Genomic insights into the Ixodes scapularis tick vector of Lyme disease

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 Thimmapuram; Jason R. Miller; Brian P. Walenz; Sergey Koren; Jessica B. Hostetler; Mathangi Thiagarajan; Vinita S. Joardar; Linda I. Hannick; Shelby Bidwell; Martin P. Hammond; Sarah Young; Qiandong Zeng; Jenica L. Abrudan; Francisca C. Almeida; Nieves Ayllón; Ketaki Bhide; Brooke W. Bissinger; Elena Bonzon-Kulichenko; Steven D. Buckingham; Daniel R. Caffrey; Melissa J. Caimano; Vincent Croset; Timothy Driscoll; Don Gilbert; Joseph J. Gillespie; Gloria I. Giraldo-Calderón; Jeffrey M. Grabowski; David Jiang; Sayed M.S. Khalil; Donghun Kim; Katherine M. Kocan; Juraj Koči; Richard J. Kuhn; Timothy J. Kurtti; Kristin Lees; Emma G. Lang; Ryan C. Kennedy; Hyeogsun Kwon; Rushika Perera; Yumin Qi; Justin D. Radolf; Joyce M. Sakamoto; Alejandro Sánchez-Gracia; Maiara S. Severo; Neal Silverman; Ladislav Šimo; Marta Tojo; Cristian Tornador; Janice P. Van Zee; Jesús Vázquez; Filipe G. Vieira; Margarita Villar; Adam R. Wespiser; Yunlong Yang; Jiwei Zhu; Peter Arensburger; Patricia V. Pietrantonio; Stephen C. Barker; Renfu Shao; Evgeny M. Zdobnov; Frank Hauser; Cornelis J.P. Grimmelikhuijzen; Yoonseong Park; Julio Rozas; Richard Benton; Joao H.F. Pedra; David R. Nelson; Maria F. Unger; Jose M.C. Tubio; Zhijian Tu; Hugh M. Robertson; Martin Shumway; Granger Sutton; Jennifer R. Wortman; Daniel Lawson; Stephen K. Wikel; Vishvanath M. Nene; Claire M. Fraser; Frank H. Collins; Bruce Birren; Karen E. Nelson; Elisabet Caler; Catherine A. Hill

doi:10.1038/ncomms10507

Genomic insights into the Ixodes scapularis tick vector of Lyme disease

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 Thimmapuram
, Jason R. Miller
, Brian P. Walenz
, Sergey Koren
, Jessica B. Hostetler
, Mathangi Thiagarajan
, Vinita S. Joardar
, Linda I. Hannick
, Shelby Bidwell
, Martin P. Hammond

Sarah Young, Qiandong Zeng, Jenica L. Abrudan, Francisca C. Almeida, Nieves Ayllón, Ketaki Bhide, Brooke W. Bissinger, Elena Bonzon-Kulichenko, Steven D. Buckingham, Daniel R. Caffrey, Melissa J. Caimano, Vincent Croset, Timothy Driscoll, Don Gilbert, Joseph J. Gillespie, Gloria I. Giraldo-Calderón, Jeffrey M. Grabowski, David Jiang, Sayed M.S. Khalil, Donghun Kim, Katherine M. Kocan, Juraj Koči, Richard J. Kuhn, Timothy J. Kurtti, Kristin Lees, Emma G. Lang, Ryan C. Kennedy, Hyeogsun Kwon, Rushika Perera, Yumin Qi, Justin D. Radolf, Joyce M. Sakamoto, Alejandro Sánchez-Gracia, Maiara S. Severo, Neal Silverman, Ladislav Šimo, Marta Tojo, Cristian Tornador, Janice P. Van Zee, Jesús Vázquez, Filipe G. Vieira, Margarita Villar, Adam R. Wespiser, Yunlong Yang, Jiwei Zhu, Peter Arensburger, Patricia V. Pietrantonio, Stephen C. Barker, Renfu Shao, Evgeny M. Zdobnov, Frank Hauser, Cornelis J.P. Grimmelikhuijzen, Yoonseong Park, Julio Rozas, Richard Benton, Joao H.F. Pedra, David R. Nelson, Maria F. Unger, Jose M.C. Tubio, Zhijian Tu, Hugh M. Robertson, Martin Shumway, Granger Sutton, Jennifer R. Wortman, Daniel Lawson, Stephen K. Wikel, Vishvanath M. Nene, Claire M. Fraser, Frank H. Collins, Bruce Birren, Karen E. Nelson, Elisabet Caler, Catherine A. Hill

Purdue University
University of Nevada, Reno
Monsanto Company
Old Dominion University
North Carolina State University
University of Geneva
Swiss Institute of Bioinformatics
Massachusetts Institute of Technology
Department of Molecular Biology
University College London
SaBio, Spain
Oklahoma State University
National Institutes of Health
Wellcome Trust
University of Cambridge
J. Craig Venter Institute
Leidos Inc
University of Notre Dame
University of Nevada, Las Vegas
University of Barcelona
AgBiome
Centro Nacional de Investigaciones Cardiovasculares Carlos III
University of Massachusetts Medical School
University of Connecticut
University of Lausanne
University of Oxford
Virginia Polytechnic Institute and State University
West Virginia University
Indiana University Bloomington
University of Maryland, Baltimore
Agricultural Research Center, Giza
Kansas State University
University of Minnesota Twin Cities
University of Manchester
National University of Singapore
University of California at San Francisco
Texas A&M University
Iowa State University
Colorado State University
Pennsylvania State University
University of California at Riverside
Max Planck Institute for Infection Biology
École nationale vétérinaire d'Alfort
University of Santiago de Compostela
Pompeu Fabra University
California State Polytechnic University Pomona
University of Queensland
University of the Sunshine Coast
University of Copenhagen
University of Tennessee Health Science Center
Wellcome Trust Sanger Institute
University of Vigo
University of Illinois at Urbana-Champaign
Seres Therapeutics, Inc.
Quinnipiac University
International Livestock Research Institute

Research output: Contribution to journal › Article › peer-review

431 Scopus citations

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.

Original language	English
Article number	10507
Journal	Nature Communications
Volume	7
DOIs	https://doi.org/10.1038/ncomms10507
State	Published - 9 Feb 2016

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SDG 3 Good Health and Well-being

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10.1038/ncomms10507

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Gulia-Nuss, M., Nuss, A. B., Meyer, J. M., Sonenshine, D. E., Roe, R. M., Waterhouse, R. M., Sattelle, D. B., De La Fuente, J., Ribeiro, J. M., Megy, K., Thimmapuram, J., Miller, J. R., Walenz, B. P., Koren, S., Hostetler, J. B., Thiagarajan, M., Joardar, V. S., Hannick, L. I., Bidwell, S., ... Hill, C. A. (2016). Genomic insights into the Ixodes scapularis tick vector of Lyme disease. Nature Communications, 7, Article 10507. https://doi.org/10.1038/ncomms10507

@article{469c6287fb82488aa18e04e9c1b269f3,

title = "Genomic insights into the Ixodes scapularis tick vector of Lyme disease",

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.",

author = "Monika Gulia-Nuss and Nuss, \{Andrew B.\} and Meyer, \{Jason M.\} and Sonenshine, \{Daniel E.\} and Roe, \{R. Michael\} and Waterhouse, \{Robert M.\} and Sattelle, \{David B.\} and \{De La Fuente\}, Jos{\'e} and Ribeiro, \{Jose M.\} and Karine Megy and Jyothi Thimmapuram and Miller, \{Jason R.\} and Walenz, \{Brian P.\} and Sergey Koren and Hostetler, \{Jessica B.\} and Mathangi Thiagarajan and Joardar, \{Vinita S.\} and Hannick, \{Linda I.\} and Shelby Bidwell and Hammond, \{Martin P.\} and Sarah Young and Qiandong Zeng and Abrudan, \{Jenica L.\} and Almeida, \{Francisca C.\} and Nieves Ayll{\'o}n and Ketaki Bhide and Bissinger, \{Brooke W.\} and Elena Bonzon-Kulichenko and Buckingham, \{Steven D.\} and Caffrey, \{Daniel R.\} and Caimano, \{Melissa J.\} and Vincent Croset and Timothy Driscoll and Don Gilbert and Gillespie, \{Joseph J.\} and Giraldo-Calder{\'o}n, \{Gloria I.\} and Grabowski, \{Jeffrey M.\} and David Jiang and Khalil, \{Sayed M.S.\} and Donghun Kim and Kocan, \{Katherine M.\} and Juraj Ko{\v c}i and Kuhn, \{Richard J.\} and Kurtti, \{Timothy J.\} and Kristin Lees and Lang, \{Emma G.\} and Kennedy, \{Ryan C.\} and Hyeogsun Kwon and Rushika Perera and Yumin Qi and Radolf, \{Justin D.\} and Sakamoto, \{Joyce M.\} and Alejandro S{\'a}nchez-Gracia and Severo, \{Maiara S.\} and Neal Silverman and Ladislav {\v S}imo and Marta Tojo and Cristian Tornador and \{Van Zee\}, \{Janice P.\} and Jes{\'u}s V{\'a}zquez and Vieira, \{Filipe G.\} and Margarita Villar and Wespiser, \{Adam R.\} and Yunlong Yang and Jiwei Zhu and Peter Arensburger and Pietrantonio, \{Patricia V.\} and Barker, \{Stephen C.\} and Renfu Shao and Zdobnov, \{Evgeny M.\} and Frank Hauser and Grimmelikhuijzen, \{Cornelis J.P.\} and Yoonseong Park and Julio Rozas and Richard Benton and Pedra, \{Joao H.F.\} and Nelson, \{David R.\} and Unger, \{Maria F.\} and Tubio, \{Jose M.C.\} and Zhijian Tu and Robertson, \{Hugh M.\} and Martin Shumway and Granger Sutton and Wortman, \{Jennifer R.\} and Daniel Lawson and Wikel, \{Stephen K.\} and Nene, \{Vishvanath M.\} and Fraser, \{Claire M.\} and Collins, \{Frank H.\} and Bruce Birren and Nelson, \{Karen E.\} and Elisabet Caler and Hill, \{Catherine A.\}",

year = "2016",

month = feb,

day = "9",

doi = "10.1038/ncomms10507",

language = "English",

volume = "7",

journal = "Nature Communications",

issn = "2041-1723",

publisher = "Nature Research",

}

Gulia-Nuss, M, Nuss, AB, Meyer, JM, Sonenshine, DE, Roe, RM, Waterhouse, RM, Sattelle, DB, De La Fuente, J, Ribeiro, JM, Megy, K, Thimmapuram, J, Miller, JR, Walenz, BP, Koren, S, Hostetler, JB, Thiagarajan, M, Joardar, VS, Hannick, LI, Bidwell, S, Hammond, MP, Young, S, Zeng, Q, Abrudan, JL, Almeida, FC, Ayllón, N, Bhide, K, Bissinger, BW, Bonzon-Kulichenko, E, Buckingham, SD, Caffrey, DR, Caimano, MJ, Croset, V, Driscoll, T, Gilbert, D, Gillespie, JJ, Giraldo-Calderón, GI, Grabowski, JM, Jiang, D, Khalil, SMS, Kim, D, Kocan, KM, Koči, J, Kuhn, RJ, Kurtti, TJ, Lees, K, Lang, EG, Kennedy, RC, Kwon, H, Perera, R, Qi, Y, Radolf, JD, Sakamoto, JM, Sánchez-Gracia, A, Severo, MS, Silverman, N, Šimo, L, Tojo, M, Tornador, C, Van Zee, JP, Vázquez, J, Vieira, FG, Villar, M, Wespiser, AR, Yang, Y, Zhu, J, Arensburger, P, Pietrantonio, PV, Barker, SC, Shao, R, Zdobnov, EM, Hauser, F, Grimmelikhuijzen, CJP, Park, Y, Rozas, J, Benton, R, Pedra, JHF, Nelson, DR, Unger, MF, Tubio, JMC, Tu, Z, Robertson, HM, Shumway, M, Sutton, G, Wortman, JR, Lawson, D, Wikel, SK, Nene, VM, Fraser, CM, Collins, FH, Birren, B, Nelson, KE, Caler, E & Hill, CA 2016, 'Genomic insights into the Ixodes scapularis tick vector of Lyme disease', Nature Communications, vol. 7, 10507. https://doi.org/10.1038/ncomms10507

TY - JOUR

T1 - Genomic insights into the Ixodes scapularis tick vector of Lyme disease

AU - Gulia-Nuss, Monika

AU - Nuss, Andrew B.

AU - Meyer, Jason M.

AU - Sonenshine, Daniel E.

AU - Roe, R. Michael

AU - Waterhouse, Robert M.

AU - Sattelle, David B.

AU - De La Fuente, José

AU - Ribeiro, Jose M.

AU - Megy, Karine

AU - Thimmapuram, Jyothi

AU - Miller, Jason R.

AU - Walenz, Brian P.

AU - Koren, Sergey

AU - Hostetler, Jessica B.

AU - Thiagarajan, Mathangi

AU - Joardar, Vinita S.

AU - Hannick, Linda I.

AU - Bidwell, Shelby

AU - Hammond, Martin P.

AU - Young, Sarah

AU - Zeng, Qiandong

AU - Abrudan, Jenica L.

AU - Almeida, Francisca C.

AU - Ayllón, Nieves

AU - Bhide, Ketaki

AU - Bissinger, Brooke W.

AU - Bonzon-Kulichenko, Elena

AU - Buckingham, Steven D.

AU - Caffrey, Daniel R.

AU - Caimano, Melissa J.

AU - Croset, Vincent

AU - Driscoll, Timothy

AU - Gilbert, Don

AU - Gillespie, Joseph J.

AU - Giraldo-Calderón, Gloria I.

AU - Grabowski, Jeffrey M.

AU - Jiang, David

AU - Khalil, Sayed M.S.

AU - Kim, Donghun

AU - Kocan, Katherine M.

AU - Koči, Juraj

AU - Kuhn, Richard J.

AU - Kurtti, Timothy J.

AU - Lees, Kristin

AU - Lang, Emma G.

AU - Kennedy, Ryan C.

AU - Kwon, Hyeogsun

AU - Perera, Rushika

AU - Qi, Yumin

AU - Radolf, Justin D.

AU - Sakamoto, Joyce M.

AU - Sánchez-Gracia, Alejandro

AU - Severo, Maiara S.

AU - Silverman, Neal

AU - Šimo, Ladislav

AU - Tojo, Marta

AU - Tornador, Cristian

AU - Van Zee, Janice P.

AU - Vázquez, Jesús

AU - Vieira, Filipe G.

AU - Villar, Margarita

AU - Wespiser, Adam R.

AU - Yang, Yunlong

AU - Zhu, Jiwei

AU - Arensburger, Peter

AU - Pietrantonio, Patricia V.

AU - Barker, Stephen C.

AU - Shao, Renfu

AU - Zdobnov, Evgeny M.

AU - Hauser, Frank

AU - Grimmelikhuijzen, Cornelis J.P.

AU - Park, Yoonseong

AU - Rozas, Julio

AU - Benton, Richard

AU - Pedra, Joao H.F.

AU - Nelson, David R.

AU - Unger, Maria F.

AU - Tubio, Jose M.C.

AU - Tu, Zhijian

AU - Robertson, Hugh M.

AU - Shumway, Martin

AU - Sutton, Granger

AU - Wortman, Jennifer R.

AU - Lawson, Daniel

AU - Wikel, Stephen K.

AU - Nene, Vishvanath M.

AU - Fraser, Claire M.

AU - Collins, Frank H.

AU - Birren, Bruce

AU - Nelson, Karen E.

AU - Caler, Elisabet

AU - Hill, Catherine A.

PY - 2016/2/9

Y1 - 2016/2/9

N2 - 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.

AB - 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.

UR - https://www.scopus.com/pages/publications/84957895144

U2 - 10.1038/ncomms10507

DO - 10.1038/ncomms10507

M3 - Article

C2 - 26856261

AN - SCOPUS:84957895144

SN - 2041-1723

VL - 7

JO - Nature Communications

JF - Nature Communications

M1 - 10507

ER -

Genomic insights into the Ixodes scapularis tick vector of Lyme disease

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