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Genomic insights into the Ixodes scapularis tick vector of Lyme disease

Author

Listed:
  • Monika Gulia-Nuss

    (Purdue University
    Present address: Department of Biochemistry and Molecular Biology, University of Nevada, Reno, Nevada 89503, USA)

  • Andrew B. Nuss

    (Purdue University
    Present address: Department of Agriculture, Nutrition, and Veterinary Science, University of Nevada, Reno, Nevada 89557, USA)

  • Jason M. Meyer

    (Purdue University
    Present address: Department of Biotechnology, Monsanto Company, Chesterfield, Missouri 63017, USA)

  • Daniel E. Sonenshine

    (Old Dominion University)

  • R. Michael Roe

    (North Carolina State University)

  • Robert M. Waterhouse

    (University of Geneva Medical School
    Swiss Institute of Bioinformatics
    Computer Science and Artificial Intelligence Laboratory, Massachusetts Institute of Technology
    The Broad Institute of MIT and Harvard)

  • David B. Sattelle

    (Centre for Respiratory Biology, University College London)

  • José de la Fuente

    (SaBio, Instituto de Investigación en Recursos Cinegéticos, IREC-CSIC-UCLM-JCCM, Ronda de Toledo sn
    Center for Veterinary Health Sciences, Oklahoma State University)

  • Jose M. Ribeiro

    (Laboratory of Malaria and Vector Research, NIAID)

  • Karine Megy

    (VectorBase/EMBL-EBI, Wellcome Trust Genome Campus
    Present address: Department of Haematology, University of Cambridge, NHSBT Building, Long Road, Cambridge CB2 0PT, UK)

  • Jyothi Thimmapuram

    (Bioinformatics Core, Purdue University)

  • Jason R. Miller

    (J. Craig Venter Institute)

  • Brian P. Walenz

    (J. Craig Venter Institute
    Present address: Genome Informatics Section, Computational and Statistical Genomics Branch, National Human Genome Research Institute, National Institutes of Health, Bethesda, Maryland 20892, USA)

  • Sergey Koren

    (J. Craig Venter Institute
    Present address: Genome Informatics Section, Computational and Statistical Genomics Branch, National Human Genome Research Institute, National Institutes of Health, Bethesda, Maryland 20892, USA)

  • Jessica B. Hostetler

    (J. Craig Venter Institute
    Present address: Laboratory of Malaria and Vector Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland 20892, USA)

  • Mathangi Thiagarajan

    (J. Craig Venter Institute
    Present address: Leidos Biomedical Research Inc., Frederick National Laboratory for Cancer Research, Frederick, Maryland 21702, USA)

  • Vinita S. Joardar

    (J. Craig Venter Institute
    Present address: National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, Maryland 20894, USA)

  • Linda I. Hannick

    (J. Craig Venter Institute
    Present address: Leidos Biomedical Research Inc., Frederick National Laboratory for Cancer Research, Frederick, Maryland 21702, USA)

  • Shelby Bidwell

    (J. Craig Venter Institute
    Present address: National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, Maryland 20894, USA)

  • Martin P. Hammond

    (VectorBase/EMBL-EBI, Wellcome Trust Genome Campus)

  • Sarah Young

    (Genome Sequencing and Analysis Program, Broad Institute)

  • Qiandong Zeng

    (Genome Sequencing and Analysis Program, Broad Institute)

  • Jenica L. Abrudan

    (University of Notre Dame
    Present address: Nevada Institute of Personalized Medicine, University of Nevada, Las Vegas, Nevada, 89154, USA)

  • Francisca C. Almeida

    (Departament de Genètica & Institut de Recerca de la Biodiversitat (IRBio), Universitat de Barcelona)

  • Nieves Ayllón

    (SaBio, Instituto de Investigación en Recursos Cinegéticos, IREC-CSIC-UCLM-JCCM, Ronda de Toledo sn)

  • Ketaki Bhide

    (Bioinformatics Core, Purdue University)

  • Brooke W. Bissinger

    (North Carolina State University
    Present address: AgBiome, Inc., Research Triangle Park, North Carolina 27709, USA)

  • Elena Bonzon-Kulichenko

    (Vascular Physiopathology, Centro Nacional de Investigaciones Cardiovasculares)

  • Steven D. Buckingham

    (Centre for Respiratory Biology, University College London)

  • Daniel R. Caffrey

    (University of Massachusetts Medical School)

  • Melissa J. Caimano

    (University of Connecticut Health Center)

  • Vincent Croset

    (Center for Integrative Genomics, Faculty of Biology and Medicine, University of Lausanne
    Present address: Centre for Neural Circuits and Behaviour, University of Oxford, Oxford OX1 3SR, UK)

  • Timothy Driscoll

    (Genetics, Bioinformatics, and Computational Biology Program, Virginia Bioinformatics Institute at Virginia Tech
    Present address: Department of Biology, West Virginia University, Morgantown 26505, West Virginia)

  • Don Gilbert

    (Indiana University)

  • Joseph J. Gillespie

    (Genetics, Bioinformatics, and Computational Biology Program, Virginia Bioinformatics Institute at Virginia Tech
    Present address: Department of Microbiology & Immunology, University of Maryland School of Medicine, Baltimore, Maryland 21201, USA)

  • Gloria I. Giraldo-Calderón

    (Purdue University
    University of Notre Dame)

  • Jeffrey M. Grabowski

    (Purdue University
    Markey Center for Structural Biology, Purdue University
    Present address: Rocky Mountain Laboratories, Biology of Vector-Borne Viruses Section, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Hamilton, Montana 59840, USA)

  • David Jiang

    (Virginia Tech)

  • Sayed M. S. Khalil

    (Agricultural Genetic Engineering Research Institute)

  • Donghun Kim

    (Texas A&M University
    Present address: Department of Entomology, Kansas State University, Manhattan, Kansas 66506, USA)

  • Katherine M. Kocan

    (Center for Veterinary Health Sciences, Oklahoma State University)

  • Juraj Koči

    (Kansas State University
    Present address: Department of Veterinary Medicine, University of Maryland, School of Medicine, Baltimore, Maryland 21201, USA)

  • Richard J. Kuhn

    (Markey Center for Structural Biology, Purdue University)

  • Timothy J. Kurtti

    (University of Minnesota)

  • Kristin Lees

    (Faculty of Life Sciences, University of Manchester
    Present address: Department of Medicine, Yong Loo Lin School of Medicine, National University of Singapore, Singapore 119074)

  • Emma G. Lang

    (Purdue University)

  • Ryan C. Kennedy

    (University of California)

  • Hyeogsun Kwon

    (Texas A&M University
    Present address: Department of Entomology, Iowa State University, Ames, Iowa 50011, USA)

  • Rushika Perera

    (Markey Center for Structural Biology, Purdue University
    Present address: Department of Microbiology, Immunology, and Pathology, Arthropod-borne & Infectious Diseases Laboratory, Colorado State University, Fort Collins, Colorado 80523, USA)

  • Yumin Qi

    (Virginia Tech)

  • Justin D. Radolf

    (University of Connecticut Health Center)

  • Joyce M. Sakamoto

    (The Pennsylvania State University)

  • Alejandro Sánchez-Gracia

    (Departament de Genètica & Institut de Recerca de la Biodiversitat (IRBio), Universitat de Barcelona)

  • Maiara S. Severo

    (Center for Disease Vector Research, University of California
    Present address: National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, Maryland 20894, USA)

  • Neal Silverman

    (University of Massachusetts Medical School)

  • Ladislav Šimo

    (Kansas State University
    Present address: French National Institute of Agricultural Research, UMR-BIPAR INRA-ANSES-ENVA, Maisons-Alfort, 94700 France)

  • Marta Tojo

    (Cambridge Genomic Services, University of Cambridge
    School of Medicine-CIMUS-Instituto de Investigaciones Sanitarias, University of Santiago de Compostela)

  • Cristian Tornador

    (Universidad Pompeu Fabra)

  • Janice P. Van Zee

    (Purdue University)

  • Jesús Vázquez

    (Vascular Physiopathology, Centro Nacional de Investigaciones Cardiovasculares)

  • Filipe G. Vieira

    (Departament de Genètica & Institut de Recerca de la Biodiversitat (IRBio), Universitat de Barcelona)

  • Margarita Villar

    (SaBio, Instituto de Investigación en Recursos Cinegéticos, IREC-CSIC-UCLM-JCCM, Ronda de Toledo sn)

  • Adam R. Wespiser

    (University of Massachusetts Medical School)

  • Yunlong Yang

    (Texas A&M University)

  • Jiwei Zhu

    (North Carolina State University)

  • Peter Arensburger

    (California State Polytechnic University)

  • Patricia V. Pietrantonio

    (Texas A&M University)

  • Stephen C. Barker

    (Parasitology Section, School of Chemistry & Molecular Biosciences, University of Queensland)

  • Renfu Shao

    (GeneCology Research Centre, Faculty of Science, Health, Education and Engineering, University of the Sunshine Coast)

  • Evgeny M. Zdobnov

    (University of Geneva Medical School
    Swiss Institute of Bioinformatics)

  • Frank Hauser

    (Center for Functional and Comparative Insect Genomics, University of Copenhagen)

  • Cornelis J. P. Grimmelikhuijzen

    (Center for Functional and Comparative Insect Genomics, University of Copenhagen)

  • Yoonseong Park

    (Kansas State University)

  • Julio Rozas

    (Departament de Genètica & Institut de Recerca de la Biodiversitat (IRBio), Universitat de Barcelona)

  • Richard Benton

    (Center for Integrative Genomics, Faculty of Biology and Medicine, University of Lausanne)

  • Joao H. F. Pedra

    (Center for Disease Vector Research, University of California
    Present address: Department of Microbiology & Immunology, University of Maryland School of Medicine, Baltimore, Maryland 21201, USA)

  • David R. Nelson

    (Immunology & Biochemistry, University of Tennessee Health Science Center)

  • Maria F. Unger

    (University of Notre Dame)

  • Jose M. C. Tubio

    (Cancer Genome Project, Wellcome Trust Sanger Institute
    Genetics and Immunology, University of Vigo)

  • Zhijian Tu

    (Virginia Tech)

  • Hugh M. Robertson

    (University of Illinois at Urbana-Champaign)

  • Martin Shumway

    (J. Craig Venter Institute
    Present address: Department of Vector Biology, Max-Planck-Institut für Infektionsbiologie, Charitéplatz 1, 10117 Berlin, Germany)

  • Granger Sutton

    (J. Craig Venter Institute)

  • Jennifer R. Wortman

    (J. Craig Venter Institute
    Present address: Seres Therapeutics, Cambridge, MA 02142, USA)

  • Daniel Lawson

    (VectorBase/EMBL-EBI, Wellcome Trust Genome Campus)

  • Stephen K. Wikel

    (Frank H. Netter MD School of Medicine at Quinnipiac University)

  • Vishvanath M. Nene

    (J. Craig Venter Institute
    Present address: International Livestock Research Institute, Nairobi 00100, Kenya)

  • Claire M. Fraser

    (Institute for Genome Sciences, University of Maryland, School of Medicine)

  • Frank H. Collins

    (University of Notre Dame)

  • Bruce Birren

    (The Broad Institute of MIT and Harvard)

  • Karen E. Nelson

    (J. Craig Venter Institute)

  • Elisabet Caler

    (J. Craig Venter Institute
    Present address: National Heart, Lung, and Blood Institute, Division of Lung Diseases, National Institutes of Health, Bethesda, Maryland 20892, USA)

  • Catherine A. Hill

    (Purdue University)

Abstract

Ticks transmit more pathogens to humans and animals than any other arthropod. We describe the 2.1 Gbp nuclear genome of the tick, Ixodes scapularis (Say), which vectors pathogens that cause Lyme disease, human granulocytic anaplasmosis, babesiosis and other diseases. The large genome reflects accumulation of repetitive DNA, new lineages of retro-transposons, and gene architecture patterns resembling ancient metazoans rather than pancrustaceans. Annotation of scaffolds representing ∼57% of the genome, reveals 20,486 protein-coding genes and expansions of gene families associated with tick–host interactions. We report insights from genome analyses into parasitic processes unique to ticks, including host ‘questing’, prolonged feeding, cuticle synthesis, blood meal concentration, novel methods of haemoglobin digestion, haem detoxification, vitellogenesis and prolonged off-host survival. We identify proteins associated with the agent of human granulocytic anaplasmosis, an emerging disease, and the encephalitis-causing Langat virus, and a population structure correlated to life-history traits and transmission of the Lyme disease agent.

Suggested Citation

  • Monika Gulia-Nuss & Andrew B. Nuss & Jason M. Meyer & Daniel E. Sonenshine & R. Michael Roe & Robert M. Waterhouse & David B. Sattelle & José de la Fuente & Jose M. Ribeiro & Karine Megy & Jyothi Thim, 2016. "Genomic insights into the Ixodes scapularis tick vector of Lyme disease," Nature Communications, Nature, vol. 7(1), pages 1-13, April.
    • Handle: RePEc:nat:natcom:v:7:y:2016:i:1:d:10.1038_ncomms10507
    DOI: 10.1038/ncomms10507
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