Discovery of a second SALMFamide gene in the sea urchin Strongylocentrotus purpuratus reveals that L-type and F-type SALMFamide neuropeptides coexist in an echinoderm species

Abstract

The SALMFamides are a family of neuropeptides that act as muscle relaxants in the phylum Echinodermata. Two types of SALMFamides have been identified in echinoderms: firstly, the prototypical L-type SALMFamide peptides with the Cterminal sequence Leu-X-Phe-NH 2 (where X is variable), which have been identified in several starfish species and in the sea cucumber Holothuria glaberrima; secondly, F-type SALMFamide peptides with the C-terminal sequence Phe-X-Phe-NH 2 , which have been identified in the sea cucumber Apostichopus japonicus. However, the genetic basis and functional significance of the occurrence of these two types of SALMFamides in echinoderms are unknown. Here we have obtained a new insight on this issue with the discovery that in the sea urchin Strongylocentrotus purpuratus there are two SALMFamide genes. In addition to a gene encoding seven putative Ftype SALMFamide neuropeptides with the C-terminal sequence Phe-X-Phe-NH 2 (SpurS1-SpurS7), which has been reported previously (Elphick and Thorndyke, 2005; J. Exp. Biol., 208, 4273-4282 [1]), we have identified a gene that is expressed in the nervous system and that encodes a precursor of two putative L-type SALMFamide neuropeptides with the C-terminal sequences Ile-X-Phe-NH 2 (SpurS8) and Leu-XPhe-NH 2 (SpurS9). Our discovery has revealed for the first time that L-type and Ftype SALMFamide neuropeptides can coexist in an echinoderm species but are encoded by different genes. We speculate that this feature of Strongylocentrotus purpuratus may apply to other echinoderms and further insights on this issue will be possible if genomic and/or neural cDNA sequence data are obtained for other echinoderm species.3

The neuropeptide transcriptome of a model echinoderm, the sea urchin Strongylocentrotus purpuratus

“…These findings demonstrated that known neuropeptide precursors are represented amongst the collection of 2026 radial nerve ESTs analysed, providing an important indication that more detailed scrutiny of the EST dataset might reveal additional neuropeptide precursors. The first novel neuropeptide precursor identified by analysis of the EST dataset was the L-type SALMFamide precursor reported previously [68], which we have designated as ''S. purpuratus neuropeptide precursor 1'' or Spnp1 (Figs.…”

“…Here we present a complementary strategy, namely the analysis of expressed sequence tag (EST) data obtained from a S. purpuratus nerve cord cDNA library. We recently demonstrated the utility of this approach with the identification of a second SALMFamide precursor gene in S. purpuratus (Spnp1; [68]) and here we have extended the use of this approach with the identification of 19 other putative neuropeptide precursor genes (Spnp2 -Spnp20). The data presented here provide novel insights on the evolution of neuropeptide signaling systems as well as providing a basis for studies in which the expression and physiological/ behavioral roles of neuropeptides are investigated in a model echinoderm species.…”

The Protein Precursors of Peptides That Affect the Mechanics of Connective Tissue and/or Muscle in the Echinoderm Apostichopus japonicus

“…Three of these are also putative F-type SALMFamide neuropeptides: ARYSPFTFamide, GHRGGQFSQFKFamide and FKSSFYLamide. However, the third peptide, FKSSFYLamide, is unusual because it has a C-terminal leucine residue, whereas all of the SALMFamide neuropeptides previously identified in echinoderms have a C-terminal phenylalanine residue [14], [29]. In addition, the precursor contains the putative peptide GVPPYVVKVTYamide, which exhibits even greater structural divergence from the SxL/FxFamide motif that characterises SALMFamides.…”

“…This is interesting because analysis of sequence data from the sea urchin S. purpuratus revealed that in this species F-type and L-type SALMFamide neuropeptides are encoded by different genes, with seven F-type SALMFamides (SpurS1 – SpurS7) derived from one precursor protein and two L-type SALMFamides (SpurS8 and SpurS9) derived from a second precursor protein [29], [30]. The existence of a SALMFamide precursor in A. japonicus containing both F-type and L-type SALMFamides may reflect conservation of a characteristic of the common ancestor of sea cucumbers and sea urchins.…”

“…Accordingly, the existence of separate precursors for F-type and L-type SALMFamides in S. purpuratus is presumably a consequence of duplication of a single SALMFamide gene in an ancestor of sea urchins, with subsequent loss of L-type and F-type SALMFamides in the gene copies that gave rise to genes encoding F-type and L-type SALMFamide precursors in S. purpuratus , respectively. Thus far, F-type SALMFamides have only been found in sea cucumbers and sea urchins, whereas L-type SALMFamides have been found in all echinoderms for which peptide sequence data are available (starfish, sea cucumbers and sea urchins) [29]. It is possible, therefore, that L-type SALMFamides occur throughout the echinoderms, with F-type SALMFamides being restricted to the echinoderm clade comprising extant holothurians and echinoids.…”