey mangoes of sour taste. Evolutionary biologists suggest that the perception of sour taste was probably the earliest gustatory sense to evolve. With scientific support, it has been predicted that the necessity of sensing acidic environments appeared in jawless vertebrates, which were filter-feeding organisms that gathered food particles from the water in a non-selective manner {7}. A recent report has revealed the genetic basis of sour taste perception in birds. The mechanism behind sour tolerance of birds is due to certain changes in their sour taste receptor.  A recent report has revealed that the inherited gene regulates the sour taste perception in birds. The degree of tolerance to sourness among avian species is due to certain changes in their sour taste receptors. As per scientific data, there are nearly 9,700 species of birds across the globe {8}. The only gene so far associated with the sour taste receptor is called OTOP1. Just seven years ago, scientists discovered a sour taste receptor in vertebrates called otopetrin1{9}. Findings from electrophysiological recordings have shown that OTOP1 is activated by both acid and alkali, and protons are transferred inside or outside the cell membrane in response to extracellular acid or alkali stimulation.

Sour taste receptor as a proton gatekeeper.

Unlike mammalian species, the tongue of birds is devoid of taste papillae. Because birds secrete very little saliva and swallow food rapidly, avian species retain food in the oral cavity for only a short time. Birds are a highly diverse group of vertebrates, with more than 10,000 species identified. Compared to humans, they have a relatively poor sense of taste, as they possess far fewer taste buds. For example, chickens have about 767 taste buds, whereas humans have approximately 7,902. {10}.The avian tongue is not considered a major sensory organ. Its surface is typically covered by keratinized lingual epithelium and generally lacks appendages or specialized structures such as taste papillae {11}. In birds, most taste buds are located on the soft, glandular epithelia of the palate {12}. Each taste bud consists of a cluster of approximately 50–100 cells. These taste buds are distributed across the lingual epithelium, palate, upper oesophagus, pharynx, and larynx. Within a taste bud, elongated taste receptor cells are densely packed, projecting an apical process into a taste pore, an opening in the epithelial surface measuring ~2–10 μm in diameter. Based on ultrastructural features, taste cells are classified into four types (I–IV). Among these, type II and type III cells are responsible for transducing sensory signals, whereas type IV cells act as basal precursor cells, and type I cells are glial-like supportive cells, whose precise role remains unclear {13}. Otopetrin-1 (OTOP1) was first identified for its role in the vestibular system, where it is essential for maintaining balance, sensing gravity, and coordinating limb orientation. Mutations in this gene are linked to vestibular disorders {14}. OTOP1 encodes a highly conserved multi-transmembrane protein found across vertebrates, arthropods, and nematodes. It is strongly expressed in brown and white adipose tissue, mast cells, adrenal glands, and in both vestibular and taste cells. Functionally, OTOP1 contributes to the development of gravity-sensing otoconia in the vestibular system by forming proton-mediated ion channels.Uniquely, it acts as a proton-activated channel (fig. 1), allowing protons (H⁺ ions) to cross cell membranes {9}.Sour taste in vertebrates is triggered by acidic pH and by organic acids, such as acetic acid, that can cross the cell membrane {1}. Across species, the perception of sourness may be either pleasant or aversive, depending on its intensity, the context, the species, and other factors. Preference for sourness typically follows an ‘inverted U-shaped pattern,’ where liking increases with acidity up to a point, but declines at higher concentrations {15}. In mice, acid-sensing taste receptor cells are enriched with OTOP1, which mediates Zn²⁺-sensitive proton conductance. Two additional murine genes, Otop2 and Otop3, as well as a Drosophila ortholog, also encode proton channels. The evolutionary conservation of this gene family and its widespread tissue distribution suggest a fundamental role for proton channels in physiology and pathophysiology {9}. High sodium (Na⁺) and hydrogen ions (H⁺) elicit salty and sour tastes, respectively, and are detected by type III taste receptor cells (TRCs) within taste buds. The mechanisms underlying salt and sour taste perception differ from those for sugars, bitter compounds, and L-glutamate, which are sensed by type II TRCs. However, genetic analysis of the OTOP1 gene provides limited insight into the evolutionary changes of sour taste. This is because the OTOP1 receptor is not exclusively expressed in taste cells but is also widely distributed in brown and white adipose tissue, mast cells, adrenal glands, and vestibular cells of the inner ear. Consequently, interspecies or population differences in OTOP1 are not necessarily attributable to selection for sour taste perception, nor do they primarily reflect changes in sour taste. For instance, certain OTOP1 mutations are instead associated with vestibular disorders {14}. Nonetheless, recent studies have emphasized its critical role in mediating cellular and neural responses to sour stimuli {16}. The protein OTOP1 also functions as a sensor for ammonium chloride and alkali, highlighting its broader role in taste perception {17}. Many cultivated fruits, such as sweet oranges derived from a sour orange × mandarin cross, exhibit reduced acidity compared to their wild ancestors. Regulatory genes underlying fruit acidity suggest that ancestral counterparts were several times more acidic than present-day cultivars {18}. While sourness is generally aversive to most mammalian species, many birds show tolerance and readily consume acidic fruits without disinclination. In mammals, acids often evoke discomfort and even pain because they activate both taste receptors and somatosensory neurons innervating the oral cavity. Early electrophysiological studies demonstrated that exposure of the tongue to acids generates electrical activity in taste nerves, likely representing the fundamental neural basis of sour taste perception {9}. Taste behaviour, taste receptor function, and feeding preferences are closely associated to ecological adaptations in animals {20}. From experimentation on avian species, it has been revealed that the taste rejection responses and thresholds for acid aversion differ considerably among birds. For example, feral pigeons (Columba livia) completely rejected an acidic solution of 0.02 N HCl, while Barred Plymouth Rock–Rhode Island Red cross-bred chicks required a concentration of 0.1 N for a similar rejection response. In contrast, Bobwhite quail (Colinus v. virginianus) did not fully reject acidic solutions until exposed to concentrations as high as 0.5 N HCl {21}. These findings suggest that taste perception plays a significant role in dietary selection, influencing the nutritional ecology of different bird species in nature {22}.

Preference or tolerance

Several approaches, such as pharmacological interventions in avian species, transgenic models of mice, and chimeric receptor designing to probe receptor function, have given supporting evidence that sour tolerance is linked with the functional evolution of OTOP1. Data obtained from animal behaviour studies suggested that birds can tolerate higher levels of sour taste. Among avian families, ~60% of bird families have fruit-taking behaviour. Prevalence of fruit-taking behaviour among avian phylogeny has shown that in nature, birds consumed ripe fruits having a pH range from 2.5 to 3.5 {23}. As this feeding behaviour is observed in their natural habitat and not derived from forceful feeding experimental data, so scientists are of the view that tolerance to the low pH of fruits might have evolved gradually in nature. While domestic pigeons and canaries have exhibited a slight aversion to citric acid at 10-and 20-mM concentrations, unlike to it, repulsive responses towards similar concentrations of citric acid were observed in rodents’ families (mice, rat, and shrews), which are closer to primates; this provides some clue that birds are more tolerant towards acidic food. Several studies have confirmed the expression of the Otop1 gene in oral tissues such as the palate, pharynx, and tongue. In addition, heterologous expression of Otop1 has been successfully established in the HEK293 human cell line.” The physiological function of both the expressed mouse and pigeon OTOP1 receptor was found to be acid-activated ion channels. It indicates that OTOP1, whether of mouse or avian species, once expressed in phylogenetically distinct cell types like the human kidney, yet its functional character as an ion channel remains unchanged. However, with the lowering of pH from 3.5 to 2.5, the magnitude of current flow through the ion channel (OTOP1) increases in the case of mouse OTOP1, and for pigeon, the current flow decreases at the lowering of pH, as observed in a recent report {24}. The magnitude of current flow through OTOP1 of mouse and pigeon in response to pH variation, as reported by Zhang and his team (not exact data, rather representative values) may be elaborated in a graphical representation for better understanding (fig-2).This finding has specified that the activity of the mouse OTOP1 receptor escalates with an increase in acidity. It means more acidic foods are recognised to mice, and other mammals, including humans, as increasingly sour. However, the pigeon and canary versions of OTOP1 became less active in acidic solutions. For example, an acidic lemon would not feel as much of a sour taste, allowing the birds to take advantage of the fruits that mammals cannot consume. Cell biology and functional tests have suggested polycystic-kidney disease-like (PKD) ion channel, PKD2L1, and its associated partner, PKD1L3, the members of transient receptor potential (TRP) ion channel families function as a likely candidate for a mammalian sour taste receptor {25}.Various mechanisms, including acid-sensing ion channels (ASICs), hyperpolarization-activated cyclic nucleotide-gated (HCN) channels, and two-pore domain K+ channels (K2P) have been proposed to serve in the detection of sour taste.{26}. Carvacrol, a phenolic compound a novel OTOP1 channel agonist that activates the OTOP1 channel, independent of extracellular protons. Carvacrol activates the mouse OTOP1 (mOTOP1) channel under neutral and acidic conditions. The Carvacrol compound restrictively stimulates mouse OTOP1, whereas under neutral pH conditions, OTOP1 of green sea turtle (Chelonia mydas, CmOTOP1) remains insensitive to carvacrol induction. {27}. Nootkatone, a highly valued citrus flavour originally isolated from the heartwood of the Nootka cypress (Callitropsis nootkatensis), has also been utilized as a natural insect repellent and insecticide {28}. The same compound has been used as a pharmacological agent to detect its agonistic effect on the OTOP1 receptor of birds. Taste receptor OTOP1 of pigeons and canaries has never shown a preference for either nootkatone or vehicle (blank). Experiment with citric acid, the birds exhibited avoidance of acid when nootkatone was added to it, but not to acid only. It indicated the agonistic effect of nootkatone towards sour taste through inhibition of OTOP1. Subsequently, using the knock-in approach in mice, replacing mOTOP1 with cOTOP1, it has been observed that inhibition of OTOP1 confers mouse gustatory nerve with sour tolerance. While mutating the OTOP1gene of several avian and mammalian species has identified four candidate amino acids as conserved residues (H239, L306, H314, and G378) within the protein that are responsible for sour tolerance in birds. Similarly, sequence analysis of several mammalian and avian species has given a strong indication that residue H314 to be critical and conserved in birds. Sequence alignment studies of OTOP1 have shown H239 (Histidine at position 239) is conserved across jawed vertebrates, whereas residue G378, exclusively present in canary species, provides greater sour tolerance than the pigeon, which lacks this variance {24}.

Conclusion

Gustation and taste are the same terminology used in biological science for the chemo-sensory system present in the oral cavity of avian species. It has been predicted that the enhanced sour tolerance in birds probably appeared several million years ago. As per the view of evolutionary ornithologists, seed dispersion through the feces of birds is the natural way of propagation of plants to a distant location. A single-residue mutation (G378) in OTOP1 further increases acid-induced inhibition of songbirds so making them further sour-tolerant. In a comparative scale, canaries are more acid-tolerant than pigeons.  It is not clear how the sour taste evolved. Sour taste likely evolved in ancient fish and has not been lost in most vertebrate species. A neonate human baby can recognise sour taste and once allowed to taste sour food, they pucker their lips.{29}. Most species are aversive to sour taste, and a few avian species are more tolerant of acidic taste than their other counterparts. The receptor for sour taste is OTOP1, an unusual type of protein that allows the proton to cross the cell membrane, influencing taste perception. Acid-tolerance behaviour of birds can be judged in the reproductive interest of plants to bear their fruits for the taste preferences of birds. Simultaneously, fruit consumption behaviour of birds positively supports the maintenance of global vegetation through seed dispersion. In a larger perspective, consumption of acidic fruits favours the existence of birds and supports their survival during periods of food scarcity. Fruits having a sweet and sour taste combination allow different avian species to satisfy their respective preference and survival without competing each other on the same fruit.

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