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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 Coyne1*, Linda Hannick2, Dhanasekaran Shanmugam3, Jessica B Hostetler4, Daniel Brami5, Vinita S Joardar2, Justin Johnson2, Diana Radune4, Irtisha Singh6, Jonathan H Badger7, Ujjwal Kumar8, Milton Saier8, Yufeng Wang9, Hong Cai9, Jianying Gu10, Michael W Mather10, Akhil B Vaidya10, David E Wilkes11, Vidyalakshmi Rajagopalan11, David J Asai12, Chad G Pearson13, Robert C Findly14, Harry W Dickerson14, Martin Wu15, Cindy Martens16, Yves Van de Peer16, David S Roos17, Donna M Cassidy-Hanley18 and Theodore G Clark18

Author Affiliations

1 Genomic Medicine, J Craig Venter Institute, 9704 Medical Center Dr., Rockville, MD 20850, USA

2 Informatics, J Craig Venter Institute, 9704 Medical Center Dr., Rockville, MD 20850, USA

3 Biology, University of Pennsylvania, 3451 Walnut St, Philadelphia, PA 19104, USA

4 Joint Technology Center, J Craig Venter Institute, 9704 Medical Center Dr., Rockville, MD 20850, USA

5 Informatics, J Craig Venter Institute, 10355 Science Center Drive, San Diego, CA 92121, USA

6 Microbial and Environmental Genomics, J Craig Venter Institute, 9704 Medical Center Dr., Rockville, MD 20850, USA

7 Microbial and Environmental Genomics, J Craig Venter Institute, 10355 Science Center Drive, San Diego, CA 92121, USA

8 Biological Sciences, University of California - San Diego, 9500 Gilman Dr., La Jolla, CA 92093, USA

9 Biology, University of Texas at San Antonio, 1 UTSA Circle, San Antonio, TX 78249, USA

10 Microbiology and Immunology, Drexel University College of Medicine, 2900 Queen Lane, Philadelphia, PA 19129, USA

11 Biological Sciences, Indiana University - South Bend, 1700 Mishawaka Avenue, South Bend, IN 46634, USA

12 Undergraduate Science Education Program, Howard Hughes Medical Institute, 4000 Jones Bridge Road, Chevy Chase, MD 20815, USA

13 Cell and Developmental Biology, University of Colorado - Denver, 13001 E. 17th Place, Aurora, CO 80045, USA

14 Infectious Diseases, College of Veterinary Medicine, University of Georgia, 501 DW Brooks Dr, Athens, GA 30602, USA

15 Department of Biology, University of Virginia, 485 McCormick Road, Charlottesville, VA 22903, USA

16 Plant Systems Biology, Ghent University, Technologiepark 927, Ghent, B-9052, Belgium

17 Biology and Penn Genome Frontiers Institute, University of Pennsylvania, 3451 Walnut St., Philadelphia, PA 19104, USA

18 Microbiology and Immunology, College of Veterinary Medicine, Cornell University, C5 181 Veterinary Medical Center, Ithaca, NY 14853, USA

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Genome Biology 2011, 12:R100  doi:10.1186/gb-2011-12-10-r100

Published: 17 October 2011

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.