title: The genomes of four tapeworm species reveal adaptations to parasitism.
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.
authors.affiliation: Parasite Genomics, Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SA, UK.
authors.forename: Isheng J
authors.initials: IJ
authors.lastname: Tsai
authors.affiliation: Parasite Genomics, Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SA, UK.
authors.forename: Magdalena
authors.initials: M
authors.lastname: Zarowiecki
authors.affiliation: Parasite Genomics, Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SA, UK.
authors.forename: Nancy
authors.initials: N
authors.lastname: Holroyd
authors.affiliation: Institute of Biotechnology, Universidad Nacional Autónoma de México, 04510 México D.F., México.
authors.forename: Alejandro
authors.initials: A
authors.lastname: Garciarrubio
authors.affiliation: Parasite Genomics, Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SA, UK; Institute of Biotechnology, Universidad Nacional Autónoma de México, 04510 México D.F., México.
authors.forename: Alejandro
authors.initials: A
authors.lastname: Sánchez-Flores
authors.affiliation: Parasite Genomics, Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SA, UK.
authors.forename: Karen L
authors.initials: KL
authors.lastname: Brooks
authors.affiliation: Parasite Genomics, Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SA, UK.
authors.forename: Alan
authors.initials: A
authors.lastname: Tracey
authors.affiliation: Institute of Biomedical Research, Universidad Nacional Autónoma de México, 04510 México D.F., México.
authors.forename: Raúl J
authors.initials: RJ
authors.lastname: Bobes
authors.affiliation: Institute of Biomedical Research, Universidad Nacional Autónoma de México, 04510 México D.F., México.
authors.forename: Gladis
authors.initials: G
authors.lastname: Fragoso
authors.affiliation: Institute of Biomedical Research, Universidad Nacional Autónoma de México, 04510 México D.F., México.
authors.forename: Edda
authors.initials: E
authors.lastname: Sciutto
authors.affiliation: Parasite Genomics, Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SA, UK.
authors.forename: Martin
authors.initials: M
authors.lastname: Aslett
authors.affiliation: Parasite Genomics, Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SA, UK.
authors.forename: Helen
authors.initials: H
authors.lastname: Beasley
authors.affiliation: Parasite Genomics, Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SA, UK.
authors.forename: Hayley M
authors.initials: HM
authors.lastname: Bennett
authors.affiliation: 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.
authors.forename: Xuepeng
authors.initials: X
authors.lastname: Cai
authors.affiliation: 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.
authors.forename: Federico
authors.initials: F
authors.lastname: Camicia
authors.affiliation: Parasite Genomics, Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SA, UK.
authors.forename: Richard
authors.initials: R
authors.lastname: Clark
authors.affiliation: 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.
authors.forename: Marcela
authors.initials: M
authors.lastname: Cucher
authors.affiliation: Parasite Genomics, Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SA, UK.
authors.forename: Nishadi
authors.initials: N
authors.lastname: De Silva
authors.affiliation: Department of Biomedical Sciences, Iowa State University, Ames, Iowa 50011, USA.
authors.forename: Tim A
authors.initials: TA
authors.lastname: Day
authors.affiliation: Institute of Parasitology, Vetsuisse Faculty, University of Zürich, Winterthurerstrasse 266a, CH-8057 Zürich, Switzerland.
authors.forename: Peter
authors.initials: P
authors.lastname: Deplazes
authors.affiliation: Institute of Biotechnology, Universidad Nacional Autónoma de México, 04510 México D.F., México.
authors.forename: Karel
authors.initials: K
authors.lastname: Estrada
authors.affiliation: Cátedra de Inmunologá, Facultad de Quámica, Universidad de la República. Av. Alfredo Navarro 3051, piso 2, Montevideo, CP 11600, Uruguay.
authors.forename: Cecilia
authors.initials: C
authors.lastname: Fernández
authors.affiliation: Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS, UK.
authors.forename: Peter W H
authors.initials: PWH
authors.lastname: Holland
authors.affiliation: 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.
authors.forename: Junling
authors.initials: J
authors.lastname: Hou
authors.affiliation: Beijing Institute of Genomics, Chinese Academy of Sciences, No.7 Beitucheng West Road, Chaoyang District, Beijing 100029, PR China.
authors.forename: Songnian
authors.initials: S
authors.lastname: Hu
authors.affiliation: Parasite Genomics, Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SA, UK.
authors.forename: Thomas
authors.initials: T
authors.lastname: Huckvale
authors.affiliation: Department of Biochemistry & Molecular and Medical Genetics, University of Toronto, Program in Molecular Structure & Function, The Hospital for Sick Children, Toronto, Ontario, Canada.
authors.forename: Stacy S
authors.initials: SS
authors.lastname: Hung
authors.affiliation: 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.
authors.forename: Laura
authors.initials: L
authors.lastname: Kamenetzky
authors.affiliation: Parasite Genomics, Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SA, UK.
authors.forename: Jacqueline A
authors.initials: JA
authors.lastname: Keane
authors.affiliation: University of Würzburg, Institute of Hygiene and Microbiology, Würzburg, Germany.
authors.forename: Ferenc
authors.initials: F
authors.lastname: Kiss
authors.affiliation: University of Würzburg, Institute of Hygiene and Microbiology, Würzburg, Germany.
authors.forename: Uriel
authors.initials: U
authors.lastname: Koziol
authors.affiliation: Parasite Genomics, Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SA, UK.
authors.forename: Olivia
authors.initials: O
authors.lastname: Lambert
authors.affiliation: Beijing Institute of Genomics, Chinese Academy of Sciences, No.7 Beitucheng West Road, Chaoyang District, Beijing 100029, PR China.
authors.forename: Kan
authors.initials: K
authors.lastname: Liu
authors.affiliation: 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.
authors.forename: Xuenong
authors.initials: X
authors.lastname: Luo
authors.affiliation: Beijing Institute of Genomics, Chinese Academy of Sciences, No.7 Beitucheng West Road, Chaoyang District, Beijing 100029, PR China.
authors.forename: Yingfeng
authors.initials: Y
authors.lastname: Luo
authors.affiliation: 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.
authors.forename: Natalia
authors.initials: N
authors.lastname: Macchiaroli
authors.affiliation: Parasite Genomics, Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SA, UK.
authors.forename: Sarah
authors.initials: S
authors.lastname: Nichol
authors.affiliation: Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS, UK.
authors.forename: Jordi
authors.initials: J
authors.lastname: Paps
authors.affiliation: Department of Biochemistry & Molecular and Medical Genetics, University of Toronto, Program in Molecular Structure & Function, The Hospital for Sick Children, Toronto, Ontario, Canada.
authors.forename: John
authors.initials: J
authors.lastname: Parkinson
authors.affiliation: Department of Life Sciences, The Natural History Museum, Cromwell Road, London SW7 5BD, UK.
authors.forename: Natasha
authors.initials: N
authors.lastname: Pouchkina-Stantcheva
authors.affiliation: Department of Life Sciences, The Natural History Museum, Cromwell Road, London SW7 5BD, UK; Department of Zoology, School of Natural Sciences and Regenerative Medicine Institute (REMEDI), National University of Ireland Galway, University Road, Galway, Ireland.
authors.forename: Nick
authors.initials: N
authors.lastname: Riddiford
authors.affiliation: 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.
authors.forename: Mara
authors.initials: M
authors.lastname: Rosenzvit
authors.affiliation: Cátedra de Inmunologá, Facultad de Quámica, Universidad de la República. Av. Alfredo Navarro 3051, piso 2, Montevideo, CP 11600, Uruguay.
authors.forename: Gustavo
authors.initials: G
authors.lastname: Salinas
authors.affiliation: Department of Ecosystem and Public Health, Faculty of Veterinary Medicine, University of Calgary, Calgary, Canada.
authors.forename: James D
authors.initials: JD
authors.lastname: Wasmuth
authors.affiliation: Institute of Parasitology, McGill University, 2111 Lakeshore Road, Ste. Anne de Bellevue, Quebec, H9X 3V9. Canada.
authors.forename: Mostafa
authors.initials: M
authors.lastname: Zamanian
authors.affiliation: 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.
authors.forename: Yadong
authors.initials: Y
authors.lastname: Zheng
authors.affiliation: 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.
authors.forename: Jianping
authors.initials: J
authors.lastname: Cai
authors.affiliation: Institute of Biotechnology, Universidad Nacional Autónoma de México, 04510 México D.F., México; National Institute of Genomic Medicine, Ministry of Health, 01900, México D.F., México.
authors.forename: Xavier
authors.initials: X
authors.lastname: Soberón
authors.affiliation: Department of Life Sciences, The Natural History Museum, Cromwell Road, London SW7 5BD, UK.
authors.forename: Peter D
authors.initials: PD
authors.lastname: Olson
authors.affiliation: Institute of Biomedical Research, Universidad Nacional Autónoma de México, 04510 México D.F., México.
authors.forename: Juan P
authors.initials: JP
authors.lastname: Laclette
authors.affiliation: University of Würzburg, Institute of Hygiene and Microbiology, Würzburg, Germany.
authors.forename: Klaus
authors.initials: K
authors.lastname: Brehm
authors.affiliation: Parasite Genomics, Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SA, UK.
authors.forename: Matthew
authors.initials: M
authors.lastname: Berriman
mesh_terms: D000222:Adaptation, Physiological / Q000235:genetics*; D000818:Animals; D005075:Biological Evolution; D002589:Cestoda / Q000187:drug effects / Q000235:genetics* / Q000502:physiology; D002590:Cestode Infections / Q000188:drug therapy / Q000378:metabolism; D017124:Conserved Sequence / Q000235:genetics; D048209:Echinococcus granulosus / Q000235:genetics; D048210:Echinococcus multilocularis / Q000187:drug effects / Q000235:genetics / Q000378:metabolism; D017238:Genes, Helminth / Q000235:genetics; D005801:Genes, Homeobox / Q000235:genetics; D049751:Genome, Helminth / Q000235:genetics*; D018840:HSP70 Heat-Shock Proteins / Q000235:genetics; D006801:Humans; D006926:Hymenolepis / Q000235:genetics; D053858:Metabolic Networks and Pathways / Q000235:genetics; D058990:Molecular Targeted Therapy; D010271:Parasites / Q000187:drug effects / Q000235:genetics* / Q000502:physiology; D020543:Proteome / Q000235:genetics; D013234:Stem Cells / Q000166:cytology / Q000378:metabolism; D041201:Taenia solium / Q000235:genetics
chemical_list: D018840:HSP70 Heat-Shock Proteins; D020543:Proteome