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. HammondSarah 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 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

Research output: Contribution to journalArticle

161 Citations (Scopus)

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 languageEnglish (US)
Article number10507
JournalNature communications
Volume7
DOIs
StatePublished - Feb 9 2016

Fingerprint

Ixodes
Lyme Disease
genome
Ticks
Genes
Anaplasmosis
Genome
genes
pathogens
encephalitis
arthropods
Vitellogenesis
Babesiosis
Tick-Borne Encephalitis Viruses
proteins
annotations
Pathogens
Arthropods
hemoglobin
viruses

All Science Journal Classification (ASJC) codes

  • Chemistry(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Physics and Astronomy(all)

Cite this

Gulia-Nuss, M., Nuss, A. B., Meyer, J. M., Sonenshine, D. E., Roe, R. M., Waterhouse, R. M., ... Hill, C. A. (2016). Genomic insights into the Ixodes scapularis tick vector of Lyme disease. Nature communications, 7, [10507]. https://doi.org/10.1038/ncomms10507

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

In: Nature communications, Vol. 7, 10507, 09.02.2016.

Research output: Contribution to journalArticle

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, D, 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
Gulia-Nuss M, Nuss AB, Meyer JM, Sonenshine DE, Roe RM, Waterhouse RM et al. Genomic insights into the Ixodes scapularis tick vector of Lyme disease. Nature communications. 2016 Feb 9;7. 10507. https://doi.org/10.1038/ncomms10507
Gulia-Nuss, Monika ; Nuss, Andrew B. ; Meyer, Jason M. ; Sonenshine, Daniel E. ; Roe, R. Michael ; Waterhouse, Robert M. ; Sattelle, David B. ; De La Fuente, José ; Ribeiro, Jose M. ; Megy, Karine ; Thimmapuram, Jyothi ; Miller, Jason R. ; Walenz, Brian P. ; Koren, Sergey ; Hostetler, Jessica B. ; Thiagarajan, Mathangi ; Joardar, Vinita S. ; Hannick, Linda I. ; Bidwell, Shelby ; Hammond, Martin P. ; Young, Sarah ; Zeng, Qiandong ; Abrudan, Jenica L. ; Almeida, Francisca C. ; Ayllón, Nieves ; Bhide, Ketaki ; Bissinger, Brooke W. ; Bonzon-Kulichenko, Elena ; Buckingham, Steven D. ; Caffrey, Daniel R. ; Caimano, Melissa J. ; Croset, Vincent ; Driscoll, Timothy ; Gilbert, Don ; Gillespie, Joseph J. ; Giraldo-Calderón, Gloria I. ; Grabowski, Jeffrey M. ; Jiang, David ; Khalil, Sayed M.S. ; Kim, Donghun ; Kocan, Katherine M. ; Koči, Juraj ; Kuhn, Richard J. ; Kurtti, Timothy J. ; Lees, Kristin ; Lang, Emma G. ; Kennedy, Ryan C. ; Kwon, Hyeogsun ; Perera, Rushika ; Qi, Yumin ; Radolf, Justin D. ; Sakamoto, Joyce M. ; Sánchez-Gracia, Alejandro ; Severo, Maiara S. ; Silverman, Neal ; Šimo, Ladislav ; Tojo, Marta ; Tornador, Cristian ; Van Zee, Janice P. ; Vázquez, Jesús ; Vieira, Filipe G. ; Villar, Margarita ; Wespiser, Adam R. ; Yang, Yunlong ; Zhu, Jiwei ; Arensburger, Peter ; Pietrantonio, Patricia V. ; Barker, Stephen C. ; Shao, Renfu ; Zdobnov, Evgeny M. ; Hauser, Frank ; Grimmelikhuijzen, Cornelis J.P. ; Park, Yoonseong ; Rozas, Julio ; Benton, Richard ; Pedra, Joao H.F. ; Nelson, David ; Unger, Maria F. ; Tubio, Jose M.C. ; Tu, Zhijian ; Robertson, Hugh M. ; Shumway, Martin ; Sutton, Granger ; Wortman, Jennifer R. ; Lawson, Daniel ; Wikel, Stephen K. ; Nene, Vishvanath M. ; Fraser, Claire M. ; Collins, Frank H. ; Birren, Bruce ; Nelson, Karen E. ; Caler, Elisabet ; Hill, Catherine A. / Genomic insights into the Ixodes scapularis tick vector of Lyme disease. In: Nature communications. 2016 ; Vol. 7.
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AU - Waterhouse, Robert M.

AU - Sattelle, David B.

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AU - Thimmapuram, Jyothi

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AU - Hannick, Linda I.

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AU - Hammond, Martin P.

AU - Young, Sarah

AU - Zeng, Qiandong

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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.

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AU - Vázquez, Jesús

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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

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.

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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.

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