Discovery and functional characterisation of a luqin-type neuropeptide signalling system in a deuterostome

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Abstract

Neuropeptides are diverse and evolutionarily ancient regulators of physiological/behavioural processes in animals. Here we have investigated the evolution and comparative physiology of luqin-type neuropeptide signalling, which has been characterised previously in protostomian invertebrates. Phylogenetic analysis indicates that luqin-type receptors and tachykinin-type receptors are paralogous and probably originated in a common ancestor of the Bilateria. In the deuterostomian lineage, luqin-type signalling has been lost in chordates but interestingly it has been retained in ambulacrarians. Therefore, here we characterised luqin-type signalling for the first time in an ambulacrarian – the starfish Asterias rubens (phylum Echinodermata). A luqin-like neuropeptide with a C-terminal RWamide motif (ArLQ; EEKTRFPKFMRW-NH ₂) was identified as the ligand for two luqin-type receptors in A. rubens, ArLQR1 and ArLQR2. Furthermore, analysis of the expression of the ArLQ precursor using mRNA in situ hybridisation revealed expression in the nervous system, digestive system and locomotory organs (tube feet) and in vitro pharmacology revealed that ArLQ causes dose-dependent relaxation of tube feet. Accordingly, previous studies have revealed that luqin-type signalling regulates feeding and locomotor activity in protostomes. In conclusion, our phylogenetic analysis combined with characterisation of luqin-type signalling in a deuterostome has provided new insights into neuropeptide evolution and function in the animal kingdom.

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How many bootstrap replicates are necessary?

Nicholas D Pattengale, Masoud Alipour, Olaf Bininda-Emonds … (2010)

Phylogenetic bootstrapping (BS) is a standard technique for inferring confidence values on phylogenetic trees that is based on reconstructing many trees from minor variations of the input data, trees called replicates. BS is used with all phylogenetic reconstruction approaches, but we focus here on one of the most popular, maximum likelihood (ML). Because ML inference is so computationally demanding, it has proved too expensive to date to assess the impact of the number of replicates used in BS on the relative accuracy of the support values. For the same reason, a rather small number (typically 100) of BS replicates are computed in real-world studies. Stamatakis et al. recently introduced a BS algorithm that is 1 to 2 orders of magnitude faster than previous techniques, while yielding qualitatively comparable support values, making an experimental study possible. In this article, we propose stopping criteria--that is, thresholds computed at runtime to determine when enough replicates have been generated--and we report on the first large-scale experimental study to assess the effect of the number of replicates on the quality of support values, including the performance of our proposed criteria. We run our tests on 17 diverse real-world DNA--single-gene as well as multi-gene--datasets, which include 125-2,554 taxa. We find that our stopping criteria typically stop computations after 100-500 replicates (although the most conservative criterion may continue for several thousand replicates) while producing support values that correlate at better than 99.5% with the reference values on the best ML trees. Significantly, we also find that the stopping criteria can recommend very different numbers of replicates for different datasets of comparable sizes. Our results are thus twofold: (i) they give the first experimental assessment of the effect of the number of BS replicates on the quality of support values returned through BS, and (ii) they validate our proposals for stopping criteria. Practitioners will no longer have to enter a guess nor worry about the quality of support values; moreover, with most counts of replicates in the 100-500 range, robust BS under ML inference becomes computationally practical for most datasets. The complete test suite is available at http://lcbb.epfl.ch/BS.tar.bz2, and BS with our stopping criteria is included in the latest release of RAxML v7.2.5, available at http://wwwkramer.in.tum.de/exelixis/software.html.

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Global view of the evolution and diversity of metazoan neuropeptide signaling.

Gáspár Jékely (2013)

Neuropeptides are signaling molecules that commonly act via G protein-coupled receptors (GPCRs) and are generated in neurons by proneuropeptide (pNP) cleavage. Present in both cnidarians and bilaterians, neuropeptides represent an ancient and widespread mode of neuronal communication. Due to the inherent difficulties of analyzing highly diverse and repetitive pNPs, the relationships among different families are often elusive. Using similarity-based clustering and sensitive similarity searches, I obtained a global view of metazoan pNP diversity and evolution. Clustering revealed a large and diffuse network of sequences connected by significant sequence similarity encompassing one-quarter of all families. pNPs belonging to this cluster were also identified in the early-branching neuronless animal Trichoplax adhaerens. Clustering of neuropeptide GPCRs identified several orthology groups and allowed the reconstruction of the phyletic distribution of receptor families. GPCR phyletic distribution closely paralleled that of pNPs, indicating extensive conservation and long-term coevolution of receptor-ligand pairs. Receptor orthology and intermediate sequences also revealed the homology of pNPs so far considered unrelated, including allatotropin and orexin. These findings, together with the identification of deuterostome achatin and luqin and protostome opioid pNPs, extended the neuropeptide complement of the urbilaterian. Several pNPs were also identified from the hemichordate Saccoglossus kowalevskii and the cephalochordate Branchiostoma floridae, elucidating pNP evolution in deuterostomes. Receptor-ligand conservation also allowed ligand predictions for many uncharacterized GPCRs from nonmodel species. The reconstruction of the neuropeptide-signaling repertoire at deep nodes of the animal phylogeny allowed the formulation of a testable scenario of the evolution of animal neuroendocrine systems.

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Molecular evolution of peptidergic signaling systems in bilaterians.

Jean-Stéphane Joly, Olivier Mirabeau (2013)

Peptide hormones and their receptors are widespread in metazoans, but the knowledge we have of their evolutionary relationships remains unclear. Recently, accumulating genome sequences from many different species have offered the opportunity to reassess the relationships between protostomian and deuterostomian peptidergic systems (PSs). Here we used sequences of all human rhodopsin and secretin-type G protein-coupled receptors as bait to retrieve potential homologs in the genomes of 15 bilaterian species, including nonchordate deuterostomian and lophotrochozoan species. Our phylogenetic analysis of these receptors revealed 29 well-supported subtrees containing mixed sets of protostomian and deuterostomian sequences. This indicated that many vertebrate and arthropod PSs that were previously thought to be phyla specific are in fact of bilaterian origin. By screening sequence databases for potential peptides, we then reconstructed entire bilaterian peptide families and showed that protostomian and deuterostomian peptides that are ligands of orthologous receptors displayed some similarity at the level of their primary sequence, suggesting an ancient coevolution between peptide and receptor genes. In addition to shedding light on the function of human G protein-coupled receptor PSs, this work presents orthology markers to study ancestral neuron types that were probably present in the last common bilaterian ancestor.

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Author and article information

Contributors

Maurice R. Elphick:

ORCID: http://orcid.org/0000-0002-9169-0048

m.r.elphick@qmul.ac.uk

Journal

Journal ID (nlm-ta): Sci Rep

Journal ID (iso-abbrev): Sci Rep

Title: Scientific Reports

Publisher: Nature Publishing Group UK (London )

ISSN (Electronic): 2045-2322

Publication date (Electronic): 8 May 2018

Publication date PMC-release: 8 May 2018

Publication date Collection: 2018

Volume: 8

Electronic Location Identifier: 7220

Affiliations

[1 ]ISNI 0000 0001 2171 1133, GRID grid.4868.2, Queen Mary University of London, , School of Biological & Chemical Sciences, ; Mile End Road, London, E1 4NS UK

[2 ]ISNI 0000 0000 8809 1613, GRID grid.7372.1, Waters/Warwick Centre for BioMedical Mass Spectrometry and Proteomics, , School of Life Sciences, University of Warwick, ; Coventry, CV4 7AL UK

[3 ]Present Address: University of Mons, Research Institute for Biosciences, Biology of Marine Organisms and Biomimetics, 23 Place du Parc, Mons, 7000 Belgium

[4 ]ISNI 0000000109410645, GRID grid.11794.3a, Present Address: Department of Functional Biology, , CIBUS, Faculty of Biology, Universidade de Santiago de Compostela, ; 15782 Santiago de Compostela, Spain

[5 ]Present Address: Waters Corporation, Stamford Avenue, Altrincham Road, Wilmslow, SK9 4AX UK

[6 ]ISNI 0000 0001 2325 1783, GRID grid.26597.3f, Present Address: School of Science, , Engineering & Design, Stephenson Street, Teesside University, ; Middlesbrough TS1 3BX, Tees Valley TS1 3BA UK

Author information

Luis Alfonso Yañez-Guerra http://orcid.org/0000-0002-2523-1310

Jérôme Delroisse http://orcid.org/0000-0002-9233-6470

Antón Barreiro-Iglesias http://orcid.org/0000-0002-7507-080X

Maurice R. Elphick http://orcid.org/0000-0002-9169-0048

Article

Publisher ID: 25606

DOI: 10.1038/s41598-018-25606-2

PMC ID: 5940834

PubMed ID: 29740074

SO-VID: 995ee7e4-2130-4ad6-b801-ad6c11110435

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Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

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Date received : 9 January 2018

Date accepted : 24 April 2018

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Discovery and functional characterisation of a luqin-type neuropeptide signalling system in a deuterostome

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Most cited references 39

How many bootstrap replicates are necessary?

Global view of the evolution and diversity of metazoan neuropeptide signaling.

Molecular evolution of peptidergic signaling systems in bilaterians.

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Cited by 15

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