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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.

Liu G, Zhou Y, Liu D, Wang Q, Ruan Z, He Q, Zhang L - PLoS ONE (2015)

Bottom Line: 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.This is the first description of degenerative disease-associated genes in jellyfish.The findings of this study may also be used in comparative studies of gene expression profiling among different jellyfish species.

View Article: PubMed Central - PubMed

Affiliation: Marine Bio-pharmaceutical Institute, Second Military Medical University, Shanghai 200433, China.

ABSTRACT

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.

No MeSH data available.


Related in: MedlinePlus

(A) Multiple sequence alignment of the amino acid sequence of unigene 6213 with other known CfTX-like cnidarian toxins. The abbreviations and sequence accession numbers for the aligned sequences are as follows: Aurelia aurita TX2 (AFK76349), Chiropsalmus quadrigatus CqTX-A (BAB82520), Carybdea rastonii CrTX-A (BAB12728), Carybdea alata CaTX-A (BAB12727), and Chironex fleckeri CfTX-A, CfTX-B, CfTX-1 and CfTX-2 (AFQ00676, AFQ00677, ABS30940 and ABS30941, respectively). The putative highly conserved transmembrane spanning region (TSR1) in the N-terminal sequences of this toxin family is boxed. (B) Phylogenetic relationships of the CfTX-like cnidarian toxins.
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pone.0142680.g005: (A) Multiple sequence alignment of the amino acid sequence of unigene 6213 with other known CfTX-like cnidarian toxins. The abbreviations and sequence accession numbers for the aligned sequences are as follows: Aurelia aurita TX2 (AFK76349), Chiropsalmus quadrigatus CqTX-A (BAB82520), Carybdea rastonii CrTX-A (BAB12728), Carybdea alata CaTX-A (BAB12727), and Chironex fleckeri CfTX-A, CfTX-B, CfTX-1 and CfTX-2 (AFQ00676, AFQ00677, ABS30940 and ABS30941, respectively). The putative highly conserved transmembrane spanning region (TSR1) in the N-terminal sequences of this toxin family is boxed. (B) Phylogenetic relationships of the CfTX-like cnidarian toxins.

Mentions: In this study, we identified a transcript (Unigene6213) with significant similarity to the N-terminal sequences of a family of known jellyfish toxins, including TX2 isolated from Aurelia aurita, CfTX-1,2 and CfTX-A,B from Chironex fleckeri, CqTX-A from C. quadrigatus, CrTX-A from C. rastoni and CaTX-A from C. alata [53–54]. The multiple sequence alignment and phylogenetic analysis of these similar jellyfish toxins are presented in Fig 5. This toxin family is primarily associated with potent hemolytic activity and pore-forming action [53,55]. As shown in Fig 5, a putative transmembrane spanning region (TSR1) that is highly conserved in the N-terminal sequences of this toxin family is also present in the predicted amino acid range (6–50) of Unigene6213. The presence of the transmembrane spanning region in these jellyfish toxins is very important because it may play a role in the pore-forming process [50]. Therefore, Unigene6213 is likely a new member of this family of jellyfish toxins, even though it does not contain a full-length ORF. Further research is needed to determine the full-length sequence, structure and biological role of this putative toxin in C. capillata.


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.

Liu G, Zhou Y, Liu D, Wang Q, Ruan Z, He Q, Zhang L - PLoS ONE (2015)

(A) Multiple sequence alignment of the amino acid sequence of unigene 6213 with other known CfTX-like cnidarian toxins. The abbreviations and sequence accession numbers for the aligned sequences are as follows: Aurelia aurita TX2 (AFK76349), Chiropsalmus quadrigatus CqTX-A (BAB82520), Carybdea rastonii CrTX-A (BAB12728), Carybdea alata CaTX-A (BAB12727), and Chironex fleckeri CfTX-A, CfTX-B, CfTX-1 and CfTX-2 (AFQ00676, AFQ00677, ABS30940 and ABS30941, respectively). The putative highly conserved transmembrane spanning region (TSR1) in the N-terminal sequences of this toxin family is boxed. (B) Phylogenetic relationships of the CfTX-like cnidarian toxins.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4638339&req=5

pone.0142680.g005: (A) Multiple sequence alignment of the amino acid sequence of unigene 6213 with other known CfTX-like cnidarian toxins. The abbreviations and sequence accession numbers for the aligned sequences are as follows: Aurelia aurita TX2 (AFK76349), Chiropsalmus quadrigatus CqTX-A (BAB82520), Carybdea rastonii CrTX-A (BAB12728), Carybdea alata CaTX-A (BAB12727), and Chironex fleckeri CfTX-A, CfTX-B, CfTX-1 and CfTX-2 (AFQ00676, AFQ00677, ABS30940 and ABS30941, respectively). The putative highly conserved transmembrane spanning region (TSR1) in the N-terminal sequences of this toxin family is boxed. (B) Phylogenetic relationships of the CfTX-like cnidarian toxins.
Mentions: In this study, we identified a transcript (Unigene6213) with significant similarity to the N-terminal sequences of a family of known jellyfish toxins, including TX2 isolated from Aurelia aurita, CfTX-1,2 and CfTX-A,B from Chironex fleckeri, CqTX-A from C. quadrigatus, CrTX-A from C. rastoni and CaTX-A from C. alata [53–54]. The multiple sequence alignment and phylogenetic analysis of these similar jellyfish toxins are presented in Fig 5. This toxin family is primarily associated with potent hemolytic activity and pore-forming action [53,55]. As shown in Fig 5, a putative transmembrane spanning region (TSR1) that is highly conserved in the N-terminal sequences of this toxin family is also present in the predicted amino acid range (6–50) of Unigene6213. The presence of the transmembrane spanning region in these jellyfish toxins is very important because it may play a role in the pore-forming process [50]. Therefore, Unigene6213 is likely a new member of this family of jellyfish toxins, even though it does not contain a full-length ORF. Further research is needed to determine the full-length sequence, structure and biological role of this putative toxin in C. capillata.

Bottom Line: 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.This is the first description of degenerative disease-associated genes in jellyfish.The findings of this study may also be used in comparative studies of gene expression profiling among different jellyfish species.

View Article: PubMed Central - PubMed

Affiliation: Marine Bio-pharmaceutical Institute, Second Military Medical University, Shanghai 200433, China.

ABSTRACT

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.

No MeSH data available.


Related in: MedlinePlus