Holothurians have a reduced GPCR and odorant receptor-like repertoire compared to other echinoderms

Nathalie Marquet,Sandra C. Silva,João C. R. Cardoso,Stefan A. Fernandes,Bruno Louro,Adelino V. M. Canário

doi:10.1038/s41598-020-60167-3

Abstract

Sea cucumbers lack vision and rely on chemical sensing to reproduce and survive. However, how they recognize and respond to environmental cues remains unknown. Possible candidates are the odorant receptors (ORs), a diverse family of G protein-coupled receptors (GPCRs) involved in olfaction. The present study aimed at characterizing the chemosensory GPCRs in sea cucumbers. At least 246 distinct GPCRs, of which ca. 20% putative ORs, were found in a transcriptome assembly of putative chemosensory (tentacles, oral cavity, calcareous ring, and papillae/tegument) and reproductive (ovary and testis) tissues from Holothuria arguinensis (57 ORs) and in the Apostichopus japonicus genome (79 ORs). The sea cucumber ORs clustered with those of sea urchin and starfish into four main clades of gene expansions sharing a common ancestor and evolving under purifying selection. However, the sea cucumber ORs repertoire was the smallest among the echinoderms and the olfactory receptor signature motif LxxPxYxxxxxLxxxDxxxxxxxxP was better conserved in cluster OR-l1 which also had more members. ORs were expressed in tentacles, oral cavity, calcareous ring, and papillae/tegument, supporting their potential role in chemosensing. This study is the first comprehensive survey of chemosensory GPCRs in sea cucumbers, and provides the molecular basis to understand how they communicate.

Highlights

All living organisms perceive and respond to chemical cues in their environment, which mediate a variety of activities such as feeding, predator avoidance, mating and social behaviours[1,2]
A large group of chemosensory receptors belong to the G protein-coupled receptors (GPCRs), one of the largest superfamilies of seven transmembrane domain receptors found in metazoans[8]
The H. arguinensis transcriptome originated a total of 1,580 contigs with five, six and seven predicted transmembrane domains (TMs), of which 474 were retained as putative GPCRs

Summary

Introduction

All living organisms perceive and respond to chemical cues in their environment, which mediate a variety of activities such as feeding, predator avoidance, mating and social behaviours[1,2]. Chemosensory functions have been associated with the glutamate-receptor family and the rhodopsin-type family[11,12] The latter contains the largest number and the most diverse repertoire of GPCRs involved in vertebrate olfaction[8]. A unique OR-like gene repertoire characterized by large groups of independently expanded receptor genes was described in the sea urchin Strongylocentrotus purpuratus genome (referred to as the surreal-GPCRs)[33] and in the crown-of-thorn starfish Acanthaster planci[34,35] These receptors have been mostly found in tissues that are in direct contact with the environment such as pedicellariae, spine, tube feet, mouth, body wall and tentacles, they were present in internal organs including stomach, testis and radial nerves[33,34,35,36]

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