Transcriptomic discovery and comparative analysis of neuropeptide precursors in sea cucumbers (Holothuroidea)

Abstract

Neuropeptides synthesized and released by neuronal cells play important roles in the regulation of many processes, e.g. growth, feeding, reproduction, and behavior. In the past decade, next-generation sequencing technologies have helped to facilitate the identification of multiple neuropeptide genes in a variety of taxa, including arthropods, molluscs and echinoderms. In this study, we extend these studies to Holothuria scabra, a sea cucumber species that is widely cultured for human consumption. In silico analysis of H. scabra neural and gonadal transcriptomes enabled the identification of 28 transcripts that encode a total of 26 bilaterian and echinoderm-specific neuropeptide precursors. Furthermore, publicly available sequence data from another sea cucumber, Holothuria glaberrima, allowed a more in-depth comparative investigation. Interestingly, two isoforms of a calcitonin-type peptide precursor (CTPP) were deduced from the H. scabra transcriptome - HscCTPP-long and HscCTPP-short, likely the result of alternative splicing. We also identified a sea cucumber relaxin-type peptide precursor, which is of interest because relaxin-type peptides have been shown to act as gonadotropic hormones in starfish. Two neuropeptides that appear to be holothurian-specific are GLRFA, and GN-19. In H. scabra, the expression of GLRFA was restricted to neural tissues, while GN-19 expression was additionally found in the longitudinal muscle and intestinal tissues. In conclusion, we have obtained new insights into the neuropeptide signaling systems of holothurians, which will facilitate physiological studies that may enable advances in the aquaculture of sea cucumbers.

Characterization of an evolutionarily conserved calcitonin signaling system in a lophotrochozoan, the Pacific oyster (Crassostrea gigas)

“…Besides these similarities, there were clearly two types of peptides based on the spacing of the cysteine residues: with respect to the cleavage site, the CTa-types displayed the C9/8XC motif, while the CTb-types displayed the C7XC motif. The arrangement of the oyster CTPs with two mature peptides is particularly intriguing as deuterostome CT-type peptide precursors contain either a single peptide (Muff et al, 1995;Sekiguchi et al, 2009) or two peptides, as observed in echinoderm CT-type precursors (Rowe et al, 2014;Suwansa-ard et al, 2018;Zandawala et al, 2017). In the protostomes, the annelid P. dumerilii CT and DH31 precursors (Conzelmann et al, 2013) and the DH31 and CT-A precursors in arthropods (Alexander et al, 2018;Christie, 2008;Christie et al, 2010;Coast et al, 2001;Gard et al, 2009;Li et al, 2007;Veenstra, 2014 comprise only one peptide.…”

Evolution and Comparative Physiology of Luqin-Type Neuropeptide Signaling

“…Through analysis of transcriptome/genome sequence data, luqin-type neuropeptide precursors have subsequently been identified in other echinoderm classes, including Holothuroidea (sea cucumbers), Asteroidea (starfish or sea stars), and Ophiuroidea (brittle stars). In the sea cucumbers Apostichopus japonicus, Holothuria glaberrima, Holothuria scabra, and Holothuria leucospilota, the precursor comprises a single neuropeptide with the same predicted structure in all four species-KPYKFMRW-NH 2 (Rowe et al, 2014;Suwansa-Ard et al, 2018;Chen et al, 2019;Chieu et al, 2019). Luqin-type precursors identified in the starfish species A. rubens and Acanthaster planci comprise a single putative neuropeptide with the amino acid sequence EKGRFPKFMRW-NH 2 and EEKTRFPKFMRW-NH 2 , respectively Smith et al, 2017).…”

Changes in the neuropeptide complement correlate with nervous system architectures in xenacoelomorphs

“…Most transcriptomes were made from several whole adults and should thus include neuronal expression (see Supplementary Table 1 for details). To obtain reference and query sequences, we collected neuropeptide-precursor and neuropeptide receptor sequences from previous publications [1, 2, 54-60] and public databases (i.e., NCBI and UniProt). We aimed for a broad sampling across Bilateria and covered different clades of chordates (i.e., Craniata, Cephalochordata, and Urochordata), ambulacrarians (i.e, Echinodermata and Hemichordata) ecdysozoans (i.e., Nematoda and Arthropoda) and spiralians (i.e., Mollusca and Annelida).…”