Taste and odorant receptors of the coelacanth—A gene repertoire in transition

Abstract

G-protein coupled chemosensory receptors (GPCR-CRs) aid in the perception of odors and tastes in vertebrates. So far, six GPCR-CR families have been identified that are conserved in most vertebrate species. Phylogenetic analyses indicate differing evolutionary dynamics between teleost fish and tetrapods. The coelacanth Latimeria chalumnae belongs to the lobe-finned fishes, which represent a phylogenetic link between these two groups. We searched the genome of L. chalumnae for GPCR-CRs and found that coelacanth taste receptors are more similar to those in tetrapods than in teleost fish: two coelacanth T1R2s co-segregate with the tetrapod T1R2s that recognize sweet substances, and our phylogenetic analyses indicate that the teleost T1R2s are closer related to T1R1s (umami taste receptors) than to tetrapod T1R2s. Furthermore, coelacanths are the first fish with a large repertoire of bitter taste receptors (58 T2Rs). Considering current knowledge on feeding habits of coelacanths the question arises if perception of bitter taste is the only function of these receptors. Similar to teleost fish, coelacanths have a variety of olfactory receptors (ORs) necessary for perception of water-soluble substances. However, they also have seven genes in the two tetrapod OR subfamilies predicted to recognize airborne molecules. The two coelacanth vomeronasal receptor families are larger than those in teleost fish, and similar to tetrapods and form V1R and V2R monophyletic clades. This may point to an advanced development of the vomeronasal organ as reported for lungfish. Our results show that the intermediate position of Latimeria in the phylogeny is reflected in its GPCR-CR repertoire.

The Physiology of Taste in Fish: Potential Implications for Feeding Stimulation and Gut Chemical Sensing

“…Current evidence suggests that the ancestral genes responded to AAs and that, during the evolution of mammals, T1R2/T1R3 receptors acquired sugar-responding ability. Moreover, the coelacanth Latimeria chalumnae might be the first fish to recognize sweet substances (Oike et al, 2007;Picone et al, 2014). Accordingly, teleost T1R2s are more closely related to T1R1s (umami receptor) than to tetrapod T1R2s, while two coelacanth genes grouped together with the tetrapod, rather than the teleost, T1R2s (Picone et al, 2014).…”

“…Moreover, the coelacanth Latimeria chalumnae might be the first fish to recognize sweet substances (Oike et al, 2007;Picone et al, 2014). Accordingly, teleost T1R2s are more closely related to T1R1s (umami receptor) than to tetrapod T1R2s, while two coelacanth genes grouped together with the tetrapod, rather than the teleost, T1R2s (Picone et al, 2014). In the case of T2Rs, these responded to the bitter compound denatonium (Oike et al, 2007).…”

The taste system of small fish species

“…4) Concerning the G proteins that transduces the signals from T1R and cells are different between teleosts and mammals. 5) Co-expression patterns of taste signaling molecules are also different between species, showing the diversification of taste receptor cells in fish.…”

The Molecular Biology of Vertebrate Olfaction

“…The overall number of OR genes was reported to be similar to that of teleost fish but the distribution of OR genes among all of the α‐ζ and η subgroups is considered to be more similar to amphibians. Seven genes were identified which they propose may represent the ancestral clades of ORs for detecting airborne odors (Picone et al, ).…”