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

Research output: Contribution to journalArticlepeer-review

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

Bibliographical 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 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.

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