1887

Abstract

Surprisingly, unlike most Apicomplexa, appears to lack a plastid genome. Primers based upon the highly conserved plastid small- or large-subunit rRNA (SSU/LSU rRNA) and the -tRNA genes of other members of the phylum Apicomplexa failed to amplify products from intracellular stages of , whereas products were obtained from the plastid-containing apicomplexans and , as well as the plants and . Dot-blot hybridization of sporozoite genomic DNA (gDNA) supported these PCR results. A plastid-specific set of probes containing SSU/LSU rRNA and -tRNA genes strongly hybridized to gDNA from a diverse group of plastid-containing organisms including three Apicomplexa, two plants, and , but not to those without this organelle including , three kinetoplastids, the yeast , mammals and the eubacterium . Since the origin of the plastid in other apicomplexans is postulated to be the result of a secondary symbiogenesis of either a red or a green alga, the most parsimonious explanation for its absence in is that it has been secondarily lost. If confirmed, this would indicate an alternative evolutionary fate for this organelle in one member of the Apicomplexa. It also suggests that unlike the situation with other diseases caused by members of the Apicomplexa, drug development against cryptosporidiosis targeting a plastid genome or metabolic pathways associated with it may not be useful.

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2000-02-01
2021-10-24
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References

  1. Barta J. R., Martin D. S., Liberator P. A.9 other authors 1997; Phylogenetic relationships among eight Eimeria species infecting domestic fowl inferred using complete small subunit ribosomal DNA sequences. J Parasitol 83:262–271 [CrossRef]
    [Google Scholar]
  2. Beckers C. J., Roos D. S., Donald R. G., Luft B. J., Schwab J. C., Cao Y., Joiner K. A. 1995; Inhibition of cytoplasmic and organellar protein synthesis in Toxoplasma gondii. Implications for the target of macrolide antibiotics. J Clin Invest 95:367–376 [CrossRef]
    [Google Scholar]
  3. Blanchard J., Hicks J. S. 1999; The non-photosynthetic plastid in malarial parasites and other apicomplexans is derived from outside the green plastid lineage. J Eukaryot Microbiol 46:367–375 [CrossRef]
    [Google Scholar]
  4. Blunt D. S., Khramtsov N. V., Upton S. J., Montelone B. A. 1997; Molecular karyotype analysis of Cryptosporidium parvum: evidence for eight chromosomes and a low-molecular-size molecule. Clin Diagn Lab Immunol 4:11–13
    [Google Scholar]
  5. Coombs G. H. 1999; Biochemical pecularities and drug targets in Cryptosporidium parvum: lessons from other coccidian parasites. Parasitol Today 15:333–338 [CrossRef]
    [Google Scholar]
  6. Denny P., Preiser P., Williamson D., Wilson I. 1998; Evidence for a single origin of the 35 kb plastid DNA in apicomplexans. Protist 149:51–59 [CrossRef]
    [Google Scholar]
  7. Dunn P. P., Stephens P. J., Shirley M. W. 1998; Eimeria tenella – two species of extrachromosomal DNA revealed by pulsed-field gel electrophoresis. Parasitol Res 84:272–275 [CrossRef]
    [Google Scholar]
  8. Embley T. M., Hirt R. P. 1998; Early branching eukaryotes?. Curr Opin Genet Dev 8:624–629 [CrossRef]
    [Google Scholar]
  9. Escalante A. A., Ayala F. J. 1995; Evolutionary origin of Plasmodium and other Apicomplexa based on rRNA genes. Proc Natl Acad Sci USA 92:5793–5797 [CrossRef]
    [Google Scholar]
  10. Fayer R., Speer C. A., Dubey J. P. 1997; The General Biology of Cryptosporidium. In Cryptosporidium and Cryptosporidiosis pp. 1–42Edited by Fayer R. Boca Raton, FL: CRC Press;
    [Google Scholar]
  11. Fichera M. E., Roos D. S. 1997; A plastid organelle as a drug target in apicomplexan parasites. Nature 390:407–409 [CrossRef]
    [Google Scholar]
  12. Gajadhar A. A., Marquardt W. C., Hall R., Gunderson J., Ariztia-Carmona E. V., Sogin M. L. 1991; Ribosomal RNA sequences of Sarcocystis muris, Theileria annulata and Crypthecodinium cohnii reveal evolutionary relationships among apicomplexans, dinoflagellates, and ciliates. Mol Biochem Parasitol 45:147–154 [CrossRef]
    [Google Scholar]
  13. Gozar M. M., Bagnara A. S. 1995; An organelle-like small subunit ribosomal RNA gene from Babesia bovis: nucleotide sequence, secondary structure of the transcript and preliminary phylogenetic analysis. Int J Parasitol 25:929–938 [CrossRef]
    [Google Scholar]
  14. Hackstein J. H., Mackenstedt U., Mehlhorn H., Meijerink J. P., Schubert H., Leunissen J. A. 1995; Parasitic apicomplexans harbor a chlorophyll a–D1 complex, the potential target for therapeutic triazines. Parasitol Res 81:207–216
    [Google Scholar]
  15. Hashimoto T., Sanchez L. B., Shirakura T., Muller M., Hasegawa M. 1998; Secondary absence of mitochondria in Giardia lamblia and Trichomonas vaginalis revealed by valyl-tRNA synthetase phylogeny. Proc Natl Acad Sci USA 95:6860–6865 [CrossRef]
    [Google Scholar]
  16. Keithly J. S., Zhu G., Upton S. J., Woods K. M., Martinez M. P., Yarlett N. 1997; Polyamine biosynthesis in Cryptosporidium parvum and its implications for chemotherapy. Mol Biochem Parasitol 88:35–42 [CrossRef]
    [Google Scholar]
  17. Kohler S., Delwiche C. F., Denny P. W., Tilney L. G., Webster P., Wilson R. J., Palmer J. D., Roos D. S. 1997; A plastid of probable green algal origin in Apicomplexan parasites. Science 275:1485–1489 [CrossRef]
    [Google Scholar]
  18. Martin W., Muller M. 1998; The hydrogen hypothesis for the first eukaryote. Nature 392:37–41 [CrossRef]
    [Google Scholar]
  19. Morrison D. A., Ellis J. T. 1997; Effects of nucleotide sequence alignment on phylogeny estimation: a case study of 18S rDNAs of Apicomplexa. Mol Biol Evol 14:428–441 [CrossRef]
    [Google Scholar]
  20. Muller M. 1998; Enzymes and compartmentation of core energy metabolism of anaerobic protists – a special case in eukaryotic evolution. In Evolutionary Relationships among Protozoa pp. 109–127Edited by Coombs G. H., Vickerman K., Sleigh M. A., Warren A. Dordrecht: Kluwer;
    [Google Scholar]
  21. Riordan C. E., Langreth S. G., Sanchez L. B., Kayser O., Keithly J. S. 1999; Preliminary evidence for a mitochondrion in Cryptosporidium parvum: phylogenetic and therapeutic implications. J Eukaryot Microbiol 46:52–55s
    [Google Scholar]
  22. Srivastava I. K., Rottenberg H., Vaidya A. B. 1997; Atovaquone, a broad spectrum antiparasitic drug, collapses mitochondrial membrane potential in a malarial parasite. J Biol Chem 272:3961–3966 [CrossRef]
    [Google Scholar]
  23. Supplick K., Akella R., Saul A., Vaidya A. B. 1988; Molecular cloning and partial sequence of a 5·8 kilobase pair repetitive DNA from Plasmodium falciparum. Mol Biochem Parasitol 30:289–290 [CrossRef]
    [Google Scholar]
  24. Tetley L., Brown S. M. A., McDonald V., Coombs G. H. 1998; Ultrastructural analysis of the sporozoite of Cryptosporium parvum. Microbiology 144:3249–3255 [CrossRef]
    [Google Scholar]
  25. Van de Peer Y., De Wachter R. 1997; Evolutionary relationships among the eukaryotic crown taxa taking into account site-to-site rate variation in 18S rRNA. J Mol Evol 45:619–630 [CrossRef]
    [Google Scholar]
  26. Waller R. F., Keeling P. J., Donald R. G.7 other authors 1998; Nuclear-encoded proteins target to the plastid in Toxoplasma gondii and Plasmodium falciparum. Proc Natl Acad Sci USA 95:12352–12357 [CrossRef]
    [Google Scholar]
  27. Williamson D. H., Gardner M. J., Preiser P., Moore D. J., Rangachari K., Wilson R. J. 1994; The evolutionary origin of the 35 kb circular DNA of Plasmodium falciparum: new evidence supports a possible rhodophyte ancestry. Mol Gen Genet 243:249–252
    [Google Scholar]
  28. Wilson R. J., Williamson D. H. 1997; Extrachromosomal DNA in the Apicomplexa. Microbiol Mol Biol Rev 61:1–16
    [Google Scholar]
  29. Wilson R. J., Denny P. W., Preiser P. R.8 other authors 1996; Complete gene map of the plastid-like DNA of the malaria parasite Plasmodium falciparum. J Mol Biol 261:155–172 [CrossRef]
    [Google Scholar]
  30. Woods K. M., Nesterenko M. V., Upton S. J. 1996; Efficacy of 101 antimicrobials and other agents on the development of Cryptosporidium parvum in vitro. Ann Trop Med Parasitol 90:603–615
    [Google Scholar]
  31. Yap M. W., Kara U. A., ten Heggeler-Bordier B., Ting R. C., Tan T. M. 1997; Partial nucleotide sequence and organisation of extrachromosomal plastid-like DNA in Plasmodium berghei. Gene 200:91–98 [CrossRef]
    [Google Scholar]
  32. Yeo A. E., Rieckmann K. H. 1994; Prolonged exposure of Plasmodium falciparum to ciprofloxacin increases anti-malarial activity. J Parasitol 80:158–160 [CrossRef]
    [Google Scholar]
  33. Zhang Z. D., Green B. R., Cavalier-Smith T. 1999; Single gene circles in dinoflagellate chloroplast genomes. Nature 400:155–159 [CrossRef]
    [Google Scholar]
  34. Zhu G., Keithly J. S. 1997; Molecular analysis of a P-type ATPase from Cryptosporidium parvum. Mol Biochem Parasitol 90:307–316 [CrossRef]
    [Google Scholar]
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