Cargando…

De novo transcriptome assembly of the cubomedusa Tripedalia cystophora, including the analysis of a set of genes involved in peptidergic neurotransmission

BACKGROUND: The phyla Cnidaria, Placozoa, Ctenophora, and Porifera emerged before the split of proto- and deuterostome animals, about 600 million years ago. These early metazoans are interesting, because they can give us important information on the evolution of various tissues and organs, such as e...

Descripción completa

Detalles Bibliográficos
Autores principales: Nielsen, Sofie K. D., Koch, Thomas L., Hauser, Frank, Garm, Anders, Grimmelikhuijzen, Cornelis J. P.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6402141/
https://www.ncbi.nlm.nih.gov/pubmed/30836949
http://dx.doi.org/10.1186/s12864-019-5514-7
_version_ 1783400330345578496
author Nielsen, Sofie K. D.
Koch, Thomas L.
Hauser, Frank
Garm, Anders
Grimmelikhuijzen, Cornelis J. P.
author_facet Nielsen, Sofie K. D.
Koch, Thomas L.
Hauser, Frank
Garm, Anders
Grimmelikhuijzen, Cornelis J. P.
author_sort Nielsen, Sofie K. D.
collection PubMed
description BACKGROUND: The phyla Cnidaria, Placozoa, Ctenophora, and Porifera emerged before the split of proto- and deuterostome animals, about 600 million years ago. These early metazoans are interesting, because they can give us important information on the evolution of various tissues and organs, such as eyes and the nervous system. Generally, cnidarians have simple nervous systems, which use neuropeptides for their neurotransmission, but some cnidarian medusae belonging to the class Cubozoa (box jellyfishes) have advanced image-forming eyes, probably associated with a complex innervation. Here, we describe a new transcriptome database from the cubomedusa Tripedalia cystophora. RESULTS: Based on the combined use of the Illumina and PacBio sequencing technologies, we produced a highly contiguous transcriptome database from T. cystophora. We then developed a software program to discover neuropeptide preprohormones in this database. This script enabled us to annotate seven novel T. cystophora neuropeptide preprohormone cDNAs: One coding for 19 copies of a peptide with the structure pQWLRGRFamide; one coding for six copies of a different RFamide peptide; one coding for six copies of pQPPGVWamide; one coding for eight different neuropeptide copies with the C-terminal LWamide sequence; one coding for thirteen copies of a peptide with the RPRAamide C-terminus; one coding for four copies of a peptide with the C-terminal GRYamide sequence; and one coding for seven copies of a cyclic peptide, of which the most frequent one has the sequence CTGQMCWFRamide. We could also identify orthologs of these seven preprohormones in the cubozoans Alatina alata, Carybdea xaymacana, Chironex fleckeri, and Chiropsalmus quadrumanus. Furthermore, using TBLASTN screening, we could annotate four bursicon-like glycoprotein hormone subunits, five opsins, and 52 other family-A G protein-coupled receptors (GPCRs), which also included two leucine-rich repeats containing G protein-coupled receptors (LGRs) in T. cystophora. The two LGRs are potential receptors for the glycoprotein hormones, while the other GPCRs are candidate receptors for the above-mentioned neuropeptides. CONCLUSIONS: By combining Illumina and PacBio sequencing technologies, we have produced a new high-quality de novo transcriptome assembly from T. cystophora that should be a valuable resource for identifying the neuronal components that are involved in vision and other behaviors in cubomedusae. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-019-5514-7) contains supplementary material, which is available to authorized users.
format Online
Article
Text
id pubmed-6402141
institution National Center for Biotechnology Information
language English
publishDate 2019
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-64021412019-03-14 De novo transcriptome assembly of the cubomedusa Tripedalia cystophora, including the analysis of a set of genes involved in peptidergic neurotransmission Nielsen, Sofie K. D. Koch, Thomas L. Hauser, Frank Garm, Anders Grimmelikhuijzen, Cornelis J. P. BMC Genomics Research Article BACKGROUND: The phyla Cnidaria, Placozoa, Ctenophora, and Porifera emerged before the split of proto- and deuterostome animals, about 600 million years ago. These early metazoans are interesting, because they can give us important information on the evolution of various tissues and organs, such as eyes and the nervous system. Generally, cnidarians have simple nervous systems, which use neuropeptides for their neurotransmission, but some cnidarian medusae belonging to the class Cubozoa (box jellyfishes) have advanced image-forming eyes, probably associated with a complex innervation. Here, we describe a new transcriptome database from the cubomedusa Tripedalia cystophora. RESULTS: Based on the combined use of the Illumina and PacBio sequencing technologies, we produced a highly contiguous transcriptome database from T. cystophora. We then developed a software program to discover neuropeptide preprohormones in this database. This script enabled us to annotate seven novel T. cystophora neuropeptide preprohormone cDNAs: One coding for 19 copies of a peptide with the structure pQWLRGRFamide; one coding for six copies of a different RFamide peptide; one coding for six copies of pQPPGVWamide; one coding for eight different neuropeptide copies with the C-terminal LWamide sequence; one coding for thirteen copies of a peptide with the RPRAamide C-terminus; one coding for four copies of a peptide with the C-terminal GRYamide sequence; and one coding for seven copies of a cyclic peptide, of which the most frequent one has the sequence CTGQMCWFRamide. We could also identify orthologs of these seven preprohormones in the cubozoans Alatina alata, Carybdea xaymacana, Chironex fleckeri, and Chiropsalmus quadrumanus. Furthermore, using TBLASTN screening, we could annotate four bursicon-like glycoprotein hormone subunits, five opsins, and 52 other family-A G protein-coupled receptors (GPCRs), which also included two leucine-rich repeats containing G protein-coupled receptors (LGRs) in T. cystophora. The two LGRs are potential receptors for the glycoprotein hormones, while the other GPCRs are candidate receptors for the above-mentioned neuropeptides. CONCLUSIONS: By combining Illumina and PacBio sequencing technologies, we have produced a new high-quality de novo transcriptome assembly from T. cystophora that should be a valuable resource for identifying the neuronal components that are involved in vision and other behaviors in cubomedusae. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-019-5514-7) contains supplementary material, which is available to authorized users. BioMed Central 2019-03-06 /pmc/articles/PMC6402141/ /pubmed/30836949 http://dx.doi.org/10.1186/s12864-019-5514-7 Text en © The Author(s). 2019 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided 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 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.
spellingShingle Research Article
Nielsen, Sofie K. D.
Koch, Thomas L.
Hauser, Frank
Garm, Anders
Grimmelikhuijzen, Cornelis J. P.
De novo transcriptome assembly of the cubomedusa Tripedalia cystophora, including the analysis of a set of genes involved in peptidergic neurotransmission
title De novo transcriptome assembly of the cubomedusa Tripedalia cystophora, including the analysis of a set of genes involved in peptidergic neurotransmission
title_full De novo transcriptome assembly of the cubomedusa Tripedalia cystophora, including the analysis of a set of genes involved in peptidergic neurotransmission
title_fullStr De novo transcriptome assembly of the cubomedusa Tripedalia cystophora, including the analysis of a set of genes involved in peptidergic neurotransmission
title_full_unstemmed De novo transcriptome assembly of the cubomedusa Tripedalia cystophora, including the analysis of a set of genes involved in peptidergic neurotransmission
title_short De novo transcriptome assembly of the cubomedusa Tripedalia cystophora, including the analysis of a set of genes involved in peptidergic neurotransmission
title_sort de novo transcriptome assembly of the cubomedusa tripedalia cystophora, including the analysis of a set of genes involved in peptidergic neurotransmission
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6402141/
https://www.ncbi.nlm.nih.gov/pubmed/30836949
http://dx.doi.org/10.1186/s12864-019-5514-7
work_keys_str_mv AT nielsensofiekd denovotranscriptomeassemblyofthecubomedusatripedaliacystophoraincludingtheanalysisofasetofgenesinvolvedinpeptidergicneurotransmission
AT kochthomasl denovotranscriptomeassemblyofthecubomedusatripedaliacystophoraincludingtheanalysisofasetofgenesinvolvedinpeptidergicneurotransmission
AT hauserfrank denovotranscriptomeassemblyofthecubomedusatripedaliacystophoraincludingtheanalysisofasetofgenesinvolvedinpeptidergicneurotransmission
AT garmanders denovotranscriptomeassemblyofthecubomedusatripedaliacystophoraincludingtheanalysisofasetofgenesinvolvedinpeptidergicneurotransmission
AT grimmelikhuijzencornelisjp denovotranscriptomeassemblyofthecubomedusatripedaliacystophoraincludingtheanalysisofasetofgenesinvolvedinpeptidergicneurotransmission