Global Transcriptome Analysis of the Tentacle of the Jellyfish Cyanea capillata Using Deep Sequencing and Expressed Sequence Tags: Insight into the Toxin- and Degenerative Disease-Related Transcripts

PLOS ONE, Dec 2019

Background Jellyfish contain diverse toxins and other bioactive components. However, large-scale identification of novel toxins and bioactive components from jellyfish has been hampered by the low efficiency of traditional isolation and purification methods. Results We performed de novo transcriptome sequencing of the tentacle tissue of the jellyfish Cyanea capillata. A total of 51,304,108 reads were obtained and assembled into 50,536 unigenes. Of these, 21,357 unigenes had homologues in public databases, but the remaining unigenes had no significant matches due to the limited sequence information available and species-specific novel sequences. Functional annotation of the unigenes also revealed general gene expression profile characteristics in the tentacle of C. capillata. A primary goal of this study was to identify putative toxin transcripts. As expected, we screened many transcripts encoding proteins similar to several well-known toxin families including phospholipases, metalloproteases, serine proteases and serine protease inhibitors. In addition, some transcripts also resembled molecules with potential toxic activities, including cnidarian CfTX-like toxins with hemolytic activity, plancitoxin-1, venom toxin-like peptide-6, histamine-releasing factor, neprilysin, dipeptidyl peptidase 4, vascular endothelial growth factor A, angiotensin-converting enzyme-like and endothelin-converting enzyme 1-like proteins. Most of these molecules have not been previously reported in jellyfish. Interestingly, we also characterized a number of transcripts with similarities to proteins relevant to several degenerative diseases, including Huntington’s, Alzheimer’s and Parkinson’s diseases. This is the first description of degenerative disease-associated genes in jellyfish. Conclusion We obtained a well-categorized and annotated transcriptome of C. capillata tentacle that will be an important and valuable resource for further understanding of jellyfish at the molecular level and information on the underlying molecular mechanisms of jellyfish stinging. The findings of this study may also be used in comparative studies of gene expression profiling among different jellyfish species.

A PDF file should load here. If you do not see its contents the file may be temporarily unavailable at the journal website or you do not have a PDF plug-in installed and enabled in your browser.

Alternatively, you can download the file locally and open with any standalone PDF reader:

https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0142680&type=printable

Global Transcriptome Analysis of the Tentacle of the Jellyfish Cyanea capillata Using Deep Sequencing and Expressed Sequence Tags: Insight into the Toxin- and Degenerative Disease-Related Transcripts

November Global Transcriptome Analysis of the Tentacle of the Jellyfish Cyanea capillata Using Deep Sequencing and Expressed Sequence Tags: Insight into the Toxin- and Degenerative Disease-Related Transcripts Guoyan Liu 0 1 Yonghong Zhou 0 1 Dan Liu 0 1 Qianqian Wang 0 1 Zengliang Ruan 0 1 Qian He 0 1 Liming Zhang 0 1 0 1 Marine Bio-pharmaceutical Institute, Second Military Medical University , Shanghai 200433, China , 2 Department of Marine Biotechnology, Faculty of Naval Medicine, Second Military Medical University , Shanghai 200433, China , 3 Department of Gynecology, Third Affiliated Hospital, Second Military Medical University , Shanghai 200433 , China 1 Editor: Israel Silman, Weizmann Institute of Science , ISRAEL - Funding: This work was supported by the Young Scientists Fund of National Natural Science Foundation of China (41306136), the Natural Science Foundation of Shanghai Municipal Government (12ZR1437000) and the National High Technology Research and Development Program of China (863 Program) (2013AA092904). The funders had no role Jellyfish contain diverse toxins and other bioactive components. However, large-scale identification of novel toxins and bioactive components from jellyfish has been hampered by the low efficiency of traditional isolation and purification methods. We performed de novo transcriptome sequencing of the tentacle tissue of the jellyfish Cyanea capillata. A total of 51,304,108 reads were obtained and assembled into 50,536 unigenes. Of these, 21,357 unigenes had homologues in public databases, but the remaining unigenes had no significant matches due to the limited sequence information available and species-specific novel sequences. Functional annotation of the unigenes also revealed general gene expression profile characteristics in the tentacle of C. capillata. A primary goal of this study was to identify putative toxin transcripts. As expected, we screened many transcripts encoding proteins similar to several well-known toxin families including phospholipases, metalloproteases, serine proteases and serine protease inhibitors. In addition, some transcripts also resembled molecules with potential toxic activities, including cnidarian CfTX-like toxins with hemolytic activity, plancitoxin-1, venom toxin-like peptide-6, histamine-releasing factor, neprilysin, dipeptidyl peptidase 4, vascular endothelial growth factor A, angiotensin-converting enzyme-like and endothelin-converting enzyme 1-like proteins. Most of these molecules have not been previously reported in jellyfish. Interestingly, we also characterized a number of transcripts with similarities to proteins relevant to several in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. degenerative diseases, including Huntington’s, Alzheimer’s and Parkinson’s diseases. This is the first description of degenerative disease-associated genes in jellyfish. We obtained a well-categorized and annotated transcriptome of C. capillata tentacle that will be an important and valuable resource for further understanding of jellyfish at the molecular level and information on the underlying molecular mechanisms of jellyfish stinging. The findings of this study may also be used in comparative studies of gene expression profiling among different jellyfish species. In recent decades, frequent outbreaks of jellyfish have occurred in oceans, potentially due to overfishing by humans, nutrient pollution and global warming. Jellyfish outbreaks have a strong adverse impact on marine ecological balance. However, the large amount of jellyfish biomass could be considered a valuable source of bioactive compounds. Thus, the overall development and comprehensive utilization of jellyfish have also triggered interest among many scientists. Jellyfish bodies contain a great variety of natural bioactive components, among which the most studied are jellyfish nematocyst toxins. Nematocysts are densely located on the tentacles, and each contains a tiny dose of venom. People stung by toxic jellyfish may develop severe pain, dyspnea or even cardiorespiratory failure [1]. Many studies have explored the physicochemical properties of nematocyst toxins, which are now believed to be a type of novel protein or peptide. Jellyfish nematocyst toxins exhibit various bioactivities, such as hemolytic, enzymatic, neurotoxic, myotoxic and cardiovascular activities [2–4]. In addition to nematocyst toxins, the jellyfish body contains a wide range of novel proteins or peptides that exhibit activities such as antioxidation, antibiosis and immune reinforcing. Antioxidant activity of the giant jellyfish Nemopilema nomurai was observed by Kazuki [5]. We previously reported the first peroxiredoxin (Prx) and thioredoxin (Trx) genes from the jellyfish Cyanea capillata; both of these genes exhibit general intracellular antioxidant activity [6–7]. The je (...truncated)


This is a preview of a remote PDF: https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0142680&type=printable

Guoyan Liu, Yonghong Zhou, Dan Liu, Qianqian Wang, Zengliang Ruan, Qian He, Liming Zhang. Global Transcriptome Analysis of the Tentacle of the Jellyfish Cyanea capillata Using Deep Sequencing and Expressed Sequence Tags: Insight into the Toxin- and Degenerative Disease-Related Transcripts, PLOS ONE, 2015, Volume 10, Issue 11, DOI: 10.1371/journal.pone.0142680