A singular shark bitter taste receptor provides insights into the evolution of bitter taste perception

Abstract

Many animal and plant species synthesize toxic compounds as deterrent; thus, detection of these compounds is of vital importance to avoid their ingestion. Often, such compounds are recognized by taste 2 receptors that mediate bitter taste in humans. Until now, bitter taste receptors have only been found in bony vertebrates, where they occur as a large family already in coelacanth, a “living fossil” and the earliest-diverging extant lobe-finned fish. Here, we have revisited the evolutionary origin of taste 2 receptors (T2Rs) making use of a multitude of recently available cartilaginous fish genomes. We have identified a singular T2R in 12 cartilaginous fish species (9 sharks, 1 sawfish, and 2 skates), which represents a sister clade to all bony fish T2Rs. We have examined its ligands for two shark species, a catshark and a bamboo shark. The ligand repertoire of bamboo shark represents a subset of that of the catshark, with roughly similar thresholds. Amarogentin, one of the most bitter natural substances for humans, also elicited the highest signal amplitudes with both shark receptors. Other subsets of ligands are shared with basal bony fish T2Rs indicating an astonishing degree of functional conservation over nearly 500 mya of separate evolution. Both shark receptors respond to endogenous steroids as well as xenobiotic compounds, whereas separate receptors exist for xenobiotics both in early- and late-derived bony vertebrates (coelacanth, zebrafish, and human), consistent with the shark T2R reflecting the original ligand repertoire of the ancestral bitter taste receptor at the evolutionary origin of this family.

Membrane-bound chemoreception of bitter bile acids and peptides is mediated by the same subset of bitter taste receptors

“…6 ) suggests that for these receptors the co-sensitivity might originate from a common ancestral receptor. In light of the strong functional conservation of phylogenetically old bitter taste receptors such as in sharks [ 44 ] and bony fish [ 13 ], a selective pressure originating from the need to maintain an extra-gustatory function, e.g. to detect endogenous agonists such as bile acids, could counteract the rapid evolutionary development of xenobiotics-directed detection properties and hence, a gene sharing mechanism similar to crystallin genes [ 45 ] could exist.…”

Influence of Sodium Chloride on Human Bitter Taste Receptor Responses

“…The functional screening experiments were performed in accordance with earlier publications. − HEK 293T-Gα16gust44 cells were grown in poly- d -lysine-coated 96 well plates under standard conditions (DMEM, 10% FCS, 1% penicillin/streptomycin, 1% glutamine; 37°C, 5% CO 2 , 95% humidity), and lipofectamine 2000 (Thermo Fisher Scientific, Darmstadt, Germany) was used to transiently transfect cells with TAS2R cDNA constructs. Empty vector (mock) was used to transfect cells as a negative control.…”