Discovery of novel representatives of bilaterian neuropeptide families and reconstruction of neuropeptide precursor evolution in ophiuroid echinoderms

Abstract

Neuropeptides are a diverse class of intercellular signalling molecules that mediate neuronal regulation of many physiological and behavioural processes. Recent advances in genome/transcriptome sequencing are enabling identification of neuropeptide precursor proteins in species from a growing variety of animal taxa, providing new insights into the evolution of neuropeptide signalling. Here, detailed analysis of transcriptome sequence data from three brittle star species, Ophionotus victoriae, Amphiura filiformis and Ophiopsila aranea, has enabled the first comprehensive identification of neuropeptide precursors in the class Ophiuroidea of the phylum Echinodermata. Representatives of over 30 bilaterian neuropeptide precursor families were identified, some of which occur as paralogues. Furthermore, homologues of endothelin/CCHamide, eclosion hormone, neuropeptide-F/Y and nucleobinin/nesfatin were discovered here in a deuterostome/echinoderm for the first time. The majority of ophiuroid neuropeptide precursors contain a single copy of a neuropeptide, but several precursors comprise multiple copies of identical or non-identical, but structurally related, neuropeptides. Here, we performed an unprecedented investigation of the evolution of neuropeptide copy number over a period of approximately 270 Myr by analysing sequence data from over 50 ophiuroid species, with reference to a robust phylogeny. Our analysis indicates that the composition of neuropeptide ‘cocktails’ is functionally important, but with plasticity over long evolutionary time scales.

Pedal peptide/orcokinin‐type neuropeptide signaling in a deuterostome: The anatomy and pharmacology of starfish myorelaxant peptide in Asterias rubens

“…Abbreviations: LSM, longitudinal supra-ambulacral muscle; TF, tube foot; TIM, transverse infra-ambulacral muscle; TSM, transverse supra-ambulacral muscle. Scale bars: 200 lm in (a); 20 lm in (b), (c), (e), (f), (g); 100 lm in (d) anatomy of a neuropeptide signaling system in starfish has been adapted for life in different niches.Extending the comparative approach further, precursors of PP/ OK-type neuropeptides have been identified in three of the four other extant echinoderm classes: echinoids (e.g., the sea urchin S. purpuratus;Rowe & Elphick, 2012), holothurians (e.g., the sea cucumber A. japonicus;Rowe, Achhala, & Elphick, 2014) and ophiuroids (e.g., the brittle star Ophionotus victoriae;Zandawala et al, 2017). However, nothing is known about the physiological roles of PP/OK-type neuropeptides in other echinoderms.…”

A G-protein-coupled receptor mediates neuropeptide-induced oocyte maturation in the jellyfish Clytia

“…Much progress has been made in understanding the relationships between GPCR-neuropeptide families between protostomes and deuterostomes [20,25,28,35,36], and more recently with those in acoels and cnidarians [37]. We performed sequence-similarity based clustering to explore the relationship of the Clytia MIHR sequence with known GPCR families in Bilateria using established datasets from human and the annelid Platynereis [25,28 Fig.…”

Urbilaterian origin and evolution of sNPF-type neuropeptide signalling

“…The sequence of a transcript (contig 1060225; accession number MK033631.1) 183 encoding the precursor of an NPY-like neuropeptide has been reported previously based on 184 analysis of A. rubens neural transcriptome sequence data (Zandawala et al 2017). Here, a 185 cDNA encoding this precursor was cloned and sequenced, revealing that the open reading 186 frame encodes a 108-residue protein comprising a predicted 19-residue signal peptide, a 23-187 residue NPY-like peptide sequence with an N-terminal glutamine residue and a C-terminal 188 glycine residue, followed by a putative monobasic cleavage site (Supplementary Figure 1A).…”

“…PrRP-type genes supports the hypothesis that echinoderm sNPF-type neuropeptides are 490 orthologs of hemichordate PrRP-like and chordate PrRP-type neuropeptides. 491 492 Precursors of peptides that share sequence similarity with members of the bilaterian 520 NPY/NPF-type neuropeptide family were discovered recently in the phylum Echinodermata 521 (Zandawala et al 2017). These include proteins identified in several brittle star species (class 522…”

“…Furthermore, it was the sequence similarity that echinoderm peptides share with NPY/NPF-773 type peptides that originally facilitated their discovery (Zandawala et al, 2017). Additionally, 774…”