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The Genome Sequence of the Malaria of the Most Efficient Malaria Vectors in the World

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The Genome Sequence of the Malaria of the Most Efficient Malaria Vectors in the World R ESEARCH A RTICLES Anopheles gambiae is the major vector of Plasmodium falciparum in Africa and is one The Genome Sequence of the Malaria of the most efficient malaria vectors in the world. Its blood meals come almost exclu- Mosquito Anopheles gambiae sively from humans, its larvae develop in temporary bodies of water produced by hu- 1 1 1 Robert A. Holt, *† G. Mani Subramanian, Aaron Halpern, man activities (e.g., agricultural irrigation or Granger G. Sutton,1 Rosane Charlab,1 Deborah R. Nusskern,1 flooded human or domestic animal foot- Patrick Wincker,2 Andrew G. Clark,3 Jose´M. C. Ribeiro,4 Ron Wides,5 prints), and adults rest primarily in human Steven L. Salzberg,6 Brendan Loftus,6 Mark Yandell,1 William H. Majoros,1,6 dwellings. During the 1950s and early 1960s, Douglas B. Rusch,1 Zhongwu Lai,1 Cheryl L. Kraft,1 Josep F. Abril,7 the World Health Organization ( WHO) ma- laria eradication campaign succeeded in erad- Veronique Anthouard,2 Peter Arensburger,8 Peter W. Atkinson,8 1 2 1 9 icating malaria from Europe and sharply re- Holly Baden, Veronique de Berardinis, Danita Baldwin, Vladimir Benes, duced its prevalence in many other parts of 10 9 1 2 Jim Biedler, Claudia Blass, Randall Bolanos, Didier Boscus, the world, primarily through programs that Mary Barnstead,1 Shuang Cai,1 Angela Center,1 Kabir Chatuverdi,1 combined mosquito control with antimalarial George K. Christophides,9 Mathew A. Chrystal,11 Michele Clamp,12 drugs such as chloroquine. Sub-Saharan Af- Anibal Cravchik,1 Val Curwen,12 Ali Dana,11 Art Delcher,1 Ian Dew,1 Cheryl A. Evans,1 Michael Flanigan,1 Anne Grundschober-Freimoser,13 1Celera Genomics, 45 West Gude Drive, Rockville, MD Lisa Friedli,8 Zhiping Gu,1 Ping Guan,1 Roderic Guigo,7 Maureen E. Hillenmeyer,11 20850, USA. 2Genoscope/Centre National de Sequen- 1 11 11 1 cage and CNRS-UMR 8030, 2 rue Gaston Cremieux, Susanne L. Hladun, James R. Hogan, Young S. Hong, Jeffrey Hoover, 91057 Evry Cedex 06, France. 3Molecular Biology and Olivier Jaillon,2 Zhaoxi Ke,1,11 Chinnappa Kodira,1 Elena Kokoza,14 Genetics, Cornell University, Ithaca, NY 14853, USA. 4 15,16 9 1 1 Laboratory of Malaria and Vector Research, National Anastasios Koutsos, Ivica Letunic, Alex Levitsky, Yong Liang, Institute of Allergy and Infectious Diseases (NIAID), Jhy-Jhu Lin,1,6 Neil F. Lobo,11 John R. Lopez,1 Joel A. Malek,6‡ Tina C. Building 4, Room 126, 4 Center Drive, MSC-0425, 1 9 1 1 Bethesda, MD 20892, USA. 5Faculty of Life Sciences, McIntosh, Stephan Meister, Jason Miller, Clark Mobarry, Bar-Ilan University, Ramat-Gan, Israel. 6The Institute 17 1 13 Emmanuel Mongin, Sean D. Murphy, David A. O’Brochta, for Genomic Research (TIGR), 9712 Medical Center on December 1, 2015 Cynthia Pfannkoch,1 Rong Qi,1 Megan A. Regier,1 Karin Remington,1 Drive, Rockville, MD 20850, USA. 7Grup de Recerca en 10 11 1 Informatica Biomedica, IMIM/UPF/CRG, Barcelona, Hongguang Shao, Maria V. Sharakhova, Cynthia D. Sitter, Catalonia, Spain. 8Department of Entomology, Uni- Jyoti Shetty,6 Thomas J. Smith,1 Renee Strong,1 Jingtao Sun,1 versity of California, Riverside, CA 92521, USA. 9Eu- 9 11 15 10 ropean Molecular Biology Laboratory, Meyerhofstr.1, Dana Thomasova, Lucas Q. Ton, Pantelis Topalis, Zhijian Tu, 69117 Heidelberg, Germany. 10Virginia Polytechnic 11 1 1 1 1 Maria F. Unger, Brian Walenz, Aihui Wang, Jian Wang, Mei Wang, Institute and State University, Blacksburg, VA 24061, Xuelan Wang,11§ Kerry J. Woodford,1 Jennifer R. Wortman,1,6 Martin Wu,6 USA. 11Center for Tropical Disease Research and 1 9 1 1 Training, University of Notre Dame, Galvin Life Sci- Alison Yao, Evgeny M. Zdobnov, Hongyu Zhang, Qi Zhao, ences Building, Notre Dame, IN 46556, USA. 12Well- 6 1 14 18 come Trust Sanger Institute, Wellcome Trust Genome Shaying Zhao, Shiaoping C. Zhu, Igor Zhimulev, Mario Coluzzi, www.sciencemag.org 13 18 19 15,16 Campus, Hinxton, Cambridge CB10 1SA, UK. Center Alessandra della Torre, Charles W. Roth, Christos Louis, for Agricultural Biotechnology, University of Mary- Francis Kalush,1 Richard J. Mural,1 Eugene W. Myers,1 Mark D. Adams,1 land Biotechnology Institute, College Park, MD 20742, 1 1 6 USA. 14Institute of Cytology and Genetics, Lavren- Hamilton O. Smith, Samuel Broder, Malcolm J. Gardner, 15 6 17 9 19 tyeva ave 10, Novosibirsk 630090, Russia. Institute Claire M. Fraser, Ewan Birney, Peer Bork, Paul T. Brey, of Molecular Biology and Biotechnology of the Foun- J. Craig Venter,1,6 Jean Weissenbach,2 Fotis C. Kafatos,9 dation of Research and Technology–Hellas (IMBB- 11 1࿣ FORTH), Post Office Box 1527, GR-711 10 Heraklion, Frank H. Collins, † Stephen L. Hoffman Crete, Greece, and University of Crete, GR-711 10 16 Heraklion, Crete, Greece. Department of Biology, Downloaded from Anopheles gambiae is the principal vector of malaria, a disease that afflicts more University of Crete, GR-711 10 Heraklion, Crete, than 500 million people and causes more than 1 million deaths each year. Tenfold Greece. 17European Bioinformatics Institute, Well- shotgun sequence coverage was obtained from the PEST strain of A. gambiae and come Trust Genome Campus, Hinxton, Cambridge 18 assembled into scaffolds that span 278 million base pairs. A total of 91% of the CB10 1SD, UK. Dipartimento di Scienze di Sanita` Pubblica, Sezione di Parassitologia, Universita`degli genome was organized in 303 scaffolds; the largest scaffold was 23.1 million base Studi di Roma “La Sapienza,” P.le Aldo Moro 5, 00185 pairs. There was substantial genetic variation within this strain, and the apparent Roma, Italy. 19Unite´de Biochimie et Biologie Mole´cu- existence of two haplotypes of approximately equal frequency (“dual haplotypes”) laire des Insectes, Institut Pasteur, Paris 75724 Cedex in a substantial fraction of the genome likely reflects the outbred nature of the PEST 15, France. strain. The sequence produced a conservative inference of more than 400,000 *Present address: Canada’s Michael Smith Genome single-nucleotide polymorphisms that showed a markedly bimodal density distri- Science Centre, British Columbia Cancer Agency, Room 3427, 600 West 10th Avenue, Vancouver, Brit- bution. Analysis of the genome sequence revealed strong evidence for about 14,000 ish Columbia V5Z 4E6, Canada. protein-encoding transcripts. Prominent expansions in specific families of proteins ‡Present address: Agencourt Bioscience Corporation, likely involved in cell adhesion and immunity were noted. An expressed sequence 100 Cummings Center, Suite 107J, Beverly, MA tag analysis of genes regulated by blood feeding provided insights into the phys- 01915, USA. §Present address: Department of Pharmacology, Sun iological adaptations of a hematophagous insect. Yat-Sen Medical School, Sun Yat-Sen University #74, Zhongshan 2nd Road, Guangzhou (Canton), 510089, The mosquito is both an elegant, exquisitely the tropics. Malaria, the most important parasit- P.R.China. adapted organism and a scourge of humanity. ic disease in the world, is thought to be respon- ࿣Present address: Sanaria, 308 Argosy Drive, Gaithers- The principal mosquito-borne human illnesses sible for 500 million cases of illness and up to burg, MD 20878, USA. †To whom correspondence should be addressed.E- of malaria, filariasis, dengue, and yellow fever 2.7 million deaths annually, more than 90% of mail: [email protected], [email protected] (R.A.H.), are at this time almost exclusively restricted to which occur in sub-Saharan Africa (1). [email protected] (F.H.C.). www.sciencemag.org SCIENCE VOL 298 4 OCTOBER 2002 129 T HE M OSQUITO G ENOME: A NOPHELES GAMBIAE rica, for the most part, did not benefit from pink eye mutation that can readily be used as clones spanning them, although small scaf- the malaria eradication program, but the an indicator of cross-colony contamination folds are expected to fit within interscaffold widespread availability of chloroquine and (7). The PEST strain was originally used in gaps. The sequence that is missing in the other affordable antimalarial drugs no doubt the early 1990s to measure the reservoir of intrascaffold gaps is largely composed of (i) helped to control malaria mortality and mor- mosquito-infective Plasmodium gametocytes short regions that lacked coverage because of bidity. Unfortunately, with the appearance of in people from western Kenya. The PEST random sampling, and (ii) repeat sequences chloroquine-resistant malaria parasites and strain was produced by crossing a laboratory that could not be entirely filled using mate the development of resistance of mosquitoes strain originating in Nigeria and containing pairs [sequence reads from each end of a to the insecticides used to control disease the eye mutation with the offspring of field- plasmid insert (16)]. Most intrascaffold gaps transmission, malaria in Africa is again on the collected A. gambiae from the Asembo Bay are spanned by 10-kbp clones that have been rise. Even control programs based on insec- area of western Kenya, and then reselecting archived as frozen glycerol stocks. These ticide-impregnated bed nets, now widely ad- for the pink eye phenotype (8). Outbreeding clones have been submitted to the Malaria vocated by WHO, are threatened by the de- was repeated three times, yielding a colony Research and Reference Reagent Resource velopment of insecticide resistance in A. whose genetic composition is predominantly gambiae and other vectors. New malaria con- derived from the Savanna form of A. gambiae Fig. 1 (foldout). Annotation of the Anopheles trol techniques are urgently needed in sub- found in western Kenya. This colony, when gambiae genome sequence.The genome se- Saharan Africa, and to meet this challenge we tested, was fully susceptible to P. falciparum quence is displayed on a nucleotide scale of must grasp both the ecological and molecular from western Kenya (9).
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