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 signaling 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 signaling. 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 thirty bilaterian neuropeptide precursor families were identified, some of which occur as paralogs. Furthermore, homologs 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 ~270 million years by analysing sequence data from over fifty 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.

Recent advances in neuropeptide signaling in Drosophila, from genes to physiology and behavior

“…This include neuropeptide S (NPS) and crustacean cardioactive peptide (CCAP), orexin and allatotropin, neuropeptide FF/gonadotropin-inhibitory hormone (GnIH) and SIFamide galanin and allatostatin-A (Ast-A), as well as a link between vertebrate endothelin/gastrin-releasing peptide/neuromedin-B peptides and protostomian CCHamide/elevenin/GGNG peptides. Similar in silico analyses combined with receptor characterization studies in recent years have now increased the number of this core-set of bilaterian neuropeptides [36,57,62,66,139]. Thus, the origins of as many as 30 neuropeptide genes/families can now be traced back to Urbilateria as orthologs of several vertebrate neuropeptide signaling systems have been identified in insects and other protostomes ( Fig.…”

“…Interestingly, a NUCB precursor is encoded in the Drosophila genome as well as in the transcriptomes of various echinoderms (deuterostomian invertebrates) [62];…”

“…At first, the massive amount of new information mined from sequence databases was daunting, but with the rapid development of powerful genetic and imaging tools much experimental progress has been made to increase the understanding of the multiple functions of neuropeptides, especially in the worm Caenorhabditis elegans [see [39,[47][48][49][50][51][52][53][54][55][56]] and the fly Drosophila melanogaster (as will be discussed in this review) and more recently, in the marine annelid Platynereis dumerilii [57][58][59][60][61]. It is generally accepted that many of the genes encoding neuropeptides and peptide receptors in insects and other invertebrates are ancestrally related to those found in mammals [32,33,44,57,62], and recent work has suggested that in quite a few cases functions of peptidergic signaling are also partly conserved over evolution [19,23,[63][64][65][66]. Thus, invertebrates with their less complex neuronal and endocrine systems are being explored as models of neuropeptide signaling in a variety of functions [reviewed in [1, 2, 5-7, 9, 10, 30, 31, 43, 46, 67-74]].…”

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

“…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, ), holothurians (e.g., the sea cucumber A. japonicus ; Rowe, Achhala, & Elphick, ) and ophiuroids (e.g., the brittle star Ophionotus victoriae ; Zandawala et al, ). However, nothing is known about the physiological roles of PP/OK‐type neuropeptides in other echinoderms.…”

Functional characterization of a second pedal peptide/orcokinin‐type neuropeptide signaling system in the starfish Asterias rubens

“…It will be interesting, therefore, to investigate if PPLN2‐type peptides also act as muscle relaxants in starfish that belong to other starfish orders—for example, in P. pectinifera and/or A. planci , both of which are species belonging to the order Valvatida. Looking beyond starfish, it would be of interest to determine if PP/OK‐type neuropeptides act as muscle relaxants in other echinoderms Addressing this issue is feasible because precursors of PP/OK‐type neuropeptides have been identified in other echinoderms, including two precursors in the sea urchin S. purpuratus (SpPPLNP1 and SpPPLNP2; Rowe & Elphick, ), one precursor in the sea cucumber A. japonicus (Rowe, Achhala, & Elphick, ) and one or more precursors in several brittle star species (Zandawala et al, ).…”