The evolution of neuropeptide signalling: insights from echinoderms

Abstract

Neuropeptides are evolutionarily ancient mediators of neuronal signalling that regulate a wide range of physiological processes and behaviours in animals. Neuropeptide signalling has been investigated extensively in vertebrates and protostomian invertebrates, which include the ecdysozoans Drosophila melanogaster (Phylum Arthropoda) and Caenorhabditis elegans (Phylum Nematoda). However, until recently, an understanding of evolutionary relationships between neuropeptide signalling systems in vertebrates and protostomes has been impaired by a lack of genome/transcriptome sequence data from non-ecdysozoan invertebrates. The echinoderms-a deuterostomian phylum that includes sea urchins, sea cucumbers and starfish-have been particularly important in providing new insights into neuropeptide evolution. Sequencing of the genome of the sea urchin Strongylocentrotus purpuratus (Class Echinoidea) enabled discovery of (i) the first invertebrate thyrotropin-releasing hormone-type precursor, (ii) the first deuterostomian pedal peptide/orcokinin-type precursors and (iii) NG peptides-the 'missing link' between neuropeptide S in tetrapod vertebrates and crustacean cardioactive peptide in protostomes. More recently, sequencing of the neural transcriptome of the starfish Asterias rubens (Class Asteroidea) enabled identification of 40 neuropeptide precursors, including the first kisspeptin and melanin-concentrating hormone-type precursors to be identified outside of the chordates. Furthermore, the characterization of a corazonin-type neuropeptide signalling system in A. rubens has provided important new insights into the evolution of gonadotropin-releasing hormone-related neuropeptides. Looking forward, the discovery of multiple neuropeptide signalling systems in echinoderms provides opportunities to investigate how these systems are used to regulate physiological and behavioural processes in the unique context of a decentralized, pentaradial bauplan.

Keywords: echinoderms; evolution; genomics; neuropeptide; sea urchin; starfish.

Figure 1.

Echinoderm neuropeptides that have provided new insights into the evolution of neuropeptide signalling systems. The sequences of sea urchin (S. purpuratus) and starfish (A. rubens) representatives of six selected neuropeptide types are shown. Predicted or confirmed post-translational modifications, including conversion of an N-terminal glutamine (Q) to a pyro-glutaminyl (pQ) residue and conversion of a C-terminal glycine (G) to an amide group (-NH₂), are depicted and cysteine (C) residues that form or are predicted to form a disulphide bridge are underlined. Numbers in parentheses represent the number of copies of the neuropeptide in the corresponding precursor if this is greater than one. The image of S. purpuratus was obtained from https://openclipart.org/detail/170807/sea-urchin-silhouette, while the image of A. rubens was created by M. Zandawala (Stockholm University). Key: TRH: thyrotropin-releasing hormone; MCH: melanin-concentrating hormone; GnRH: gonadotropin-releasing hormone. References: (a) [54]; (b) [59]; (c) [60]; (d) [61]; (e) [62].

Figure 2.

Evolution of the VP/OT-type and NG peptide signalling systems. The diagram shows how duplication of a VP/OT-type neuropeptide signalling system in the common ancestor of the Bilateria gave rise to the highly conserved VP/OT-type (red boxes) and the divergent NPS (blue boxes), NG peptide (purple boxes) and CCAP-type (green boxes) signalling systems in extant bilaterians. Phyla where neuropeptide ligand–receptor pairs have been pharmacologically characterized are labelled with a yellow asterisk. A blue cross (and white box) represents loss of the NPS-type signalling system in the urochordates, while a red cross (and white box) represents loss of the CCAP-type signalling system in the nematodes. The image of S. purpuratus was obtained from https://openclipart.org/detail/170807/sea-urchin-silhouette, while images of other representative species from each phylum were obtained from http://phylopic.org or were created by the authors or by M. Zandawala (Stockholm University). References: (a) [84]; (b) [85]; (c) [86]; (d) [87]; (e) [88]; (f) [89]; (g) [63]; (h) [90]; (i) [91]; (j) [92]; (k) [74]; (l) [82]; (m) [93]; (n) [94]. (A colour version of this figure is available online at: https://academic.oup.com/bfg)

Figure 3.

The NG peptide family. Schematic showing an alignment of putative or confirmed neuropeptide(s) derived from NPS, NG peptide and CCAP-type precursors in representative species from phyla across the Bilateria. The conserved NG motif of NPS, NG peptides and CCAP-type peptides are highlighted in red and cysteine (C) residues that form or are predicted to form a disulphide bridge are underlined. A red cross represents loss of the NPS-type signalling system in the urochordates (e.g. C. intestinalis) or CCAP-type signalling system in the nematodes (e.g. C. elegans). Numbers in parentheses represent the number of copies of the neuropeptide in the precursor if this is greater than one. The image of S. purpuratus was obtained from https://openclipart.org/detail/170807/sea-urchin-silhouette, while images of other representative species from each phylum were obtained from http://phylopic.org or were created by the authors or by M. Zandawala (Stockholm University). Key: H. sapiens: Homo sapiens; C. intestinalis: Ciona intestinalis; B. floridae: Branchiostoma floridae; S. kowalevskii: Saccoglossus kowalevskii; S. purpuratus: Strongylocentrotus purpuratus; L. gigantea: Lottia gigantea; A. californica: Aplysia californica; P. dumerilii: Platynereis dumerilii; T. castaneum: Tribolium castaneum; C. elegans: Caenorhabditis elegans. References: (a) [74]; (b) [73]; (c) [59]; (d) [38]; (e) [64]; (f) [95]; (g) [96]. (A colour version of this figure is available online at: https://academic.oup.com/bfg)