Urbilaterian origin and evolution of sNPF-type neuropeptide signalling

AbstractPhysiology and behaviour are controlled by neuropeptide signalling systems comprising peptide ligands and cognate receptors. Molecular phylogenetics combined with experimental identification of neuropeptide-receptor pairs has revealed that many neuropeptide signalling systems originated in the urbilaterian common ancestor of protostomes and deuterostomes. Neuropeptide-Y/neuropeptide-F (NPY/NPF)-type signalling is one such example, whereas NPY/NPF-related short-NPF (sNPF)-type signalling has hitherto only been identified in protostomes. Here we report the discovery of a neuropeptide (pQDRSKAMQAERTGQLRRLNPRF-NH2) that is the ligand for an sNPF-type receptor in a deuterostome, the starfish Asterias rubens (Phylum Echinodermata). Informed by phylogenetic analysis of sequence data, we conclude that the paralogous NPY/NPF-type and sNPF-type signalling systems originated in Urbilateria but NPY/NPF-type signalling was lost in echinoderms. Furthermore, we present evidence that sNPF-type peptides are orthologs of vertebrate prolactin-releasing peptides. Our findings demonstrate the importance of experimental studies on echinoderms for reconstructing the evolutionary history of neuropeptide signalling systems.

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Echinoderms provide missing link in the evolution of PrRP/sNPF-type neuropeptide signalling

eLife ◽

10.7554/elife.57640 ◽

2020 ◽

Vol 9 ◽

Cited By ~ 2

Author(s):

Luis Alfonso Yañez-Guerra ◽

Xingxing Zhong ◽

Ismail Moghul ◽

Thomas Butts ◽

Cleidiane G Zampronio ◽

...

Keyword(s):

Neuropeptide Y ◽

Sequence Data ◽

Experimental Studies ◽

Peptide Ligands ◽

Asterias Rubens ◽

Neuropeptide F ◽

Prolactin Releasing Peptide ◽

Type Receptor ◽

Signalling Systems

Neuropeptide signalling systems comprising peptide ligands and cognate receptors are evolutionarily ancient regulators of physiology and behaviour. However, there are challenges associated with determination of orthology between neuropeptides in different taxa. Orthologs of vertebrate neuropeptide-Y (NPY) known as neuropeptide-F (NPF) have been identified in protostome invertebrates, whilst prolactin-releasing peptide (PrRP) and short neuropeptide-F (sNPF) have been identified as paralogs of NPY/NPF in vertebrates and protostomes, respectively. Here we investigated the occurrence of NPY/NPF/PrRP/sNPF-related signalling systems in a deuterostome invertebrate phylum – the Echinodermata. Analysis of transcriptome/genome sequence data revealed loss of NPY/NPF-type signalling, but orthologs of PrRP-type neuropeptides and sNPF/PrRP-type receptors were identified in echinoderms. Furthermore, experimental studies revealed that the PrRP-type neuropeptide pQDRSKAMQAERTGQLRRLNPRF-NH2 is a potent ligand for a sNPF/PrRP-type receptor in the starfish Asterias rubens. Our findings indicate that PrRP-type and sNPF-type signalling systems are orthologous and originated as a paralog of NPY/NPF-type signalling in Urbilateria.

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Discovery of sea urchin NGFFFamide receptor unites a bilaterian neuropeptide family

Open Biology ◽

10.1098/rsob.150030 ◽

2015 ◽

Vol 5 (4) ◽

pp. 150030 ◽

Cited By ~ 27

Author(s):

Dean C. Semmens ◽

Isabel Beets ◽

Matthew L. Rowe ◽

Liisa M. Blowes ◽

Paola Oliveri ◽

...

Keyword(s):

Sea Urchin ◽

Evolutionary History ◽

Common Ancestor ◽

Strongylocentrotus Purpuratus ◽

Disulfide Bridge ◽

The Other ◽

Genes Encoding ◽

History Of ◽

Neuropeptide Evolution ◽

Signalling Systems

Neuropeptides are ancient regulators of physiology and behaviour, but reconstruction of neuropeptide evolution is often difficult owing to lack of sequence conservation. Here, we report that the receptor for the neuropeptide NGFFFamide in the sea urchin Strongylocentrotus purpuratus (phylum Echinodermata) is an orthologue of vertebrate neuropeptide-S (NPS) receptors and crustacean cardioactive peptide (CCAP) receptors. Importantly, this has facilitated reconstruction of the evolution of two bilaterian neuropeptide signalling systems. Genes encoding the precursor of a vasopressin/oxytocin-type neuropeptide and its receptor duplicated in a common ancestor of the Bilateria. One copy of the precursor retained ancestral features, as seen in highly conserved vasopressin/oxytocin–neurophysin-type precursors. The other copy diverged, but this took different courses in protostomes and deuterostomes. In protostomes, the occurrence of a disulfide bridge in neuropeptide product(s) of the precursor was retained, as in CCAP, but with loss of the neurophysin domain. In deuterostomes, we see the opposite scenario—the neuropeptides lost the disulfide bridge, and neurophysin was retained (as in the NGFFFamide precursor) but was subsequently lost in vertebrate NPS precursors. Thus, the sea urchin NGFFFamide precursor and receptor are ‘missing links’ in the evolutionary history of neuropeptides that control ecdysis in arthropods (CCAP) and regulate anxiety in humans (NPS).

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The evolutionary history of HSA7/16 synteny in vertebrates: a critical interpretation of comparative cytogenetic and genome sequence data

Caryologia ◽

10.1080/00087114.2013.829691 ◽

2013 ◽

Vol 66 (3) ◽

pp. 236-242

Author(s):

Barbara Picone ◽

Luca Sineo

Keyword(s):

Genome Sequence ◽

Evolutionary History ◽

Sequence Data ◽

Genome Sequence Data ◽

History Of ◽

Critical Interpretation

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Evolutionary history of dimethylsulfoniopropionate (DMSP) demethylation enzyme DmdA in marine bacteria

10.1101/766360 ◽

2019 ◽

Author(s):

Laura Hernández ◽

Alberto Vicens ◽

Luis Enrique Eguiarte ◽

Valeria Souza ◽

Valerie De Anda ◽

...

Keyword(s):

Gene Family ◽

Evolutionary History ◽

Common Ancestor ◽

Functional Divergence ◽

Gene Families ◽

Recent Common Ancestor ◽

Common Ancestry ◽

Demethylation Pathway ◽

History Of ◽

New Gene

ABSTRACTDimethylsulfoniopropionate (DMSP), an osmolyte produced by oceanic phytoplankton, is predominantly degraded by bacteria belonging to the Roseobacter lineage and other marine Alphaproteobacteria via DMSP-dependent demethylase A protein (DmdA). To date, the evolutionary history of DmdA gene family is unclear. Some studies indicate a common ancestry between DmdA and GcvT gene families and a co-evolution between Roseobacter and the DMSP-producing-phytoplankton around 250 million years ago (Mya). In this work, we analyzed the evolution of DmdA under three possible evolutionary scenarios: 1) a recent common ancestor of DmdA and GcvT, 2) a coevolution between Roseobacter and the DMSP-producing-phytoplankton, and 3) pre-adapted enzymes to DMSP prior to Roseobacter origin. Our analyses indicate that DmdA is a new gene family originated from GcvT genes by duplication and functional divergence driven by positive selection before a coevolution between Roseobacter and phytoplankton. Our data suggest that Roseobacter acquired dmdA by horizontal gene transfer prior to exposition to an environment with higher DMSP. Here, we propose that the ancestor that carried the DMSP demethylation pathway genes evolved in the Archean, and was exposed to a higher concentration of DMSP in a sulfur rich atmosphere and anoxic ocean, compared to recent Roseobacter ecoparalogs (copies performing the same function under different conditions), which should be adapted to lower concentrations of DMSP.

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