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The genomes of four tapeworm species reveal adaptations to parasitism

Author

Listed:
  • Isheng J. Tsai

    (Parasite Genomics, Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SA, UK
    Faculty of Medicine, University of Miyazaki, Miyazaki 889-1692, Japan)

  • 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
    Institute of Biotechnology, Universidad Nacional Autónoma de México, Cuernavaca, Morelos 62210, México)

  • 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
    School of Natural Sciences and Regenerative Medicine Institute (REMEDI), National University of Ireland Galway, University Road)

  • 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
    Instituto Nacional de Medicina Genómica, Periférico Sur No. 4809 Col. Arenal Tepepan, Delegación Tlalpan, 14610 México, D.F., 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)

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.

Suggested Citation

  • 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 Aslet, 2013. "The genomes of four tapeworm species reveal adaptations to parasitism," Nature, Nature, vol. 496(7443), pages 57-63, April.
    • Handle: RePEc:nat:nature:v:496:y:2013:i:7443:d:10.1038_nature12031
    DOI: 10.1038/nature12031
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    1. Doron Stupp & Elad Sharon & Idit Bloch & Marinka Zitnik & Or Zuk & Yuval Tabach, 2021. "Co-evolution based machine-learning for predicting functional interactions between human genes," Nature Communications, Nature, vol. 12(1), pages 1-14, December.

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