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The Genome Sequence of the Malaria Mosquito Anopheles gambiae

Robert A. Holt, G. Mani Subramanian, Aaron Halpern, Granger G. Sutton, Rosane Charlab, Deborah R. Nusskern, Patrick Wincker, Andrew G. Clark, JoséM. C. Ribeiro, Ron Wides, Steven L. Salzberg, Brendan Loftus, Mark Yandell, William H. Majoros, Douglas B. Rusch, Zhongwu Lai, Cheryl L. Kraft, Josep F. Abril, Veronique Anthouard, Peter Arensburger, Peter W. Atkinson, Holly Baden, Veronique de Berardinis, Danita Baldwin, Vladimir Benes, Jim Biedler, Claudia Blass, Randall Bolanos, Didier Boscus, Mary Barnstead, Shuang Cai, Angela Center, Kabir Chatuverdi, George K. Christophides, Mathew A. Chrystal, Michele Clamp, Anibal Cravchik, Val Curwen, Ali Dana, Art Delcher, Ian Dew, Cheryl A. Evans, Michael Flanigan, Anne Grundschober-Freimoser, Lisa Friedli, Zhiping Gu, Ping Guan, Roderic Guigo, Maureen E. Hillenmeyer, Susanne L. Hladun, James R. Hogan, Young S. Hong, Jeffrey Hoover, Olivier Jaillon, Zhaoxi Ke, Chinnappa Kodira, Elena Kokoza, Anastasios Koutsos, Ivica Letunic, Alex Levitsky, Yong Liang, Jhy-Jhu Lin, Neil F. Lobo, John R. Lopez, Joel A. Malek, Tina C. McIntosh, Stephan Meister, Jason Miller, Clark Mobarry, Emmanuel Mongin, Sean D. Murphy, David A. O'Brochta, Cynthia Pfannkoch, Rong Qi, Megan A. Regier, Karin Remington, Hongguang Shao, Maria V. Sharakhova, Cynthia D. Sitter, Jyoti Shetty, Thomas J. Smith, Renee Strong, Jingtao Sun, Dana Thomasova, Lucas Q. Ton, Pantelis Topalis, Zhijian Tu, Maria F. Unger, Brian Walenz, Aihui Wang, Jian Wang, Mei Wang, Xuelan Wang, Kerry J. Woodford, Jennifer R. Wortman, Martin Wu, Alison Yao, Evgeny M. Zdobnov, Hongyu Zhang, Qi Zhao, Shaying Zhao, Shiaoping C. Zhu, Igor Zhimulev, Mario Coluzzi, Alessandra della Torre, Charles W. Roth, Christos Louis, Francis Kalush, Richard J. Mural, Eugene W. Myers, Mark D. Adams, Hamilton O. Smith, Samuel Broder, Malcolm J. Gardner, Claire M. Fraser, Ewan Birney, Peer Bork, Paul T. Brey, J. Craig Venter, Jean Weissenbach, Fotis C. Kafatos, Frank H. Collins, and Stephen L. Hoffman
Science4 Oct 2002Vol 298, Issue 5591pp. 129-149DOI: 10.1126/science.1076181

Abstract

Anopheles gambiae is the principal vector of malaria, a disease that afflicts more than 500 million people and causes more than 1 million deaths each year. Tenfold shotgun sequence coverage was obtained from the PEST strain of A. gambiae and assembled into scaffolds that span 278 million base pairs. A total of 91% of the genome was organized in 303 scaffolds; the largest scaffold was 23.1 million base pairs. There was substantial genetic variation within this strain, and the apparent existence of two haplotypes of approximately equal frequency (“dual haplotypes”) in a substantial fraction of the genome likely reflects the outbred nature of the PEST strain. The sequence produced a conservative inference of more than 400,000 single-nucleotide polymorphisms that showed a markedly bimodal density distribution. Analysis of the genome sequence revealed strong evidence for about 14,000 protein-encoding transcripts. Prominent expansions in specific families of proteins likely involved in cell adhesion and immunity were noted. An expressed sequence tag analysis of genes regulated by blood feeding provided insights into the physiological adaptations of a hematophagous insect.

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Supported in part by NIH grant U01AI50687 (R.A.H.) and grants U01AI48846 and R01AI44273 (F.H.C.) on behalf of the Anopheles gambiae Genome Consortium, and by the French Ministry of Research. We thank K. Aultman (NIAID) for her insights and effective coordination, D. Lilley (Celera) for competent financial and administrative management, and all members of the sequencing and support teams at the sequencing centers Celera, Genoscope, and TIGR.
Supporting Online Material
Materials and Methods
Figs. S1 to S3
Tables S1 to S5

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Information

Published In

Science
Volume 298 | Issue 5591
4 October 2002

Submission history

Received: 15 July 2002
Accepted: 6 September 2002
Published in print: 4 October 2002

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Authors

Affiliations

Robert A. Holt*,
Celera Genomics, 45 West Gude Drive, Rockville, MD 20850, USA.
G. Mani Subramanian
Celera Genomics, 45 West Gude Drive, Rockville, MD 20850, USA.
Aaron Halpern
Celera Genomics, 45 West Gude Drive, Rockville, MD 20850, USA.
Granger G. Sutton
Celera Genomics, 45 West Gude Drive, Rockville, MD 20850, USA.
Rosane Charlab
Celera Genomics, 45 West Gude Drive, Rockville, MD 20850, USA.
Deborah R. Nusskern
Celera Genomics, 45 West Gude Drive, Rockville, MD 20850, USA.
Patrick Wincker
Genoscope/Centre National de Sequencage and CNRS-UMR 8030, 2 rue Gaston Cremieux, 91057 Evry Cedex 06, France.
Andrew G. Clark
Molecular Biology and Genetics, Cornell University, Ithaca, NY 14853, USA.
JoséM. C. Ribeiro
Laboratory of Malaria and Vector Research, National Institute of Allergy and Infectious Diseases (NIAID), Building 4, Room 126, 4 Center Drive, MSC-0425, Bethesda, MD 20892, USA.
Ron Wides
Faculty of Life Sciences, Bar-Ilan University, Ramat-Gan, Israel.
Steven L. Salzberg
The Institute for Genomic Research (TIGR), 9712 Medical Center Drive, Rockville, MD 20850, USA.
Brendan Loftus
The Institute for Genomic Research (TIGR), 9712 Medical Center Drive, Rockville, MD 20850, USA.
Mark Yandell
Celera Genomics, 45 West Gude Drive, Rockville, MD 20850, USA.
William H. Majoros
Celera Genomics, 45 West Gude Drive, Rockville, MD 20850, USA.
The Institute for Genomic Research (TIGR), 9712 Medical Center Drive, Rockville, MD 20850, USA.
Douglas B. Rusch
Celera Genomics, 45 West Gude Drive, Rockville, MD 20850, USA.
Zhongwu Lai
Celera Genomics, 45 West Gude Drive, Rockville, MD 20850, USA.
Cheryl L. Kraft
Celera Genomics, 45 West Gude Drive, Rockville, MD 20850, USA.
Josep F. Abril
Grup de Recerca en Informatica Biomedica, IMIM/UPF/CRG, Barcelona, Catalonia, Spain.
Veronique Anthouard
Genoscope/Centre National de Sequencage and CNRS-UMR 8030, 2 rue Gaston Cremieux, 91057 Evry Cedex 06, France.
Peter Arensburger
Department of Entomology, University of California, Riverside, CA 92521, USA.
Peter W. Atkinson
Department of Entomology, University of California, Riverside, CA 92521, USA.
Holly Baden
Celera Genomics, 45 West Gude Drive, Rockville, MD 20850, USA.
Veronique de Berardinis
Genoscope/Centre National de Sequencage and CNRS-UMR 8030, 2 rue Gaston Cremieux, 91057 Evry Cedex 06, France.
Danita Baldwin
Celera Genomics, 45 West Gude Drive, Rockville, MD 20850, USA.
Vladimir Benes
European Molecular Biology Laboratory, Meyerhofstr. 1, 69117 Heidelberg, Germany.
Jim Biedler
Virginia Polytechnic Institute and State University, Blacksburg, VA 24061, USA.
Claudia Blass
European Molecular Biology Laboratory, Meyerhofstr. 1, 69117 Heidelberg, Germany.
Randall Bolanos
Celera Genomics, 45 West Gude Drive, Rockville, MD 20850, USA.
Didier Boscus
Genoscope/Centre National de Sequencage and CNRS-UMR 8030, 2 rue Gaston Cremieux, 91057 Evry Cedex 06, France.
Mary Barnstead
Celera Genomics, 45 West Gude Drive, Rockville, MD 20850, USA.
Shuang Cai
Celera Genomics, 45 West Gude Drive, Rockville, MD 20850, USA.
Angela Center
Celera Genomics, 45 West Gude Drive, Rockville, MD 20850, USA.
Kabir Chatuverdi
Celera Genomics, 45 West Gude Drive, Rockville, MD 20850, USA.
George K. Christophides
European Molecular Biology Laboratory, Meyerhofstr. 1, 69117 Heidelberg, Germany.
Mathew A. Chrystal
Center for Tropical Disease Research and Training, University of Notre Dame, Galvin Life Sciences Building, Notre Dame, IN 46556, USA.
Michele Clamp
Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SA, UK.
Anibal Cravchik
Celera Genomics, 45 West Gude Drive, Rockville, MD 20850, USA.
Val Curwen
Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SA, UK.
Ali Dana
Center for Tropical Disease Research and Training, University of Notre Dame, Galvin Life Sciences Building, Notre Dame, IN 46556, USA.
Art Delcher
Celera Genomics, 45 West Gude Drive, Rockville, MD 20850, USA.
Ian Dew
Celera Genomics, 45 West Gude Drive, Rockville, MD 20850, USA.
Cheryl A. Evans
Celera Genomics, 45 West Gude Drive, Rockville, MD 20850, USA.
Michael Flanigan
Celera Genomics, 45 West Gude Drive, Rockville, MD 20850, USA.
Anne Grundschober-Freimoser
Center for Agricultural Biotechnology, University of Maryland Biotechnology Institute, College Park, MD 20742, USA.
Lisa Friedli
Department of Entomology, University of California, Riverside, CA 92521, USA.
Zhiping Gu
Celera Genomics, 45 West Gude Drive, Rockville, MD 20850, USA.
Ping Guan
Celera Genomics, 45 West Gude Drive, Rockville, MD 20850, USA.
Roderic Guigo
Grup de Recerca en Informatica Biomedica, IMIM/UPF/CRG, Barcelona, Catalonia, Spain.
Maureen E. Hillenmeyer
Center for Tropical Disease Research and Training, University of Notre Dame, Galvin Life Sciences Building, Notre Dame, IN 46556, USA.
Susanne L. Hladun
Celera Genomics, 45 West Gude Drive, Rockville, MD 20850, USA.
James R. Hogan
Center for Tropical Disease Research and Training, University of Notre Dame, Galvin Life Sciences Building, Notre Dame, IN 46556, USA.
Young S. Hong
Center for Tropical Disease Research and Training, University of Notre Dame, Galvin Life Sciences Building, Notre Dame, IN 46556, USA.
Jeffrey Hoover
Celera Genomics, 45 West Gude Drive, Rockville, MD 20850, USA.
Olivier Jaillon
Genoscope/Centre National de Sequencage and CNRS-UMR 8030, 2 rue Gaston Cremieux, 91057 Evry Cedex 06, France.
Zhaoxi Ke
Celera Genomics, 45 West Gude Drive, Rockville, MD 20850, USA.
Center for Tropical Disease Research and Training, University of Notre Dame, Galvin Life Sciences Building, Notre Dame, IN 46556, USA.
Chinnappa Kodira
Celera Genomics, 45 West Gude Drive, Rockville, MD 20850, USA.
Elena Kokoza
Institute of Cytology and Genetics, Lavrentyeva ave 10, Novosibirsk 630090, Russia.
Anastasios Koutsos
Institute of Molecular Biology and Biotechnology of the Foundation of Research and Technology–Hellas (IMBB-FORTH), Post Office Box 1527, GR-711 10 Heraklion, Crete, Greece, and University of Crete, GR-711 10 Heraklion, Crete, Greece.
Department of Biology, University of Crete, GR-711 10 Heraklion, Crete, Greece.
Ivica Letunic
European Molecular Biology Laboratory, Meyerhofstr. 1, 69117 Heidelberg, Germany.
Alex Levitsky
Celera Genomics, 45 West Gude Drive, Rockville, MD 20850, USA.
Yong Liang
Celera Genomics, 45 West Gude Drive, Rockville, MD 20850, USA.
Jhy-Jhu Lin
Celera Genomics, 45 West Gude Drive, Rockville, MD 20850, USA.
The Institute for Genomic Research (TIGR), 9712 Medical Center Drive, Rockville, MD 20850, USA.
Neil F. Lobo
Center for Tropical Disease Research and Training, University of Notre Dame, Galvin Life Sciences Building, Notre Dame, IN 46556, USA.
John R. Lopez
Celera Genomics, 45 West Gude Drive, Rockville, MD 20850, USA.
Joel A. Malek
The Institute for Genomic Research (TIGR), 9712 Medical Center Drive, Rockville, MD 20850, USA.
Tina C. McIntosh
Celera Genomics, 45 West Gude Drive, Rockville, MD 20850, USA.
Stephan Meister
European Molecular Biology Laboratory, Meyerhofstr. 1, 69117 Heidelberg, Germany.
Jason Miller
Celera Genomics, 45 West Gude Drive, Rockville, MD 20850, USA.
Clark Mobarry
Celera Genomics, 45 West Gude Drive, Rockville, MD 20850, USA.
Emmanuel Mongin
European Bioinformatics Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SD, UK.
Sean D. Murphy
Celera Genomics, 45 West Gude Drive, Rockville, MD 20850, USA.
David A. O'Brochta
Center for Agricultural Biotechnology, University of Maryland Biotechnology Institute, College Park, MD 20742, USA.
Cynthia Pfannkoch
Celera Genomics, 45 West Gude Drive, Rockville, MD 20850, USA.
Rong Qi
Celera Genomics, 45 West Gude Drive, Rockville, MD 20850, USA.
Megan A. Regier
Celera Genomics, 45 West Gude Drive, Rockville, MD 20850, USA.
Karin Remington
Celera Genomics, 45 West Gude Drive, Rockville, MD 20850, USA.
Hongguang Shao
Virginia Polytechnic Institute and State University, Blacksburg, VA 24061, USA.
Maria V. Sharakhova
Center for Tropical Disease Research and Training, University of Notre Dame, Galvin Life Sciences Building, Notre Dame, IN 46556, USA.
Cynthia D. Sitter
Celera Genomics, 45 West Gude Drive, Rockville, MD 20850, USA.
Jyoti Shetty
The Institute for Genomic Research (TIGR), 9712 Medical Center Drive, Rockville, MD 20850, USA.
Thomas J. Smith
Celera Genomics, 45 West Gude Drive, Rockville, MD 20850, USA.
Renee Strong
Celera Genomics, 45 West Gude Drive, Rockville, MD 20850, USA.
Jingtao Sun
Celera Genomics, 45 West Gude Drive, Rockville, MD 20850, USA.
Dana Thomasova
European Molecular Biology Laboratory, Meyerhofstr. 1, 69117 Heidelberg, Germany.
Lucas Q. Ton
Center for Tropical Disease Research and Training, University of Notre Dame, Galvin Life Sciences Building, Notre Dame, IN 46556, USA.
Pantelis Topalis
Institute of Molecular Biology and Biotechnology of the Foundation of Research and Technology–Hellas (IMBB-FORTH), Post Office Box 1527, GR-711 10 Heraklion, Crete, Greece, and University of Crete, GR-711 10 Heraklion, Crete, Greece.
Zhijian Tu
Virginia Polytechnic Institute and State University, Blacksburg, VA 24061, USA.
Maria F. Unger
Center for Tropical Disease Research and Training, University of Notre Dame, Galvin Life Sciences Building, Notre Dame, IN 46556, USA.
Brian Walenz
Celera Genomics, 45 West Gude Drive, Rockville, MD 20850, USA.
Aihui Wang
Celera Genomics, 45 West Gude Drive, Rockville, MD 20850, USA.
Jian Wang
Celera Genomics, 45 West Gude Drive, Rockville, MD 20850, USA.
Mei Wang
Celera Genomics, 45 West Gude Drive, Rockville, MD 20850, USA.
Xuelan Wang§
Center for Tropical Disease Research and Training, University of Notre Dame, Galvin Life Sciences Building, Notre Dame, IN 46556, USA.
Kerry J. Woodford
Celera Genomics, 45 West Gude Drive, Rockville, MD 20850, USA.
Jennifer R. Wortman
Celera Genomics, 45 West Gude Drive, Rockville, MD 20850, USA.
The Institute for Genomic Research (TIGR), 9712 Medical Center Drive, Rockville, MD 20850, USA.
Martin Wu
The Institute for Genomic Research (TIGR), 9712 Medical Center Drive, Rockville, MD 20850, USA.
Alison Yao
Celera Genomics, 45 West Gude Drive, Rockville, MD 20850, USA.
Evgeny M. Zdobnov
European Molecular Biology Laboratory, Meyerhofstr. 1, 69117 Heidelberg, Germany.
Hongyu Zhang
Celera Genomics, 45 West Gude Drive, Rockville, MD 20850, USA.
Qi Zhao
Celera Genomics, 45 West Gude Drive, Rockville, MD 20850, USA.
Shaying Zhao
The Institute for Genomic Research (TIGR), 9712 Medical Center Drive, Rockville, MD 20850, USA.
Shiaoping C. Zhu
Celera Genomics, 45 West Gude Drive, Rockville, MD 20850, USA.
Igor Zhimulev
Institute of Cytology and Genetics, Lavrentyeva ave 10, Novosibirsk 630090, Russia.
Mario Coluzzi
Dipartimento di Scienze di Sanità Pubblica, Sezione di Parassitologia, Universitàdegli Studi di Roma “La Sapienza,” P.le Aldo Moro 5, 00185 Roma, Italy.
Alessandra della Torre
Dipartimento di Scienze di Sanità Pubblica, Sezione di Parassitologia, Universitàdegli Studi di Roma “La Sapienza,” P.le Aldo Moro 5, 00185 Roma, Italy.
Charles W. Roth
Unité de Biochimie et Biologie Moléculaire des Insectes, Institut Pasteur, Paris 75724 Cedex 15, France.
Christos Louis
Institute of Molecular Biology and Biotechnology of the Foundation of Research and Technology–Hellas (IMBB-FORTH), Post Office Box 1527, GR-711 10 Heraklion, Crete, Greece, and University of Crete, GR-711 10 Heraklion, Crete, Greece.
Department of Biology, University of Crete, GR-711 10 Heraklion, Crete, Greece.
Francis Kalush
Celera Genomics, 45 West Gude Drive, Rockville, MD 20850, USA.
Richard J. Mural
Celera Genomics, 45 West Gude Drive, Rockville, MD 20850, USA.
Eugene W. Myers
Celera Genomics, 45 West Gude Drive, Rockville, MD 20850, USA.
Mark D. Adams
Celera Genomics, 45 West Gude Drive, Rockville, MD 20850, USA.
Hamilton O. Smith
Celera Genomics, 45 West Gude Drive, Rockville, MD 20850, USA.
Samuel Broder
Celera Genomics, 45 West Gude Drive, Rockville, MD 20850, USA.
Malcolm J. Gardner
The Institute for Genomic Research (TIGR), 9712 Medical Center Drive, Rockville, MD 20850, USA.
Claire M. Fraser
The Institute for Genomic Research (TIGR), 9712 Medical Center Drive, Rockville, MD 20850, USA.
Ewan Birney
European Bioinformatics Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SD, UK.
Peer Bork
European Molecular Biology Laboratory, Meyerhofstr. 1, 69117 Heidelberg, Germany.
Paul T. Brey
Unité de Biochimie et Biologie Moléculaire des Insectes, Institut Pasteur, Paris 75724 Cedex 15, France.
J. Craig Venter
Celera Genomics, 45 West Gude Drive, Rockville, MD 20850, USA.
The Institute for Genomic Research (TIGR), 9712 Medical Center Drive, Rockville, MD 20850, USA.
Jean Weissenbach
Genoscope/Centre National de Sequencage and CNRS-UMR 8030, 2 rue Gaston Cremieux, 91057 Evry Cedex 06, France.
Fotis C. Kafatos
European Molecular Biology Laboratory, Meyerhofstr. 1, 69117 Heidelberg, Germany.
Frank H. Collins
Center for Tropical Disease Research and Training, University of Notre Dame, Galvin Life Sciences Building, Notre Dame, IN 46556, USA.
Stephen L. Hoffman||
Celera Genomics, 45 West Gude Drive, Rockville, MD 20850, USA.

Notes

*
Present address: Canada's Michael Smith Genome Science Centre, British Columbia Cancer Agency, Room 3427, 600 West 10th Avenue, Vancouver, British Columbia V5Z 4E6, Canada.
Present address: Agencourt Bioscience Corporation, 100 Cummings Center, Suite 107J, Beverly, MA 01915, USA.
§
Present address: Department of Pharmacology, Sun Yat-Sen Medical School, Sun Yat-Sen University #74, Zhongshan 2nd Road, Guangzhou (Canton), 510089, P. R. China.
||
Present address: Sanaria, 308 Argosy Drive, Gaithersburg, MD 20878, USA.
To whom correspondence should be addressed. E-mail: [email protected], [email protected] (R.A.H.), [email protected] (F.H.C.).

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