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Nemertean, brachiopod and phoronid neuropeptidomics reveals ancestral spiralian signalling systems.

ABSTRACT: Neuropeptides are diverse signalling molecules in animals commonly acting through G-protein coupled receptors (GPCRs). Neuropeptides and their receptors underwent extensive diversification in bilaterians and the relationships of many peptide-receptor systems have been clarified. However, we lack a detailed picture of neuropeptide evolution in lophotrochozoans as in-depth studies only exist for molluscs and annelids. Here we analyse peptidergic systems in Nemertea, Brachiopoda and Phoronida. We screened transcriptomes from thirteen nemertean, six brachiopod and four phoronid species for proneuropeptides and neuropeptide GPCRs. With mass spectrometry from the nemertean Lineus longissimus, we validated several predicted peptides and identified novel ones. Molecular phylogeny combined with peptide-sequence and gene-structure comparisons allowed us to comprehensively map spiralian neuropeptide evolution. We found most mollusc and annelid peptidergic systems also in nemerteans, brachiopods and phoronids. We uncovered previously hidden relationships including the orthologies of spiralian CCWamides to arthropod agatoxin-like peptides and of mollusc APGWamides to RGWamides from annelids, with orthologues systems in nemerteans, brachiopods and phoronids. We found that pleurin neuropeptides previously only found in molluscs are also present in nemerteans and brachiopods. We also identified cases of gene family duplications and losses. These include a protostome-specific expansion of RFamide/Wamide signalling, a spiralian expansion of GnRH-related peptides, and duplications of vasopressin/oxytocin before the divergence of brachiopods, phoronids and nemerteans. This analysis expands our knowledge of peptidergic signalling in spiralians and other protostomes. Our annotated dataset of nearly 1,300 proneuropeptide sequences and 600 GPCRs presents a useful resource for further studies of neuropeptide signalling.

SUBMITTER: Thiel D

PROVIDER: S-EPMC8557429 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Neuropeptides regulate intercellular signaling as neurotransmitters of the central and peripheral nervous systems, and as peptide hormones in the endocrine system. Diverse neuropeptides of distinct primary sequences of various lengths, often with post-translational modifications, coordinate and integrate regulation of physiological functions. Mass spectrometry-based analysis of the diverse neuropeptide structures in neuropeptidomics research is necessary to define the full complement of neuropeptide signaling molecules. Human neuropeptidomics has notable importance in defining normal and dysfunctional neuropeptide signaling in human health and disease. Neuropeptidomics has great potential for expansion in translational research opportunities for defining neuropeptide mechanisms of human diseases, providing novel neuropeptide drug targets for drug discovery, and monitoring neuropeptides as biomarkers of drug responses. In consideration of the high impact of human neuropeptidomics for health, an observed gap in this discipline is the few published articles in human neuropeptidomics compared with, for example, human proteomics and related mass spectrometry disciplines. Focus on human neuropeptidomics will advance new knowledge of the complex neuropeptide signaling networks participating in the fine control of neuroendocrine systems. This commentary review article discusses several human neuropeptidomics accomplishments that illustrate the rapidly expanding diversity of neuropeptides generated by protease processing of pro-neuropeptide precursors occurring within the secretory vesicle proteome. Of particular interest is the finding that human-specific cathepsin V participates in producing enkephalin and likely other neuropeptides, indicating unique proteolytic mechanisms for generating human neuropeptides. The field of human neuropeptidomics has great promise to solve new mechanisms in disease conditions, leading to new drug targets and therapeutic agents for human diseases. Graphical Abstract ?.

Project description:BackgroundBrachiopods and molluscs are lophotrochozoans with hard external shells which are often believed to have evolved convergently. While palaeontological data indicate that both groups are descended from biomineralising Cambrian ancestors, the closest relatives of brachiopods, phoronids and bryozoans, are mineralised to a much lower extent and are comparatively poorly represented in the Palaeozoic fossil record. Although brachiopod and mollusc shells are structurally analogous, genomic and proteomic evidence indicates that their formation involves a complement of conserved, orthologous genes. Here, we study a set of genes comprised of 3 homeodomain transcription factors, one signalling molecule and 6 structural proteins which are implicated in mollusc and brachiopod shell formation, search for their orthologs in transcriptomes or genomes of brachiopods, phoronids and bryozoans, and present expression patterns of 8 of the genes in postmetamorphic juveniles of the rhynchonelliform brachiopod T. transversa.ResultsTranscriptome and genome searches for the 10 target genes in the brachiopods Terebratalia transversa, Lingula anatina, Novocrania anomala, the bryozoans Bugula neritina and Membranipora membranacea, and the phoronids Phoronis australis and Phoronopsis harmeri resulted in the recovery of orthologs of the majority of the genes in all taxa. While the full complement of genes was present in all brachiopods with a single exception in L. anatina, a bloc of four genes could consistently not be retrieved from bryozoans and phoronids. The genes engrailed, distal-less, ferritin, perlucin, sp1 and sp2 were shown to be expressed in the biomineralising mantle margin of T. transversa juveniles.ConclusionsThe gene expression patterns we recovered indicate that while mineralised shells in brachiopods and molluscs are structurally analogous, their formation builds on a homologous process that involves a conserved complement of orthologous genes. Losses of some of the genes related to biomineralisation in bryozoans and phoronids indicate that loss of the capacity to form mineralised structures occurred already in the phoronid-bryozoan stem group and supports the idea that mineralised skeletons evolved secondarily in some of the bryozoan subclades.

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Nemertean, brachiopod and phoronid neuropeptidomics reveals ancestral spiralian signalling systems.

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