The genomes of four tapeworm species reveal adaptations to parasitism

Isheng J. Tsai, Magdalena Zarowiecki, Nancy Holroyd, Alejandro Garciarrubio, Alejandro Sanchez-Flores, Karen L. Brooks, Alan Tracey, Raúl J. Bobes, Gladis Fragoso, Edda Sciutto, Martin Aslett, Helen Beasley, Hayley M. Bennett, Jianping Cai, Federico Camicia, Richard Clark, Marcela Cucher, Nishadi De Silva, Tim A. Day, Peter Deplazes, Karel Estrada, Cecilia Fernández, Peter W. H. Holland, Junling Hou, Songnian Hu, Thomas Huckvale, Stacy S. Hung, Laura Kamenetzky, Jacqueline A. Keane, Ferenc Kiss, Uriel Koziol, Olivia Lambert, Kan Liu, Xuenong Luo, Yingfeng Luo, Natalia Macchiaroli, Sarah Nichol, Jordi Paps, John Parkinson, Natasha Pouchkina-Stantcheva, Nick Riddiford, Mara Rosenzvit, Gustavo Salinas, James D. Wasmuth, Mostafa Zamanian, Yadong Zheng, Xuepeng Cai, Xavier Soberón, Peter D. Olson, Juan P. Laclette (), Klaus Brehm () and Matthew Berriman ()
Additional contact information
Isheng J. Tsai: Parasite Genomics, Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SA, UK
Magdalena Zarowiecki: Parasite Genomics, Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SA, UK
Nancy Holroyd: Parasite Genomics, Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SA, UK
Alejandro Garciarrubio: Institute of Biotechnology, Universidad Nacional Autónoma de México, Cuernavaca, Morelos 62210, México
Alejandro Sanchez-Flores: Parasite Genomics, Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SA, UK
Karen L. Brooks: Parasite Genomics, Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SA, UK
Alan Tracey: Parasite Genomics, Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SA, UK
Raúl J. Bobes: Institute of Biomedical Research, Universidad Nacional Autónoma de México
Gladis Fragoso: Institute of Biomedical Research, Universidad Nacional Autónoma de México
Edda Sciutto: Institute of Biomedical Research, Universidad Nacional Autónoma de México
Martin Aslett: Parasite Genomics, Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SA, UK
Helen Beasley: Parasite Genomics, Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SA, UK
Hayley M. Bennett: Parasite Genomics, Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SA, UK
Jianping Cai: State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, No. 1 Xujiaping, Chengguan District, Lanzhou 730046, Gansu Province, China
Federico Camicia: Instituto de Microbiología y Parasitología Médica, Universidad de Buenos Aires-Consejo Nacional de Investigaciones Científicas y Tecnológicas (IMPaM, UBA-CONICET). Facultad de Medicina, Paraguay 2155, C1121ABG Buenos Aires, Argentina
Richard Clark: Parasite Genomics, Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SA, UK
Marcela Cucher: Instituto de Microbiología y Parasitología Médica, Universidad de Buenos Aires-Consejo Nacional de Investigaciones Científicas y Tecnológicas (IMPaM, UBA-CONICET). Facultad de Medicina, Paraguay 2155, C1121ABG Buenos Aires, Argentina
Nishadi De Silva: Parasite Genomics, Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SA, UK
Tim A. Day: Iowa State University, Ames, Iowa 50011, USA
Peter Deplazes: Institute of Parasitology, Vetsuisse Faculty, University of Zürich, Winterthurerstrasse 266a, CH-8057 Zürich, Switzerland
Karel Estrada: Institute of Biotechnology, Universidad Nacional Autónoma de México, Cuernavaca, Morelos 62210, México
Cecilia Fernández: Cátedra de Inmunologá, Facultad de Quámica, Universidad de la República. Avenida Alfredo Navarro 3051, piso 2, Montevideo, CP 11600, Uruguay
Peter W. H. Holland: University of Oxford, South Parks Road, Oxford OX1 3PS, UK
Junling Hou: State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, No. 1 Xujiaping, Chengguan District, Lanzhou 730046, Gansu Province, China
Songnian Hu: Beijing Institute of Genomics, Chinese Academy of Sciences, No.7 Beitucheng West Road, Chaoyang District, Beijing 100029, China
Thomas Huckvale: Parasite Genomics, Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SA, UK
Stacy S. Hung: University of Toronto, Program in Molecular Structure and Function, The Hospital for Sick Children, Toronto, Ontario M5G 1X8, Canada
Laura Kamenetzky: Instituto de Microbiología y Parasitología Médica, Universidad de Buenos Aires-Consejo Nacional de Investigaciones Científicas y Tecnológicas (IMPaM, UBA-CONICET). Facultad de Medicina, Paraguay 2155, C1121ABG Buenos Aires, Argentina
Jacqueline A. Keane: Parasite Genomics, Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SA, UK
Ferenc Kiss: University of Würzburg, Institute of Hygiene and Microbiology
Uriel Koziol: University of Würzburg, Institute of Hygiene and Microbiology
Olivia Lambert: Parasite Genomics, Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SA, UK
Kan Liu: Beijing Institute of Genomics, Chinese Academy of Sciences, No.7 Beitucheng West Road, Chaoyang District, Beijing 100029, China
Xuenong Luo: State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, No. 1 Xujiaping, Chengguan District, Lanzhou 730046, Gansu Province, China
Yingfeng Luo: Beijing Institute of Genomics, Chinese Academy of Sciences, No.7 Beitucheng West Road, Chaoyang District, Beijing 100029, China
Natalia Macchiaroli: Instituto de Microbiología y Parasitología Médica, Universidad de Buenos Aires-Consejo Nacional de Investigaciones Científicas y Tecnológicas (IMPaM, UBA-CONICET). Facultad de Medicina, Paraguay 2155, C1121ABG Buenos Aires, Argentina
Sarah Nichol: Parasite Genomics, Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SA, UK
Jordi Paps: University of Oxford, South Parks Road, Oxford OX1 3PS, UK
John Parkinson: University of Toronto, Program in Molecular Structure and Function, The Hospital for Sick Children, Toronto, Ontario M5G 1X8, Canada
Natasha Pouchkina-Stantcheva: The Natural History Museum, Cromwell Road, London SW7 5BD, UK
Nick Riddiford: The Natural History Museum, Cromwell Road, London SW7 5BD, UK
Mara Rosenzvit: Instituto de Microbiología y Parasitología Médica, Universidad de Buenos Aires-Consejo Nacional de Investigaciones Científicas y Tecnológicas (IMPaM, UBA-CONICET). Facultad de Medicina, Paraguay 2155, C1121ABG Buenos Aires, Argentina
Gustavo Salinas: Cátedra de Inmunologá, Facultad de Quámica, Universidad de la República. Avenida Alfredo Navarro 3051, piso 2, Montevideo, CP 11600, Uruguay
James D. Wasmuth: Faculty of Veterinary Medicine, University of Calgary
Mostafa Zamanian: Institute of Parasitology, McGill University, 2111 Lakeshore Road, Ste Anne de Bellevue, Quebec H9X 3V9, Canada
Yadong Zheng: State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, No. 1 Xujiaping, Chengguan District, Lanzhou 730046, Gansu Province, China
Xuepeng Cai: State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, No. 1 Xujiaping, Chengguan District, Lanzhou 730046, Gansu Province, China
Xavier Soberón: Institute of Biotechnology, Universidad Nacional Autónoma de México, Cuernavaca, Morelos 62210, México
Peter D. Olson: The Natural History Museum, Cromwell Road, London SW7 5BD, UK
Juan P. Laclette: Institute of Biomedical Research, Universidad Nacional Autónoma de México
Klaus Brehm: University of Würzburg, Institute of Hygiene and Microbiology
Matthew Berriman: Parasite Genomics, Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SA, UK

Nature, 2013, vol. 496, issue 7443, 57-63

Abstract: 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.

Date: 2013
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DOI: 10.1038/nature12031

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