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 Jorge Garrett 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 (Cok) 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 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 Jorge Garrett 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 (Cok) 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

Cell and Neurobiology

Research output: Contribution to journal › Journal article › Research › peer-review

382 Citations (Scopus)

342 Downloads (Pure)

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
Number of pages	13
ISSN	2041-1723
DOIs	https://doi.org/10.1038/ncomms10507
Publication status	Published - 2016

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Genomic insights into the Ixodes scapularis tick vector of Lyme diseaseFinal published version, 3.37 MBLicence: CC BY

Cite this

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, [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; Garrett Vieira, Filipe Jorge; 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 (Cok); Park, Yoonseong; Rozas, Julio; Benton, Richard; Pedra, Joao H. F.; Nelson, David R; 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, 2016.

Research output: Contribution to journal › Journal article › Research › peer-review

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, Garrett Vieira, FJ, Villar, M, Wespiser, AR, Yang, Y, Zhu, J, Arensburger, P, Pietrantonio, PV, Barker, SC, Shao, R, Zdobnov, EM, Hauser, F , Grimmelikhuijzen, CC, 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

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 ; Garrett Vieira, Filipe Jorge ; 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 (Cok) ; Park, Yoonseong ; Rozas, Julio ; Benton, Richard ; Pedra, Joao H. F. ; Nelson, David R ; 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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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 {Garrett Vieira}, {Filipe Jorge} 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 (Cok)} 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",

doi = "10.1038/ncomms10507",

language = "English",

volume = "7",

journal = "Nature Communications",

issn = "2041-1723",

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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 - Garrett Vieira, Filipe Jorge

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 (Cok)

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

Y1 - 2016

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.

U2 - 10.1038/ncomms10507

DO - 10.1038/ncomms10507

M3 - Journal article

C2 - 26856261

VL - 7

JO - Nature Communications

JF - Nature Communications

SN - 2041-1723

M1 - 10507

ER -