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An evolutionary genomics view on neuropeptide genes in Hydrozoa and Endocnidozoa (Myxozoa)

BACKGROUND: The animal phylum Cnidaria consists of six classes or subphyla: Hydrozoa, Scyphozoa, Cubozoa, Staurozoa, Anthozoa, and Endocnidozoa. Cnidarians have an early evolutionary origin, diverging before the emergence of the Bilateria. Extant members from this phylum, therefore, are important re...

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Autores principales: Koch, Thomas L., Hauser, Frank, Grimmelikhuijzen, Cornelis J. P.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8638164/
https://www.ncbi.nlm.nih.gov/pubmed/34847889
http://dx.doi.org/10.1186/s12864-021-08091-2
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author Koch, Thomas L.
Hauser, Frank
Grimmelikhuijzen, Cornelis J. P.
author_facet Koch, Thomas L.
Hauser, Frank
Grimmelikhuijzen, Cornelis J. P.
author_sort Koch, Thomas L.
collection PubMed
description BACKGROUND: The animal phylum Cnidaria consists of six classes or subphyla: Hydrozoa, Scyphozoa, Cubozoa, Staurozoa, Anthozoa, and Endocnidozoa. Cnidarians have an early evolutionary origin, diverging before the emergence of the Bilateria. Extant members from this phylum, therefore, are important resources for understanding the evolution of the nervous system. Cnidarian nervous systems are strongly peptidergic. Using genomics, we have recently shown that three neuropeptide families (the X(1)PRX(2)amides, GRFamides, and GLWamides) are wide-spread in four (Scyphozoa, Cubozoa, Staurozoa, Anthozoa) out of six cnidarian classes or subphyla, suggesting that these three neuropeptide families emerged in the common cnidarian ancestor. In the current paper, we analyze the remaining cnidarian class, Hydrozoa, and the subphylum Endocnidozoa, to make firm conclusions about the evolution of neuropeptide genes in Cnidaria. RESULTS: We analyzed sixteen hydrozoan species with a sequenced genome or transcriptome, using a recently developed software program for discovering neuropeptide genes. These species belonged to various hydrozoan subclasses and orders, among them the laboratory models Hydra, Hydractinia, and Clytia. We found that each species contained three to five neuropeptide families. A common feature for all hydrozoans was that they contained genes coding for (i) X(1)PRX(2)amide peptides, (ii) GRFamide peptides, and (iii) GLWamide peptides. These results support our previous conclusions that these three neuropeptide families evolved early in evolution. In addition to these three neuropeptide families, hydrozoans expressed up to two other neuropeptide gene families, which, however, were only occurring in certain animal groups. Endocnidozoa (Myxozoa) are microscopically small endoparasites, which are strongly reduced. For long, it was unknown to which phylum these parasites belonged, but recently they have been associated with cnidarians. We analyzed nine endocnidozoan species and found that two of them (Polypodium hydriforme and Buddenbrockia plumatellae) expressed neuropeptide genes. These genes coded for neuropeptides belonging to the GRFamide and GLWamide families with structures closely resembling them from hydrozoans. CONCLUSIONS: We found X(1)PRX(2)amide, GRFamide, and GLWamide peptides in all species belonging to the Hydrozoa, confirming that these peptides originated in the common cnidarian ancestor. In addition, we discovered GRFamide and GLWamide peptide genes in some members of the Endocnidozoa, thereby linking these parasites to Hydrozoa. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-021-08091-2.
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spelling pubmed-86381642021-12-02 An evolutionary genomics view on neuropeptide genes in Hydrozoa and Endocnidozoa (Myxozoa) Koch, Thomas L. Hauser, Frank Grimmelikhuijzen, Cornelis J. P. BMC Genomics Research BACKGROUND: The animal phylum Cnidaria consists of six classes or subphyla: Hydrozoa, Scyphozoa, Cubozoa, Staurozoa, Anthozoa, and Endocnidozoa. Cnidarians have an early evolutionary origin, diverging before the emergence of the Bilateria. Extant members from this phylum, therefore, are important resources for understanding the evolution of the nervous system. Cnidarian nervous systems are strongly peptidergic. Using genomics, we have recently shown that three neuropeptide families (the X(1)PRX(2)amides, GRFamides, and GLWamides) are wide-spread in four (Scyphozoa, Cubozoa, Staurozoa, Anthozoa) out of six cnidarian classes or subphyla, suggesting that these three neuropeptide families emerged in the common cnidarian ancestor. In the current paper, we analyze the remaining cnidarian class, Hydrozoa, and the subphylum Endocnidozoa, to make firm conclusions about the evolution of neuropeptide genes in Cnidaria. RESULTS: We analyzed sixteen hydrozoan species with a sequenced genome or transcriptome, using a recently developed software program for discovering neuropeptide genes. These species belonged to various hydrozoan subclasses and orders, among them the laboratory models Hydra, Hydractinia, and Clytia. We found that each species contained three to five neuropeptide families. A common feature for all hydrozoans was that they contained genes coding for (i) X(1)PRX(2)amide peptides, (ii) GRFamide peptides, and (iii) GLWamide peptides. These results support our previous conclusions that these three neuropeptide families evolved early in evolution. In addition to these three neuropeptide families, hydrozoans expressed up to two other neuropeptide gene families, which, however, were only occurring in certain animal groups. Endocnidozoa (Myxozoa) are microscopically small endoparasites, which are strongly reduced. For long, it was unknown to which phylum these parasites belonged, but recently they have been associated with cnidarians. We analyzed nine endocnidozoan species and found that two of them (Polypodium hydriforme and Buddenbrockia plumatellae) expressed neuropeptide genes. These genes coded for neuropeptides belonging to the GRFamide and GLWamide families with structures closely resembling them from hydrozoans. CONCLUSIONS: We found X(1)PRX(2)amide, GRFamide, and GLWamide peptides in all species belonging to the Hydrozoa, confirming that these peptides originated in the common cnidarian ancestor. In addition, we discovered GRFamide and GLWamide peptide genes in some members of the Endocnidozoa, thereby linking these parasites to Hydrozoa. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-021-08091-2. BioMed Central 2021-11-30 /pmc/articles/PMC8638164/ /pubmed/34847889 http://dx.doi.org/10.1186/s12864-021-08091-2 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/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/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://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
Koch, Thomas L.
Hauser, Frank
Grimmelikhuijzen, Cornelis J. P.
An evolutionary genomics view on neuropeptide genes in Hydrozoa and Endocnidozoa (Myxozoa)
title An evolutionary genomics view on neuropeptide genes in Hydrozoa and Endocnidozoa (Myxozoa)
title_full An evolutionary genomics view on neuropeptide genes in Hydrozoa and Endocnidozoa (Myxozoa)
title_fullStr An evolutionary genomics view on neuropeptide genes in Hydrozoa and Endocnidozoa (Myxozoa)
title_full_unstemmed An evolutionary genomics view on neuropeptide genes in Hydrozoa and Endocnidozoa (Myxozoa)
title_short An evolutionary genomics view on neuropeptide genes in Hydrozoa and Endocnidozoa (Myxozoa)
title_sort evolutionary genomics view on neuropeptide genes in hydrozoa and endocnidozoa (myxozoa)
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8638164/
https://www.ncbi.nlm.nih.gov/pubmed/34847889
http://dx.doi.org/10.1186/s12864-021-08091-2
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