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

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.

Comparative transcriptional profile of the fish parasite Cryptocaryon irritans

“…This left 9,253 contigs (Coding sequence ≥ 100 amino acids) (Table 1), of which 8,569 contigs matched entries in the NR protein database, and all 9,253 contigs (Additional file 1: Tables S2 and S3) matched to the six ciliate databases, corresponding to the number of I. multifiliis annotations [33, 34]. A Venn diagram summarizing C. irritans unigenes compared with peptide sequences from Tetrahymena (four species in total), I. multifiliis , and P. tetraurelia is shown in Fig.…”

Diversity of extracellular proteins during the transition from the ‘proto-apicomplexan’ alveolates to the apicomplexan obligate parasites

“…The molecular and mechanical details underpinning the invasion strategy of bivalve haemocytes by Perkinsus are not known (Soudant et al 2013) and warrant further study, particularly utilizing the recently released high coverage genome sequence information for this alveolate pathogen. The development of cell invasion or parasitism does not necessarily lie along the evolutionary pathway to the Apicomplexa, as these features have evolved multiple times in the alveolates, including Perkinsus (Soudant et al 2013), and the endoparasite of fish epithelial tissue, the ciliate Ichthyophthirius multifiliis (Coyne et al 2011). Within the perkinsids different host targets exist, including the exquisite example of Parvilucifera prorocentri, which invades and develops within dinoflagellates (Hoppenrath and Leander, 2009).…”

“…1) to the phylum Apicomplexa, using the repertoires of predicted extracellular proteins. As a basis for this review, we have performed extensive and sensitive basic local alignment search tool (BLAST) screens of extracellular proteins in order to compare apicomplexans with other alveolates and to take advantage of new genome sequence information from the ciliates, Ichthyophthirius (Coyne et al 2011), Oxytricha (Swart et al 2013) and Stylonychia (Aeschlimann et al 2014); the chromerids, Chromera velia and Vitrella brassicaformis (Woo et al 2015); Perkinsus marinus; high coverage transcriptome sequence information for several colpodellids and GenBank-deposited genome sequence information for the apicomplexans Gregarina niphandrodes, Cryptosporidium muris, Eimeria tenella and Hammondia. Genome sequence information is also available for Tetrahymena thermophila (Eisen et al 2006), P. tetraurelia (Aury et al 2006), Babesia bovis (Brayton et al 2007) and other Babesia species (Cornillot et al 2012;Jackson et al 2014), Eimeria spp.…”

Zebrafish: an animal model for research in veterinary medicine

“…Moreover, the genome of I. multifiliis has been sequenced, which is a helpful tool for studies on this species. It could allow to reconstruct the development and metabolism of itch and compare it with the host's metabolic pathways, that would reveal potential targets for combating white spot disease (Coyne et al 2011).…”