DOI: 10.1126/science.1094786. Complete Genome Sequence of the Apicomplexan, <i>Cryptosporidium parvum</i>

Complete Genome Sequence of the Apicomplexan, Cryptosporidium parvum

10.1126/science.1094786

Crossref journal-article

American Association for the Advancement of Science (AAAS)

Science (221)

Abstract

The apicomplexan Cryptosporidium parvum is an intestinal parasite that affects healthy humans and animals, and causes an unrelenting infection in immunocompromised individuals such as AIDS patients. We report the complete genome sequence of C. parvum , type II isolate. Genome analysis identifies extremely streamlined metabolic pathways and a reliance on the host for nutrients. In contrast to Plasmodium and Toxoplasma , the parasite lacks an apicoplast and its genome, and possesses a degenerate mitochondrion that has lost its genome. Several novel classes of cell-surface and secreted proteins with a potential role in host interactions and pathogenesis were also detected. Elucidation of the core metabolism, including enzymes with high similarities to bacterial and plant counterparts, opens new avenues for drug development.

Bibliography

Abrahamsen, M. S., Templeton, T. J., Enomoto, S., Abrahante, J. E., Zhu, G., Lancto, C. A., Deng, M., Liu, C., Widmer, G., Tzipori, S., Buck, G. A., Xu, P., Bankier, A. T., Dear, P. H., Konfortov, B. A., Spriggs, H. F., Iyer, L., Anantharaman, V., Aravind, L., & Kapur, V. (2004). Complete Genome Sequence of the Apicomplexan, Cryptosporidium parvum. Science, 304(5669), 441â445.

Authors 20

Mitchell S. Abrahamsen (first)
Thomas J. Templeton (additional)
Shinichiro Enomoto (additional)
Juan E. Abrahante (additional)
Guan Zhu (additional)
Cheryl A. Lancto (additional)
Mingqi Deng (additional)
Chang Liu (additional)
Giovanni Widmer (additional)
Saul Tzipori (additional)
Gregory A. Buck (additional)
Ping Xu (additional)
Alan T. Bankier (additional)
Paul H. Dear (additional)
Bernard A. Konfortov (additional)
Helen F. Spriggs (additional)
Lakshminarayan Iyer (additional)
Vivek Anantharaman (additional)
L. Aravind (additional)
Vivek Kapur (additional)

References 29 Referenced 818

10.1128/aem.56.5.1423-1428.1990
See supporting data on Science Online.
10.1038/nature01097
A. T. Bankieret al., Genome Res.13, 1787 (2003). (10.1101/gr.1555203) / Genome Res. (2003)
10.1016/0097-8485(94)85023-2
10.1016/j.gene.2003.08.008
10.1099/00221287-146-2-315
10.1016/0166-6851(93)90144-M
10.1016/S0166-6851(99)00183-8
10.1016/S0378-1119(02)00931-9
10.1126/science.1078599
10.1093/oxfordjournals.molbev.a003853
10.1016/0166-6851(93)00020-A
10.1128/jb.179.11.3736-3745.1997
10.1073/pnas.092525699
10.1006/expr.1998.4263
10.1016/S1097-2765(05)00077-8
10.1016/S0166-6851(98)00119-4
10.1128/IAI.68.9.5167-5175.2000
10.1016/S0166-6851(99)00081-X
10.1128/IAI.72.2.980-987.2004
10.1016/S0169-4758(99)01474-X
10.1016/S0925-4439(02)00086-8
10.1017/S0031182097001121
10.1073/pnas.92.16.7148
10.1038/nature724
10.1002/cfg.86
10.1038/35106579
All DNA sequencing was completed at the Advance Genetics Analysis Center University of Minnesota. We thank S. Henning S. Bertolino T. Rowan and H.-W. Chen for their technical assistance and M. Gottlieb (National Institute of Allergy and Infectious Diseases) for his continual support and encouragement. Supported by NIH grant U01 AI 46397 (M.S.A.).

Dates

Type	When
Created	21 years, 5 months ago (March 29, 2004, 8:15 p.m.)
Deposited	1 year, 7 months ago (Jan. 9, 2024, 10:40 p.m.)
Indexed	1 day, 11 hours ago (Sept. 3, 2025, 6:14 a.m.)
Issued	21 years, 4 months ago (April 16, 2004)
Published	21 years, 4 months ago (April 16, 2004)
Published Print	21 years, 4 months ago (April 16, 2004)

Funders 0

None

BibTeX

@article{Abrahamsen_2004, title={Complete Genome Sequence of the Apicomplexan, Cryptosporidium parvum}, volume={304}, ISSN={1095-9203}, url={http://dx.doi.org/10.1126/science.1094786}, DOI={10.1126/science.1094786}, number={5669}, journal={Science}, publisher={American Association for the Advancement of Science (AAAS)}, author={Abrahamsen, Mitchell S. and Templeton, Thomas J. and Enomoto, Shinichiro and Abrahante, Juan E. and Zhu, Guan and Lancto, Cheryl A. and Deng, Mingqi and Liu, Chang and Widmer, Giovanni and Tzipori, Saul and Buck, Gregory A. and Xu, Ping and Bankier, Alan T. and Dear, Paul H. and Konfortov, Bernard A. and Spriggs, Helen F. and Iyer, Lakshminarayan and Anantharaman, Vivek and Aravind, L. and Kapur, Vivek}, year={2004}, month=apr, pages={441–445} }

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