The Chemosensory Receptor Repertoire of a True Shark Is Dominated by a Single Olfactory Receptor Family

Abstract

Throughout the animal kingdom chemical senses are one of the primary means by which organisms make sense of their environment. To achieve perception of complex chemosensory stimuli large repertoires of olfactory and gustatory receptors are employed in bony vertebrates, which are characterized by high evolutionary dynamics in receptor repertoire size and composition. However, little is known about their evolution in earlier diverging vertebrates such as cartilaginous fish, which include sharks, skates, rays, and chimeras. Recently, the olfactory repertoire of a chimera, elephant shark, was found to be curiously reduced in odorant receptor number. Elephant sharks rely heavily on electroreception to localize prey; thus, it is unclear how representative their chemosensory receptor repertoire sizes would be for cartilaginous fishes in general. Here, we have mined the genome of a true shark, Scyliorhinus canicula (catshark) for olfactory and gustatory receptors, and have performed a thorough phylogenetic study to shed light on the evolution of chemosensory receptors in cartilaginous fish. We report the presence of several gustatory receptors of the TAS1R family in catshark and elephant shark, whereas TAS2R receptors are absent. The catshark olfactory repertoire is dominated by V2R receptors, with 5–8 receptors in the other three families (OR, ORA, TAAR). Species-specific expansions are mostly limited to the V2R family. Overall, the catshark chemosensory receptor repertoires are generally similar in size to those of elephant shark, if somewhat larger, showing similar evolutionary tendencies across over 400 Myr of separate evolution between catshark and elephant shark.

Mitral cell development in the olfactory bulb of sharks: evidences of a conserved pattern of glutamatergic neurogenesis

“…In the catshark, ciliated sensory neurons, the typical cell morphology of the main OE, are lacking, and the main receptor neurons of the olfactory mucosa of Scyliorhinus canicula are the microvillous receptor neurons and crypt neurons, whose projections show a segregated distribution in the OB (Theisen et al 1986; Ferrando et al 2009). Genomic studies indicate that VNS-specific genes are present in teleost fish (for review see: Grus and Zhang 2009), cartilaginous fish (Sharma et al 2019) and sea lamprey (Grus and Zhang 2009). In the catshark, V2R, a component of the vomeronasal signaling pathway, are the predominant chemosensory receptor family, and a small number of genes for chemosensory receptors of the main olfactory system are also present (Sharma et al 2019).…”

“…Genomic studies indicate that VNS-specific genes are present in teleost fish (for review see: Grus and Zhang 2009), cartilaginous fish (Sharma et al 2019) and sea lamprey (Grus and Zhang 2009). In the catshark, V2R, a component of the vomeronasal signaling pathway, are the predominant chemosensory receptor family, and a small number of genes for chemosensory receptors of the main olfactory system are also present (Sharma et al 2019).…”

“…Although we have observed regional differences in the combined expression of Tbr1 and Tbr2 in the OB of catshark, this observation does not allow us to reach any conclusion about the existence of an accessory component in the OB of the catshark. On the other hand, genomic and other cytological data (for review see: Ferrando and Gallus 2013: Sharma et al 2019) indicate that the vomeronasal-type receptors component are the predominant in the olfactory epithelium, whereas main olfactory receptors are minority; moreover, ciliated olfactory neurons were not found in the olfactory epithelium of catshark, which suggest that the olfactory mucosa of catshark may be similar to the vomeronasal epithelia of tetrapods. Further, studies of the expression/pattern of transcription factors and neuronal markers related with the specification/differentiation of different components of the vomeronasal system in the central nervous system are key to elucidate the existence of the brain areas/connections implicated in the processing of vomeronasal-type information in the catshark.…”

“…Several studies have been referred to the cell organization of the OE of the catshark, where sensory ciliated neurons, which in tetrapod vertebrates project to the MOB, are lacking; however, in the OE, microvillous olfactory receptor neurons and crypt sensory neurons are clearly recognizable (Theisen et al 1986; Ferrando et al 2006a, b, 2009, 2010, 2012; Zaccone et al 2011). In addition, genomic studies show that the predominant olfactory receptor type in the catshark and the elephant shark is the vomeronasal type2 receptor (V2R) (Sharma et al 2019). These evidences together with ultrastructural and immunohistochemical data indicate that in the catshark the olfaction could mainly rely on a VNS (Ferrando and Gallus 2013).…”

The evolutionary origins of the vertebrate olfactory system

“…In Chondrichthyes, it was observed that the sense of smell relies primarily on microvillous OSNs coupled to G α o [ 15 ]. The chemosensory receptor repertoire of cartilaginous fishes is dominated by the expanded V2R family, although there are also a few OR, TAAR and V1R genes [ 16 ]. As in teleosts, there is also the presence of crypt neuron-like cells but their exact receptor is unknown [ 17 ].…”