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A comparative genomics study of neuropeptide genes in the cnidarian subclasses Hexacorallia and Ceriantharia

BACKGROUND: Nervous systems originated before the split of Proto- and Deuterostomia, more than 600 million years ago. Four animal phyla (Cnidaria, Placozoa, Ctenophora, Porifera) diverged before this split and studying these phyla could give us important information on the evolution of the nervous s...

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Autores principales: Koch, Thomas L., Grimmelikhuijzen, Cornelis J. P.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7523074/
https://www.ncbi.nlm.nih.gov/pubmed/32993486
http://dx.doi.org/10.1186/s12864-020-06945-9
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author Koch, Thomas L.
Grimmelikhuijzen, Cornelis J. P.
author_facet Koch, Thomas L.
Grimmelikhuijzen, Cornelis J. P.
author_sort Koch, Thomas L.
collection PubMed
description BACKGROUND: Nervous systems originated before the split of Proto- and Deuterostomia, more than 600 million years ago. Four animal phyla (Cnidaria, Placozoa, Ctenophora, Porifera) diverged before this split and studying these phyla could give us important information on the evolution of the nervous system. Here, we have annotated the neuropeptide preprohormone genes of twenty species belonging to the subclass Hexacorallia or Ceriantharia (Anthozoa: Cnidaria), using thirty-seven publicly accessible genome or transcriptome databases. Studying hexacorals is important, because they are versatile laboratory models for development (e.g., Nematostella vectensis) and symbiosis (e.g., Exaiptasia diaphana) and also are prominent reef-builders. RESULTS: We found that each hexacoral or ceriantharian species contains five to ten neuropeptide preprohormone genes. Many of these preprohormones contain multiple copies of immature neuropeptides, which can be up to 50 copies of identical or similar neuropeptide sequences. We also discovered preprohormones that only contained one neuropeptide sequence positioned directly after the signal sequence. Examples of them are neuropeptides that terminate with the sequence RWamide (the Antho-RWamides). Most neuropeptide sequences are N-terminally protected by pyroglutamyl (pQ) or one or more prolyl residues, while they are C-terminally protected by an amide group. Previously, we isolated and sequenced small neuropeptides from hexacorals that were N-terminally protected by an unusual L-3-phenyllactyl group. In our current analysis, we found that these N-phenyllactyl-peptides are derived from N-phenylalanyl-peptides located directly after the signal sequence of the preprohormone. The N-phenyllactyl- peptides appear to be confined to the hexacorallian order Actiniaria and do not occur in other cnidarians. On the other hand, (1) the neuropeptide Antho-RFamide (pQGRFamide); (2) peptides with the C-terminal sequence GLWamide; and (3) tetrapeptides with the X(1)PRX(2)amide consensus sequence (most frequently GPRGamide) are ubiquitous in Hexacorallia. CONCLUSIONS: We found GRFamide, GLWamide, and X(1)PRX(2)amide peptides in all tested Hexacorallia. Previously, we discovered these three neuropeptide classes also in Cubozoa, Scyphozoa, and Staurozoa, indicating that these neuropeptides originated in the common cnidarian ancestor and are evolutionarily ancient. In addition to these ubiquitous neuropeptides, other neuropeptides appear to be confined to specific cnidarian orders or subclasses.
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spelling pubmed-75230742020-09-30 A comparative genomics study of neuropeptide genes in the cnidarian subclasses Hexacorallia and Ceriantharia Koch, Thomas L. Grimmelikhuijzen, Cornelis J. P. BMC Genomics Research Article BACKGROUND: Nervous systems originated before the split of Proto- and Deuterostomia, more than 600 million years ago. Four animal phyla (Cnidaria, Placozoa, Ctenophora, Porifera) diverged before this split and studying these phyla could give us important information on the evolution of the nervous system. Here, we have annotated the neuropeptide preprohormone genes of twenty species belonging to the subclass Hexacorallia or Ceriantharia (Anthozoa: Cnidaria), using thirty-seven publicly accessible genome or transcriptome databases. Studying hexacorals is important, because they are versatile laboratory models for development (e.g., Nematostella vectensis) and symbiosis (e.g., Exaiptasia diaphana) and also are prominent reef-builders. RESULTS: We found that each hexacoral or ceriantharian species contains five to ten neuropeptide preprohormone genes. Many of these preprohormones contain multiple copies of immature neuropeptides, which can be up to 50 copies of identical or similar neuropeptide sequences. We also discovered preprohormones that only contained one neuropeptide sequence positioned directly after the signal sequence. Examples of them are neuropeptides that terminate with the sequence RWamide (the Antho-RWamides). Most neuropeptide sequences are N-terminally protected by pyroglutamyl (pQ) or one or more prolyl residues, while they are C-terminally protected by an amide group. Previously, we isolated and sequenced small neuropeptides from hexacorals that were N-terminally protected by an unusual L-3-phenyllactyl group. In our current analysis, we found that these N-phenyllactyl-peptides are derived from N-phenylalanyl-peptides located directly after the signal sequence of the preprohormone. The N-phenyllactyl- peptides appear to be confined to the hexacorallian order Actiniaria and do not occur in other cnidarians. On the other hand, (1) the neuropeptide Antho-RFamide (pQGRFamide); (2) peptides with the C-terminal sequence GLWamide; and (3) tetrapeptides with the X(1)PRX(2)amide consensus sequence (most frequently GPRGamide) are ubiquitous in Hexacorallia. CONCLUSIONS: We found GRFamide, GLWamide, and X(1)PRX(2)amide peptides in all tested Hexacorallia. Previously, we discovered these three neuropeptide classes also in Cubozoa, Scyphozoa, and Staurozoa, indicating that these neuropeptides originated in the common cnidarian ancestor and are evolutionarily ancient. In addition to these ubiquitous neuropeptides, other neuropeptides appear to be confined to specific cnidarian orders or subclasses. BioMed Central 2020-09-29 /pmc/articles/PMC7523074/ /pubmed/32993486 http://dx.doi.org/10.1186/s12864-020-06945-9 Text en © The Author(s) 2020 Open AccessThis 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 licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence 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 licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Koch, Thomas L.
Grimmelikhuijzen, Cornelis J. P.
A comparative genomics study of neuropeptide genes in the cnidarian subclasses Hexacorallia and Ceriantharia
title A comparative genomics study of neuropeptide genes in the cnidarian subclasses Hexacorallia and Ceriantharia
title_full A comparative genomics study of neuropeptide genes in the cnidarian subclasses Hexacorallia and Ceriantharia
title_fullStr A comparative genomics study of neuropeptide genes in the cnidarian subclasses Hexacorallia and Ceriantharia
title_full_unstemmed A comparative genomics study of neuropeptide genes in the cnidarian subclasses Hexacorallia and Ceriantharia
title_short A comparative genomics study of neuropeptide genes in the cnidarian subclasses Hexacorallia and Ceriantharia
title_sort comparative genomics study of neuropeptide genes in the cnidarian subclasses hexacorallia and ceriantharia
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7523074/
https://www.ncbi.nlm.nih.gov/pubmed/32993486
http://dx.doi.org/10.1186/s12864-020-06945-9
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