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

Sofie K D Nielsen,Anders Garm,Cornelis J P Grimmelikhuijzen,Thomas L Koch,Frank Hauser

doi:10.1186/s12864-019-5514-7

Sofie K D Nielsen, Anders Garm + Show 3 more

Open Access

https://doi.org/10.1186/s12864-019-5514-7

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Journal: BMC Genomics	Publication Date: Mar 6, 2019
Citations: 18	License type: open-access

Affiliation: University of Copenhagen

Abstract

BackgroundThe 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.ResultsBased 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.ConclusionsBy 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.

Highlights

The phyla Cnidaria, Placozoa, Ctenophora, and Porifera emerged before the split of proto- and deuterostome animals, about 600 million years ago
One of the peptides located on the second preprohormone fragment from C. quadrumanus (Fig. 4) is preceded by an acidic residue and has the likely structure pQPRSamide (Table 1). (vi) We identified a complete RYamide preprohormone in the transcriptome from T. cystophora that contained four copies of an RYamide neuropeptide
We identified 22 G protein-coupled receptor (GPCR), which the TBLASTN search software described as neuropeptide GPCR-like and 28 GPCRs which the search software described as biogenic amine GPCR-like (Table 4)

Summary

Introduction

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. Cnidarians are basal, multicellular animals such as Hydra, corals, and jellyfishes They are interesting from an evolutionary point of view, because they belong to a small group of phyla (together with Placozoa, Ctenophora, and Porifera) that evolved before the split of deuterostomes (e.g. vertebrates) and protostomes (most invertebrates, such as insects), an event that occurred about 600 million years ago [1]. The Arg (R) and Lys (K) residues are recognized by classical prohormone convertases (PC-1/3 or PC-2), which liberate the neuropeptide sequences, while the Gly (G) residues are converted into C-terminal amide groups by the enzyme peptidylglycine α-amidating monooxygenase [29, 34,35,36]

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Conclusion