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. 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 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

Entomology

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

232 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 (US)
Article number	10507
Journal	Nature communications
Volume	7
DOIs	https://doi.org/10.1038/ncomms10507
State	Published - Feb 9 2016

All Science Journal Classification (ASJC) codes

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

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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, [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 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.

@article{cf5e186cc27148a5be392e554273b0cf,

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.}",

note = "Funding Information: Wikel strain was sequenced in a joint effort by the Broad Institute and the JCVI and funded by the National Institute of Allergy and Infectious Diseases, National Institutes of Health. The I. scapularis Wikel strain (Quinnipiac University, Hamden, CT) genome was sequenced to approximately 3.8-fold coverage using Sanger sequencing and assembled using the Celera Assembler configured to accommodate high repeat content within the genome and heterozygosity in the donor population (Supplementary Table 1). The assembly and raw reads are available at GenBank under the project accession ABJB010000000, consisting of contig accessions ABJB010000001-ABJB011141594 and VectorBase as IscaW1, 3 May 2012. The annotation of the I. scapularis genome was performed via a joint effort between the JCVI and VectorBase. The genome annotation release (IscaW1.4) is available at VectorBase (https://www.vectorbase.org/) and GenBank (accession ID: ABJB010000000). Forty-five bacterial artificial chromosome clones, B183,834 ESTs and 45 microRNAs were also sequenced and annotated (Supplementary Figs 4–6 and Supplementary Tables 4–6). Funding Information: This project has been funded in part with federal funds from the National Institute of Allergy and Infectious Diseases, National Institutes of Health, Department of Health and Human Services (NIAID, NIH, DHHS) under contract numbers N01-AI30071, HHSN272200900007C, HHSN266200400001C and 5R01GM77117-5. Its contents are solely the responsibility of the authors and do not represent the official views of the NIH. Additional grants and contracts supporting work described in this manuscript were from the NIH-NIAID (HHSN266200400039C and HHSN272200900039C) to F.H.C., and a subcontract under HHSN272200900039C to C.A.H. and J.M.M., the Australian Research Council Discovery Project (DP120100240) to S.C.B. and R.S., the Ministerio de Ciencia e Innovaci{\'o}n of Spain (BFU2007–6292; BFU2010–15484) to J.R., BIO2009–07990 and BIO2012–37926 to J.V. NIH-1R01AI090062 to Y.P., L.S., and J.K., NIH 1R21AI096268 and NSF IOS-0949194 to R.M.R., the Xunta de Galicia of Spain (10PXIB918057PR) to J.M.C.T. and M.T., BFU2011–23896 and EU FP7 ANTIGONE (278976) to J.F., the USDA-NRI/CREES (2008-35302-18820) and Texas AgriLife Research Vector Biology grant to P.V.P. and European Research Council Starting Independent Researcher Grant (205202) to R.B., J.M.R was supported by the intramural program of the NIAID, R.M.W. by a Marie Curie International Outgoing Fellowship PIOF-GA-2011–303312, E.M.Z. by Swiss National Science Foundation awards 31003A-125350 and 31003A-143936, J.M.G. by an NIH-NCATS award TL1 TR000162 and NSF Graduate Research Fellowship (DGE 1333468), V.C. by a Boehringer Ingelheim Ph.D. Fellowship, F.G.V. by a Fundac¸{\~a}o para a Ci{\^e}ncia e a Tecnologia, Portugal fellowship (SFRH/BD/22360/2005), C.J.P.G. and F.H. by The Lundbeck Foundation (Denmark), and J.J.G. by NIH awards HHSN272200900040C, R01AI017828 and R01AI043006. Support from the Broad Genomics Platform is gratefully acknowledged. Publisher Copyright: {\textcopyright} 2016, Nature Publishing Group. All rights reserved. Copyright: Copyright 2018 Elsevier B.V., All rights reserved.",

year = "2016",

month = feb,

day = "9",

doi = "10.1038/ncomms10507",

language = "English (US)",

volume = "7",

journal = "Nature Communications",

issn = "2041-1723",

publisher = "Nature Publishing Group",

}

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

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 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, 09.02.2016.

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

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.

N1 - Funding Information: Wikel strain was sequenced in a joint effort by the Broad Institute and the JCVI and funded by the National Institute of Allergy and Infectious Diseases, National Institutes of Health. The I. scapularis Wikel strain (Quinnipiac University, Hamden, CT) genome was sequenced to approximately 3.8-fold coverage using Sanger sequencing and assembled using the Celera Assembler configured to accommodate high repeat content within the genome and heterozygosity in the donor population (Supplementary Table 1). The assembly and raw reads are available at GenBank under the project accession ABJB010000000, consisting of contig accessions ABJB010000001-ABJB011141594 and VectorBase as IscaW1, 3 May 2012. The annotation of the I. scapularis genome was performed via a joint effort between the JCVI and VectorBase. The genome annotation release (IscaW1.4) is available at VectorBase (https://www.vectorbase.org/) and GenBank (accession ID: ABJB010000000). Forty-five bacterial artificial chromosome clones, B183,834 ESTs and 45 microRNAs were also sequenced and annotated (Supplementary Figs 4–6 and Supplementary Tables 4–6). Funding Information: This project has been funded in part with federal funds from the National Institute of Allergy and Infectious Diseases, National Institutes of Health, Department of Health and Human Services (NIAID, NIH, DHHS) under contract numbers N01-AI30071, HHSN272200900007C, HHSN266200400001C and 5R01GM77117-5. Its contents are solely the responsibility of the authors and do not represent the official views of the NIH. Additional grants and contracts supporting work described in this manuscript were from the NIH-NIAID (HHSN266200400039C and HHSN272200900039C) to F.H.C., and a subcontract under HHSN272200900039C to C.A.H. and J.M.M., the Australian Research Council Discovery Project (DP120100240) to S.C.B. and R.S., the Ministerio de Ciencia e Innovación of Spain (BFU2007–6292; BFU2010–15484) to J.R., BIO2009–07990 and BIO2012–37926 to J.V. NIH-1R01AI090062 to Y.P., L.S., and J.K., NIH 1R21AI096268 and NSF IOS-0949194 to R.M.R., the Xunta de Galicia of Spain (10PXIB918057PR) to J.M.C.T. and M.T., BFU2011–23896 and EU FP7 ANTIGONE (278976) to J.F., the USDA-NRI/CREES (2008-35302-18820) and Texas AgriLife Research Vector Biology grant to P.V.P. and European Research Council Starting Independent Researcher Grant (205202) to R.B., J.M.R was supported by the intramural program of the NIAID, R.M.W. by a Marie Curie International Outgoing Fellowship PIOF-GA-2011–303312, E.M.Z. by Swiss National Science Foundation awards 31003A-125350 and 31003A-143936, J.M.G. by an NIH-NCATS award TL1 TR000162 and NSF Graduate Research Fellowship (DGE 1333468), V.C. by a Boehringer Ingelheim Ph.D. Fellowship, F.G.V. by a Fundac¸ão para a Ciência e a Tecnologia, Portugal fellowship (SFRH/BD/22360/2005), C.J.P.G. and F.H. by The Lundbeck Foundation (Denmark), and J.J.G. by NIH awards HHSN272200900040C, R01AI017828 and R01AI043006. Support from the Broad Genomics Platform is gratefully acknowledged. Publisher Copyright: © 2016, Nature Publishing Group. All rights reserved. Copyright: Copyright 2018 Elsevier B.V., All rights reserved.

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.

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U2 - 10.1038/ncomms10507

DO - 10.1038/ncomms10507

M3 - Article

C2 - 26856261

AN - SCOPUS:84957895144

VL - 7

JO - Nature Communications

JF - Nature Communications

SN - 2041-1723

M1 - 10507

ER -