A new subfamily of ionotropic glutamate receptors unique to the echinoderms with putative sensory role

Abstract

Chemosensation is a critical signalling process in animals and especially important in sea cucumbers, a group of ecologically and economically important marine echinoderms (Class Holothuroidea), which lack audio and visual organs and rely on chemical sensing for survival, feeding and reproduction. The ionotropic receptors are a recently identified family of chemosensory receptors in insects and other protostomes, related to ionotropic glutamate receptor family (iGluR) a large family of membrane receptors in metazoan. Here we characterize the echinoderm iGluR subunits and consider their possible role in chemical communication in sea cucumbers. Sequence similarity searches revealed that sea cucumbers have in general a higher number of iGluR subunits when compared to other echinoderms. Phylogenetic analysis and sequence comparisons revealed GluH as a specific iGluR subfamily present in all echinoderms. Homologues of the vertebrate GluA (aka αamino-3-hydroxy-5-methyl-4-isoxazolepropionic acid, AMPA), GluK (aka kainate) and GluD (aka delta) were also identified. The GluN (aka N-methyl-d-aspartate, NMDA) as well as the invertebrate deuterostome subfamily GluF (aka phi) are absent in echinoderms. The echinoderm GluH subfamily shares conserved structural protein organization with vertebrate iGluRs and the ligand binding domain (LBD) is the most conserved region and genome analysis indicates evolution via lineage and speciesspecific tandem gene duplications. GluH genes (named Grih) are the most expressed iGluRs subunit genes in tissues in the sea cucumber Holothuria arguinesis, with Griha1, Griha2 and Griha5 exclusively expressed in tentacles, making them candidates to have a chemosensory role in this species. The multiple GluH subunits may provide alternative receptor assembly combinations, thus expanding the functional possibilities and widening the range of compounds detected during aggregation and spawning in echinoderms.

Chemical communication and its role in sexual selection across Animalia

“…Chemoreceptors are encoded by some of the fastest evolving and largest gene families in the metazoan genome 185 and in some species evolved under sexual selection 186,187 . Although chemoreceptor repertoires are well-characterized primarily in vertebrates and insects 188 , this list is likely to grow rapidly with the number of animal genomes sequenced [189][190][191][192][193][194] , putting in reach an understanding of how sexual selection shapes receiver evolution at a molecular level but macroevolutionary scale. 2.…”