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Comparative Study
.2014 May;6(5):1105-17.
doi: 10.1093/gbe/evu078.

Comparative genomics of flatworms (platyhelminthes) reveals shared genomic features of ecto- and endoparastic neodermata

Affiliations
Comparative Study

Comparative genomics of flatworms (platyhelminthes) reveals shared genomic features of ecto- and endoparastic neodermata

Christoph Hahn et al. Genome Biol Evol.2014 May.

Abstract

The ectoparasitic Monogenea comprise a major part of the obligate parasitic flatworm diversity. Although genomic adaptations to parasitism have been studied in the endoparasitic tapeworms (Cestoda) and flukes (Trematoda), no representative of the Monogenea has been investigated yet. We present the high-quality draft genome of Gyrodactylus salaris, an economically important monogenean ectoparasite of wild Atlantic salmon (Salmo salar). A total of 15,488 gene models were identified, of which 7,102 were functionally annotated. The controversial phylogenetic relationships within the obligate parasitic Neodermata were resolved in a phylogenomic analysis using 1,719 gene models (alignment length of >500,000 amino acids) for a set of 16 metazoan taxa. The Monogenea were found basal to the Cestoda and Trematoda, which implies ectoparasitism being plesiomorphic within the Neodermata and strongly supports a common origin of complex life cycles. Comparative analysis of seven parasitic flatworm genomes identified shared genomic features for the ecto- and endoparasitic lineages, such as a substantial reduction of the core bilaterian gene complement, including the homeodomain-containing genes, and a loss of the piwi and vasa genes, which are considered essential for animal development. Furthermore, the shared loss of functional fatty acid biosynthesis pathways and the absence of peroxisomes, the latter organelles presumed ubiquitous in eukaryotes except for parasitic protozoans, were inferred. The draft genome of G. salaris opens for future in-depth analyses of pathogenicity and host specificity of poorly characterized G. salaris strains, and will enhance studies addressing the genomics of host-parasite interactions and speciation in the highly diverse monogenean flatworms.

Keywords: Gyrodactylus salaris; draft genome; flatworms; genomic adaptations; parasitism; phylogenomics.

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Figures

F<sc>ig</sc>. 1.—
Fig. 1.—
Aggregate properties (coverage and GC content) of contigs obtained by Celera 7.0 as (a) scatter plot and (b) heat map. Colored areas in (a) illustrate the aggressive cleaning strategy adopted in this study, that is, the removal of putative nontarget contigs of coverage <40× (red; putative host contamination) and GC content >50% (blue; putative bacterial contamination) (seesupplementary file S1,Section A for details,Supplementary Material online).
F<sc>ig</sc>. 2.—
Fig. 2.—
Phylogenetic relationships among the major groups of parasitic flatworms. BI topology (CAT-GTR model) based on a supermatrix containing the 312 gene models (135,085 amino acid positions) with the strongest phylogenetic signal (average bootstrap ≥90). Full circles represent nodes with posterior probability = 1 and boostrap support of 100. Numbers next to internodes represent IC, and are based on a subset of 311 genes available for the full taxon set.
F<sc>ig</sc>. 3.—
Fig. 3.—
Venn diagram illustrating the number of gene clusters devoid of orthologous genes of one to three parasitic flatworm groups, while present in all other nonneodermatan Bilateria in the data set.
F<sc>ig</sc>. 4.—
Fig. 4.—
Pattern of inferred homeobox gene family loss during the evolution of obligate parasitism in flatworms. Putative convergent losses are indicated in red (Monogenea and Cestoda) and green (Monogenea and Trematoda).
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