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. 2013 Apr 4;496(7443):57-63.
doi: 10.1038/nature12031. Epub 2013 Mar 13.

The genomes of four tapeworm species reveal adaptations to parasitism

Isheng J Tsai # 1 , Magdalena Zarowiecki # 1 , Nancy Holroyd # 1 , Alejandro Garciarrubio # 2 , Alejandro Sánchez-Flores 3 , Karen L Brooks 1 , Alan Tracey 1 , Raúl J Bobes 4 , Gladis Fragoso 4 , Edda Sciutto 4 , Martin Aslett 1 , Helen Beasley 1 , Hayley M Bennett 1 , Xuepeng Cai 5 , Federico Camicia 6 , Richard Clark 1 , Marcela Cucher 6 , Nishadi De Silva 1 , Tim A Day 7 , Peter Deplazes 8 , Karel Estrada 2 , Cecilia Fernández 9 , Peter W H Holland 10 , Junling Hou 5 , Songnian Hu 11 , Thomas Huckvale 1 , Stacy S Hung 12 , Laura Kamenetzky 6 , Jacqueline A Keane 1 , Ferenc Kiss 13 , Uriel Koziol 13 , Olivia Lambert 1 , Kan Liu 11 , Xuenong Luo 5 , Yingfeng Luo 11 , Natalia Macchiaroli 6 , Sarah Nichol 1 , Jordi Paps 10 , John Parkinson 12 , Natasha Pouchkina-Stantcheva 14 , Nick Riddiford 15 , Mara Rosenzvit 6 , Gustavo Salinas 9 , James D Wasmuth 16 , Mostafa Zamanian 17 , Yadong Zheng 5 ; Taenia solium Genome Consortium ; Jianping Cai 5 , Xavier Soberón 18 , Peter D Olson 14 , Juan P Laclette 4 , Klaus Brehm 13 , Matthew Berriman 1
Collaborators, Affiliations

The genomes of four tapeworm species reveal adaptations to parasitism

Isheng J Tsai et al. Nature. .

Abstract

Tapeworms (Cestoda) cause neglected diseases that can be fatal and are difficult to treat, owing to inefficient drugs. Here we present an analysis of tapeworm genome sequences using the human-infective species Echinococcus multilocularis, E. granulosus, Taenia solium and the laboratory model Hymenolepis microstoma as examples. The 115- to 141-megabase genomes offer insights into the evolution of parasitism. Synteny is maintained with distantly related blood flukes but we find extreme losses of genes and pathways that are ubiquitous in other animals, including 34 homeobox families and several determinants of stem cell fate. Tapeworms have specialized detoxification pathways, metabolism that is finely tuned to rely on nutrients scavenged from their hosts, and species-specific expansions of non-canonical heat shock proteins and families of known antigens. We identify new potential drug targets, including some on which existing pharmaceuticals may act. The genomes provide a rich resource to underpin the development of urgently needed treatments and control.

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Figures

Figure 1
Figure 1. Genome of E. multilocularis
A) The nine assembled chromosomes of E. multilocularis. Telomeres (red circle) and physical gaps in the sequence assembly (dashed lines), but which an optical map covers, are shown. (B) One-to-one orthologues connecting E. multilocularis and S. mansoni chromosomes. (C) Distribution of normalised genome coverage on strain GT10/2. Each horizontal line depicts median coverage of 100 kb windows normalised against the mean coverage for the genome (×ばつ). Even coverage was observed across the first eight chromosomes in E. multilocularis but ×ばつ coverage of chromosome 9 indicates trisomy. Similar plots for other isolates are shown in Supplementary Figure S3.1. D) Distribution of minor allele frequency (MAF) of heterozygous sites in five isolates of E. multilocularis (plot for individual isolates in Supplementary Figure S3.1), identified by mapping sequencing reads against the assembled chromosome consensus sequences. At each site, the proportion of bases that disagree with the reference is counted. For four isolates, the MAF peaks at around 0.5, indicative of diploidy, whereas JAVA05/1 peaks at 0.25 suggesting tetraploidy. *Chr 9 of GT10/2 is plotted separately from Chr1-8 and the MAF display a clear departure of 0.5 and peaks around 0.33, consistent with a trisomy.
Figure 2
Figure 2. Road to parasitism
Phylogeny of the main branches of Bilateria; Ecdysozoa - including fruit flies and nematodes, Deuterostomia - including lancelet, zebrafish, mice and humans, and Lophotrochozoans, including Platyhelminthes (flatworms), based on phylogeny in Supplementary Figure S7.1. Gains and losses of life cycle traits; A. endoparasitism evolves, B. passively transmitted between hosts, C. acquires vertebrate intermediate host, D. ability for asexual proliferation in intermediate host. Morphological traits that have evolved include E. cup-eyes were lost, F neodermatan syncytial epithelia gained, G. gut was lost, H. segmentation of body plan, I. laminated layer evolved, containing specialised apomucins. Gains and losses of genomic traits: 1. SL-trans-splicing, 2. loss of Wnt genes, 3. loss of NEK kinases, fatty acid biosynthesis and ParaHox genes, 4. anaerobic metabolic ability through the malate dismutation/rodhoquinone pathway, merger of Glutaredoxin (Grx) and thioredoxin reductase (TR) to thioredoxin glutathione reductase (TGR) 5. evolution of tapeworm and fluke specific Argonaute family, micro exon genes (MEGs) and PROF1 GPCRs, 6. loss of peroxisomal genes 7. complete loss of vasa, tudor and piwi genes, NkB pathway, loss of 24 homeobox gene families, metabolic proteases and amino acid biosynthesis, 8. in tapeworms: innovation of bimodal intron distribution and novel fatty acid transporters 9. expansion of mu glutathione-S-transferases, GP50 antigens and tetraspanins, 10. loss of molybdopterin biosynthesis pathway, loss of 10 homeobox gene families 11. fewer GPCRs and fewer neuropeptides encoded by each protopeptide, 12. expansion of heat shock proteins and species-specific antigens.
Figure 3
Figure 3. Conservation of individual metabolic pathways
Heatmap showing the conservation of individual metabolic pathways for E. multilocularis (Em), E. granulosus (Eg), T. solium (Ts), H. microstoma (Hm) and S. mansoni (Sm) compared to those of humans (Hs) and mice (Mm). Each row indicates an individual metabolic pathway grouped by their superclass membership (defined by KEGG). Coloured tiles indicate the level of conservation (percentage of enzymes detected) of each pathway within each species. KEGG pathways with insufficient evidence (i.e. containing only one enzyme) in E. multilocularis have been removed.
Figure 4
Figure 4. Heat shock protein 70 expansions in the tapeworms
Rooted tree of HSP70 sequences from the eight comparative species used in this study and tapeworms with additional sequences from baker’s yeast Saccharomyces cerevisiae, and the Pacific oyster Crassostrea gigas (a non-flatworm example of a lophotrochozoan) with a recently reported HSP70 expansion. Colour highlights different HSP70 subfamilies. Red stars indicates the E. multilocularis cytosolic HSP70 that are located in the sub-telomeres. EEVD denotes the conserved C-terminal residues of a canonical cytosolic HSP70.

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