Abstract

BackgroundIchthyophthirius 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.ResultsWe 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.ConclusionsKnowledge 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.

Highlights

  • 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

  • In the Tetrahymena genome project, MACs were physically separated from MICs, resulting in an assembly largely free of MIC-specific sequence contamination, but similar nuclear separation techniques have not been developed for Ich

  • We relied on natural enrichment of the MAC genome; during the host-associated trophont stage of parasite development (Figure 1), endoduplication of the MAC genome occurs, leading to an estimated ploidy of up to 12,000 C, in the absence of MIC genome duplication [16]

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Summary

Introduction

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. The ciliates are an ancient and diverse phylogenetic group related to the largely parasitic apicomplexans, but consisting mostly of free-living heterotrophs. By far the most important of these is Ichthyophthirius multifiliis (which we will refer to by its common name of Ich), an endoparasite that causes white spot disease in freshwater fish [1,2]. With an extremely broad host-range, Ich is responsible for large-scale die-offs in natural populations and poses a significant threat to the growing worldwide aquaculture industry. Fish that survive infection are resistant to future challenge, prophylactic and therapeutic options remain extremely limited

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