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Comparative genomics of the pathogenic ciliate Ichthyophthirius multifiliis, its free-living relatives and a host species provide insights into adoption of a parasitic lifestyle and prospects for disease control

Robert S Coyne, Linda Hannick, Dhanasekaran Shanmugam, Jessica B Hostetler, Daniel Brami, Vinita S Joardar, Justin Johnson, Diana Radune, Irtisha Singh, Jonathan H Badger, et al. (2011) GENOME BIOLOGY. 12(10).
abstract
BACKGROUND: Ichthyophthirius multifiliis, commonly known as Ich, is a highly pathogenic ciliate responsible for 'white spot', a disease causing significant economic losses to the global aquaculture industry. Options for disease control are extremely limited, and Ich's obligate parasitic lifestyle makes experimental studies challenging. Unlike most well-studied protozoan parasites, Ich belongs to a phylum composed primarily of free-living members. Indeed, it is closely related to the model organism Tetrahymena thermophila. Genomic studies represent a promising strategy to reduce the impact of this disease and to understand the evolutionary transition to parasitism. RESULTS: We report the sequencing, assembly and annotation of the Ich macronuclear genome. Compared with its free-living relative T. thermophila, the Ich genome is reduced approximately two-fold in length and gene density and three-fold in gene content. We analyzed in detail several gene classes with diverse functions in behavior, cellular function and host immunogenicity, including protein kinases, membrane transporters, proteases, surface antigens and cytoskeletal components and regulators. We also mapped by orthology Ich's metabolic pathways in comparison with other ciliates and a potential host organism, the zebrafish Danio rerio. CONCLUSIONS: Knowledge of the complete protein-coding and metabolic potential of Ich opens avenues for rational testing of therapeutic drugs that target functions essential to this parasite but not to its fish hosts. Also, a catalog of surface protein-encoding genes will facilitate development of more effective vaccines. The potential to use T. thermophila as a surrogate model offers promise toward controlling 'white spot' disease and understanding the adaptation to a parasitic lifestyle.
Please use this url to cite or link to this publication:
author
organization
year
type
journalArticle (original)
publication status
published
subject
keyword
APICOMPLEXAN PARASITES, PLASMODIUM-FALCIPARUM, MALARIA PARASITE, TRYPANOSOMA-BRUCEI, MITOCHONDRIAL GENOME, TETRAHYMENA-THERMOPHILA, TRANSFER-RNA GENES, DYNEIN HEAVY-CHAIN, TRANSPORTER CLASSIFICATION DATABASE, MULTIPLE SEQUENCE ALIGNMENT
journal title
GENOME BIOLOGY
Genome Biol.
volume
12
issue
10
article number
R100
pages
26 pages
Web of Science type
Article
Web of Science id
000301176900003
JCR category
BIOTECHNOLOGY & APPLIED MICROBIOLOGY
JCR impact factor
9.036 (2011)
JCR rank
6/157 (2011)
JCR quartile
1 (2011)
ISSN
1474-7596
DOI
10.1186/gb-2011-12-10-r100
project
Bioinformatics: from nucleotids to networks (N2N)
language
English
UGent publication?
yes
classification
A1
copyright statement
I have retained and own the full copyright for this publication
id
2078132
handle
http://hdl.handle.net/1854/LU-2078132
date created
2012-03-30 13:58:52
date last changed
2017-07-25 14:03:00
@article{2078132,
  abstract     = {BACKGROUND: Ichthyophthirius multifiliis, commonly known as Ich, is a highly pathogenic ciliate responsible for 'white spot', a disease causing significant economic losses to the global aquaculture industry. Options for disease control are extremely limited, and Ich's obligate parasitic lifestyle makes experimental studies challenging. Unlike most well-studied protozoan parasites, Ich belongs to a phylum composed primarily of free-living members. Indeed, it is closely related to the model organism Tetrahymena thermophila. Genomic studies represent a promising strategy to reduce the impact of this disease and to understand the evolutionary transition to parasitism.
RESULTS: We report the sequencing, assembly and annotation of the Ich macronuclear genome. Compared with its free-living relative T. thermophila, the Ich genome is reduced approximately two-fold in length and gene density and three-fold in gene content. We analyzed in detail several gene classes with diverse functions in behavior, cellular function and host immunogenicity, including protein kinases, membrane transporters, proteases, surface antigens and cytoskeletal components and regulators. We also mapped by orthology Ich's metabolic pathways in comparison with other ciliates and a potential host organism, the zebrafish Danio rerio.
CONCLUSIONS: Knowledge of the complete protein-coding and metabolic potential of Ich opens avenues for rational testing of therapeutic drugs that target functions essential to this parasite but not to its fish hosts. Also, a catalog of surface protein-encoding genes will facilitate development of more effective vaccines. The potential to use T. thermophila as a surrogate model offers promise toward controlling 'white spot' disease and understanding the adaptation to a parasitic lifestyle.},
  articleno    = {R100},
  author       = {Coyne, Robert S and Hannick, Linda and Shanmugam, Dhanasekaran and Hostetler, Jessica B and Brami, Daniel and Joardar, Vinita S and Johnson, Justin and Radune, Diana and Singh, Irtisha and Badger, Jonathan H and Kumar, Ujjwal and Saier, Milton and Wang, YuFeng and Cai, Hong and Gu, JianYing and Mather, Michael W and Vaidya, Akhil B and Wilkes, David E and Rajagopalan, Vidyalakshmi and Asai, David J and Pearson, Chad G and Findly, Robert C and Dickerson, Harry W and Wu, Martin and Martens, Cindy and Van de Peer, Yves and Roos, David S and Cassidy-Hanley, Donna M and Clark, Theodore G},
  issn         = {1474-7596},
  journal      = {GENOME BIOLOGY},
  keyword      = {APICOMPLEXAN PARASITES,PLASMODIUM-FALCIPARUM,MALARIA PARASITE,TRYPANOSOMA-BRUCEI,MITOCHONDRIAL GENOME,TETRAHYMENA-THERMOPHILA,TRANSFER-RNA GENES,DYNEIN HEAVY-CHAIN,TRANSPORTER CLASSIFICATION DATABASE,MULTIPLE SEQUENCE ALIGNMENT},
  language     = {eng},
  number       = {10},
  pages        = {26},
  title        = {Comparative genomics of the pathogenic ciliate Ichthyophthirius multifiliis, its free-living relatives and a host species provide insights into adoption of a parasitic lifestyle and prospects for disease control},
  url          = {http://dx.doi.org/10.1186/gb-2011-12-10-r100},
  volume       = {12},
  year         = {2011},
}

Chicago
Coyne, Robert S, Linda Hannick, Dhanasekaran Shanmugam, Jessica B Hostetler, Daniel Brami, Vinita S Joardar, Justin Johnson, et al. 2011. “Comparative Genomics of the Pathogenic Ciliate Ichthyophthirius Multifiliis, Its Free-living Relatives and a Host Species Provide Insights into Adoption of a Parasitic Lifestyle and Prospects for Disease Control.” Genome Biology 12 (10).
APA
Coyne, R. S., Hannick, L., Shanmugam, D., Hostetler, J. B., Brami, D., Joardar, V. S., Johnson, J., et al. (2011). Comparative genomics of the pathogenic ciliate Ichthyophthirius multifiliis, its free-living relatives and a host species provide insights into adoption of a parasitic lifestyle and prospects for disease control. GENOME BIOLOGY, 12(10).
Vancouver
1.
Coyne RS, Hannick L, Shanmugam D, Hostetler JB, Brami D, Joardar VS, et al. Comparative genomics of the pathogenic ciliate Ichthyophthirius multifiliis, its free-living relatives and a host species provide insights into adoption of a parasitic lifestyle and prospects for disease control. GENOME BIOLOGY. 2011;12(10).
MLA
Coyne, Robert S, Linda Hannick, Dhanasekaran Shanmugam, et al. “Comparative Genomics of the Pathogenic Ciliate Ichthyophthirius Multifiliis, Its Free-living Relatives and a Host Species Provide Insights into Adoption of a Parasitic Lifestyle and Prospects for Disease Control.” GENOME BIOLOGY 12.10 (2011): n. pag. Print.