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- A new subfamily of ionotropic glutamate receptors unique to the echinoderms with putative sensory rolePublication . Sania, Rubaiyat E.; Cardoso, João; Louro, Bruno; Marquet, Nathalie; Canario, AdelinoChemosensation 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 the 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 alpha-amino-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; genome analysis indicates evolution via lineage and species-specific tandem gene duplications. GluH genes (named Grih) are the most highly 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.
- Localization and distribution of nitric oxide synthase and other neuronal markers in the podia ofHolothuria arguinensisPublication . Marquet, Nathalie; Canario, Adelino; Power, DeborahThe organization of the nervous system of the holothurian podia-the tentacles, papillae, and tube feet-is still poorly understood, which limits the development of functional studies. Knowledge of nitric oxide (NO) signaling in sea cucumbers is nonexistent, although it is known to play an important role in many essential biological functions, including neurotransmission, throughout the animal kingdom. The objective of this study was to characterize the holothurian podia inHolothuria arguinensis. To this end, we used classical histology, nitric oxide synthase (NOS) distribution, using NADPH-diaphorase histochemistry and NOS immunostaining, and neuronal immunohistochemistry. Our results revealed an abundant distribution of NO in the nervous components of the holothurian podia, suggesting an important role for NO as a neuronal messenger in these structures. Nitrergic fibers were intensely labeled in the longitudinal nerve and the nerve plexus surrounding the stem, but were more weakly labeled in the mesothelium. NOS was also found in scattered cell bodies and abundant fibers in the podia terminal end (i.e., the discs in tentacles and tube feet, and the pointed conical structures in the papillae), with evident neuronal projections to the bud surface, especially in the tentacles. The podia terminal end was the most specialized area and was characterized by a specific nervous arrangement, consisting of a distinct nerve plate, rich in cells and fibers containing potential sensory cells staining positively for neuronal markers, which makes this the most likely candidate to be a chemosensory region and an important candidate for future exploration.
- Sea cucumbers, Holothuria arguinensis and H-mammata, from the southern Iberian Peninsula: variation in reproductive activity between populations from different habitatsPublication . Marquet, Nathalie; Conand, Chantal; Power, Deborah; Canario, Adelino; Gonzalez-Wanguemert, MercedesNew fisheries in the western Mediterranean and north eastern Atlantic target the sea cucumbers Holothuria arguinensis and H. mammata; however, lack of biological information hinders management decisions. Here, the reproductive biology of populations the two species was investigated in the southern Iberian Peninsula. Different populations located along a narrow latitudinal range displayed the same general reproductive pattern of summer-autumn spawning. However, significant differences in size, gonadal production and maturity profile between locations suggests the influence of site-specific factors. In Sagres and Ria Formosa H. arguinensis individuals were larger and had larger gonads than in Olhos de Agua, which had relatively more immature animals. The spawning and active gametogenesis periods were also longer in Sagres, possibly linked to specificity of food availability and tidal conditions. Ria Formosa also had larger H. mammata individuals with larger gonads than in Murcia and Olhos de Agua, possibly reflecting differences in feeding activity in different substrates (muddy/sandy vs rocky). Gametogenesis in H. arguinensis may be triggered by decreasing photoperiod and temperature, and spawning by increasing temperature. Altogether, these results, which include fecundity and size at first maturity, provide an important basis for the scientific management of sea cucumber fisheries in the region. (C) 2017 Elsevier B.V. All rights reserved.
- Holothurians have a reduced GPCR and odorant receptor-like repertoire compared to other echinodermsPublication . Marquet, Nathalie; Cardoso, João CR; Louro, Bruno; Fernandes, Stefan; Silva, Sandra; Canario, AdelinoSea 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.