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Comparative transcriptional profile of the fish parasite Cryptocaryon irritans

BACKGROUND: Cryptocaryon irritans is an obligate ectoparasitic ciliate pathogen of marine fishes. It can infect most marine teleosts and cause heavy economic losses in aquaculture. There is currently no effective method of controlling this disease, and little information is available regarding the g...

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Autores principales: Mo, Ze-Quan, Li, Yan-Wei, Wang, Hai-Qing, Wang, Jiu-Le, Ni, Lu-Yun, Yang, Man, Lao, Guo-Feng, Luo, Xiao-Chun, Li, An-Xing, Dan, Xue-Ming
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5142281/
https://www.ncbi.nlm.nih.gov/pubmed/27923398
http://dx.doi.org/10.1186/s13071-016-1919-1
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author Mo, Ze-Quan
Li, Yan-Wei
Wang, Hai-Qing
Wang, Jiu-Le
Ni, Lu-Yun
Yang, Man
Lao, Guo-Feng
Luo, Xiao-Chun
Li, An-Xing
Dan, Xue-Ming
author_facet Mo, Ze-Quan
Li, Yan-Wei
Wang, Hai-Qing
Wang, Jiu-Le
Ni, Lu-Yun
Yang, Man
Lao, Guo-Feng
Luo, Xiao-Chun
Li, An-Xing
Dan, Xue-Ming
author_sort Mo, Ze-Quan
collection PubMed
description BACKGROUND: Cryptocaryon irritans is an obligate ectoparasitic ciliate pathogen of marine fishes. It can infect most marine teleosts and cause heavy economic losses in aquaculture. There is currently no effective method of controlling this disease, and little information is available regarding the genes involved in its development and virulence. We aimed to investigate the distinct features of the three major life-cycle stages of C. irritans in terms of gene transcription level, and identify candidate vaccines/drug targets. We established a reference transcriptome of C. irritans by RNA-seq. METHODS: Three cDNA libraries using total poly(A)(+) mRNA isolated from trophonts, tomonts, and theronts was constructed and sequenced, respectively. Clean reads from the three stages were de novo assembled to generated unigene. Annotation of unigenes and transcriptomic comparison of three stages was performed. RESULTS: Totals of 73.15, 62.23, and 109.57 million clean reads were generated from trophont, tomont, and theront libraries, respectively. After de novo assembly, 49,104 unigenes were obtained, including 9,253 unigenes with significant similarities to proteins from other ciliates. Transcriptomic comparisons revealed that 2,470 genes were differentially expressed among the three stages, including 2,011, 1,404, and 1,797 genes that were significantly differentially expressed in tomont/theront, tomont/trophont, and theront/trophont pairwise comparisons, respectively. Based on the results of hierarchical clustering, all differentially expressed genes (DEGs) were located in five major clusters. DEGs in clusters 1 and 2 were more highly expressed in tomonts than in other stages, DEGs in cluster 3 were dominant in the tomont and trophont stages, whereas clusters 4 and 5 included genes upregulated in the theront stage. In addition, Immobilization antigens (I-antigens) and proteases have long been considered major targets for vaccine development and potential drug targets in parasites, respectively. In the present study, nine putative I-antigens transcripts and 161 protease transcripts were found in the transcriptome of C. irritans. CONCLUSION: It was concluded that DEGs enriched in tomonts were involved in cell division, to increase the number of theronts and ensure parasite continuity. DEGs enriched in theronts were associated with response to stimuli, whereas genes enriched in trophonts were related to nutrient accumulation and cell growth. In addition, the I-antigen and protease transcripts in our transcriptome could contribute to the development of vaccines or targeted drugs. Together, the results of the present study provide novel insights into the physiological processes of a marine parasitic ciliate. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13071-016-1919-1) contains supplementary material, which is available to authorized users.
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spelling pubmed-51422812016-12-15 Comparative transcriptional profile of the fish parasite Cryptocaryon irritans Mo, Ze-Quan Li, Yan-Wei Wang, Hai-Qing Wang, Jiu-Le Ni, Lu-Yun Yang, Man Lao, Guo-Feng Luo, Xiao-Chun Li, An-Xing Dan, Xue-Ming Parasit Vectors Research BACKGROUND: Cryptocaryon irritans is an obligate ectoparasitic ciliate pathogen of marine fishes. It can infect most marine teleosts and cause heavy economic losses in aquaculture. There is currently no effective method of controlling this disease, and little information is available regarding the genes involved in its development and virulence. We aimed to investigate the distinct features of the three major life-cycle stages of C. irritans in terms of gene transcription level, and identify candidate vaccines/drug targets. We established a reference transcriptome of C. irritans by RNA-seq. METHODS: Three cDNA libraries using total poly(A)(+) mRNA isolated from trophonts, tomonts, and theronts was constructed and sequenced, respectively. Clean reads from the three stages were de novo assembled to generated unigene. Annotation of unigenes and transcriptomic comparison of three stages was performed. RESULTS: Totals of 73.15, 62.23, and 109.57 million clean reads were generated from trophont, tomont, and theront libraries, respectively. After de novo assembly, 49,104 unigenes were obtained, including 9,253 unigenes with significant similarities to proteins from other ciliates. Transcriptomic comparisons revealed that 2,470 genes were differentially expressed among the three stages, including 2,011, 1,404, and 1,797 genes that were significantly differentially expressed in tomont/theront, tomont/trophont, and theront/trophont pairwise comparisons, respectively. Based on the results of hierarchical clustering, all differentially expressed genes (DEGs) were located in five major clusters. DEGs in clusters 1 and 2 were more highly expressed in tomonts than in other stages, DEGs in cluster 3 were dominant in the tomont and trophont stages, whereas clusters 4 and 5 included genes upregulated in the theront stage. In addition, Immobilization antigens (I-antigens) and proteases have long been considered major targets for vaccine development and potential drug targets in parasites, respectively. In the present study, nine putative I-antigens transcripts and 161 protease transcripts were found in the transcriptome of C. irritans. CONCLUSION: It was concluded that DEGs enriched in tomonts were involved in cell division, to increase the number of theronts and ensure parasite continuity. DEGs enriched in theronts were associated with response to stimuli, whereas genes enriched in trophonts were related to nutrient accumulation and cell growth. In addition, the I-antigen and protease transcripts in our transcriptome could contribute to the development of vaccines or targeted drugs. Together, the results of the present study provide novel insights into the physiological processes of a marine parasitic ciliate. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13071-016-1919-1) contains supplementary material, which is available to authorized users. BioMed Central 2016-12-07 /pmc/articles/PMC5142281/ /pubmed/27923398 http://dx.doi.org/10.1186/s13071-016-1919-1 Text en © The Author(s). 2016 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
Mo, Ze-Quan
Li, Yan-Wei
Wang, Hai-Qing
Wang, Jiu-Le
Ni, Lu-Yun
Yang, Man
Lao, Guo-Feng
Luo, Xiao-Chun
Li, An-Xing
Dan, Xue-Ming
Comparative transcriptional profile of the fish parasite Cryptocaryon irritans
title Comparative transcriptional profile of the fish parasite Cryptocaryon irritans
title_full Comparative transcriptional profile of the fish parasite Cryptocaryon irritans
title_fullStr Comparative transcriptional profile of the fish parasite Cryptocaryon irritans
title_full_unstemmed Comparative transcriptional profile of the fish parasite Cryptocaryon irritans
title_short Comparative transcriptional profile of the fish parasite Cryptocaryon irritans
title_sort comparative transcriptional profile of the fish parasite cryptocaryon irritans
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5142281/
https://www.ncbi.nlm.nih.gov/pubmed/27923398
http://dx.doi.org/10.1186/s13071-016-1919-1
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