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A photosynthetic alveolate closely related to apicomplexan parasites

A Corrigendum to this article was published on 17 April 2008

Abstract

Many parasitic Apicomplexa, such as Plasmodium falciparum, contain an unpigmented chloroplast remnant termed the apicoplast, which is a target for malaria treatment. However, no close relative of apicomplexans with a functional photosynthetic plastid has yet been described. Here we describe a newly cultured organism that has ultrastructural features typical for alveolates, is phylogenetically related to apicomplexans, and contains a photosynthetic plastid. The plastid is surrounded by four membranes, is pigmented by chlorophyll a, and uses the codon UGA to encode tryptophan in the psbA gene. This genetic feature has been found only in coccidian apicoplasts and various mitochondria. The UGA-Trp codon and phylogenies of plastid and nuclear ribosomal RNA genes indicate that the organism is the closest known photosynthetic relative to apicomplexan parasites and that its plastid shares an origin with the apicoplasts. The discovery of this organism provides a powerful model with which to study the evolution of parasitism in Apicomplexa.

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Figure 1: Ultrastructure of new alveolate Chromera velia.
Figure 2: Nuclear and plastid phylogenies of Chromera velia.
Figure 3: Evolution of Chromera velia , apicomplexans and dinoflagellates.

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References

  1. Adl, S. M. et al. The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. J. Eukaryot. Microbiol. 52, 399–451 (2005)

    Article  Google Scholar 

  2. Scheer, H. in Light-Harvesting Antennas in Photosynthesis Vol. 13 (eds Green, B. R. & Parsons, W. W.) 29–82 (Springer/Kluwer Academic Publishers, Dordrecht, the Netherlands, 2003)

    Book  Google Scholar 

  3. Cavalier-Smith, T. in The Biology of Free-living Heterotrophic Flagellates (eds Patterson, D. J. & Larsen, J.) 113–131 (Oxford Univ. Press, Oxford, 1991)

    Google Scholar 

  4. Leander, B. S. & Keeling, P. J. Morphostasis in alveolate evolution. Trends Ecol. Evol. 18, 395–402 (2003)

    Article  Google Scholar 

  5. Adl, S. M. et al. Diversity, nomenclature, and taxonomy of protists. Syst. Biol. 56, 684–689 (2007)

    Article  Google Scholar 

  6. Ralph, S. A. et al. Tropical infectious diseases: metabolic maps and functions of the Plasmodium falciparum apicoplast. Nature Rev. Microbiol. 2, 203–216 (2004)

    Article  CAS  Google Scholar 

  7. Tenter, A. M., Heckeroth, A. R. & Weiss, L. M. Toxoplasma gondii: from animals to humans. Int. J. Parasitol. 30, 1217–1258 (2000)

    Article  CAS  Google Scholar 

  8. Ralph, S. A., D’Ombrain, M. C. & McFadden, G. I. The apicoplast as an antimalarial drug target. Drug Resist. Updat. 4, 145–151 (2001)

    Article  CAS  Google Scholar 

  9. Toso, M. A. & Omoto, C. K. Gregarina niphandrodes may lack both a plastid genome and organelle. J. Eukaryot. Microbiol. 54, 66–72 (2007)

    Article  CAS  Google Scholar 

  10. Barta, J. R. & Thompson, R. C. A. What is Cryptosporidium? Reappraising its biology and phylogenetic affinities. Trends Parasitol. 22, 463–468 (2006)

    Article  Google Scholar 

  11. Zhu, G., Marchewka, M. J. & Keithly, J. S. Cryptosporidium parvum appears to lack a plastid genome. Microbiology 146, 315–321 (2000)

    Article  CAS  Google Scholar 

  12. Kuvardina, O. N. et al. The phylogeny of colpodellids (Alveolata) using small subunit rRNA gene sequences suggests they are the free-living sister group to apicomplexans. J. Eukaryot. Microbiol. 49, 498–504 (2002)

    Article  CAS  Google Scholar 

  13. Fast, N. M., Kissinger, J. C., Roos, D. S. & Keeling, P. J. Nuclear-encoded, plastid-targeted genes suggest a single common origin for apicomplexan and dinoflagellate plastids. Mol. Biol. Evol. 18, 418–426 (2001)

    Article  CAS  Google Scholar 

  14. Zhang, Z., Green, B. R. & Cavalier-Smith, T. Phylogeny of ultra-rapidly evolving dinoflagellate chloroplast genes: A possible common origin for sporozoan and dinoflagellate plastids. J. Mol. Evol. 51, 26–40 (2000)

    Article  ADS  CAS  Google Scholar 

  15. Cavalier-Smith, T. Principles of protein and lipid targeting in secondary symbiogenesis: Euglenoid, dinoflagellate, and sporozoan plastid origins and the eukaryote family tree. J. Eukaryot. Microbiol. 46, 347–366 (1999)

    Article  CAS  Google Scholar 

  16. Keeling, P. J. Diversity and evolutionary history of plastids and their hosts. Am. J. Bot. 91, 1481–1493 (2004)

    Article  Google Scholar 

  17. Cavalier-Smith, T. & Chao, E. E. Protalveolate phylogeny and systematics and the origins of Sporozoa and dinoflagellates (phylum Myzozoa nom. nov.). Eur. J. Protistol. 40, 185–212 (2004)

    Article  Google Scholar 

  18. Lang-Unnasch, N. & Aiello, D. P. Sequence evidence for an altered genetic code in the Neospora caninum plastid. Int. J. Parasitol. 29, 1557–1562 (1999)

    Article  CAS  Google Scholar 

  19. Kremp, A. et al. Woloszynskia halophila (Biecheler) comb. nov.: A bloom-forming cold-water dinoflagellate co-occurring with Scrippsiella hangoei (Dinophyceae) in the Baltic Sea. J. Phycol. 41, 629–642 (2005)

    Article  Google Scholar 

  20. Cavalier-Smith, T. Membrane heredity and early chloroplast evolution. Trends Plant Sci. 5, 174–182 (2000)

    Article  CAS  Google Scholar 

  21. Hopkins, J. et al. The plastid in Plasmodium falciparum asexual blood stages: a three-dimensional ultrastructural analysis. Protist 150, 283–295 (1999)

    Article  CAS  Google Scholar 

  22. Köhler, S. Multi-membrane-bound structures of Apicomplexa: I. the architecture of the Toxoplasma gondii apicoplast. Parasitol. Res. 96, 258–272 (2005)

    Article  Google Scholar 

  23. York, R. H. in Coral Reef Population Biology (eds Jokiel, P. L., Richmond, R. H. & Rogers, R. A.) 486–487 (Hawaii Univ. Sea Grant Coll. Program, Honolulu, Hawaii, 1986)

    Google Scholar 

  24. Wakefield, T. S., Farmer, M. A. & Kempf, S. C. Revised description of the fine structure of in situ “zooxanthellae” genus Symbiodinium. Biol. Bull. 199, 76–84 (2000)

    Article  CAS  Google Scholar 

  25. Huang, J. et al. Phylogenomic evidence supports past endosymbiosis, intracellular and horizontal gene transfer in Cryptosporidium parvum. Genome Biol. 5, R88 (2004)

    Article  Google Scholar 

  26. Teles-Grilo, M. L. et al. Is there a plastid in Perkinsus atlanticus (Phylum Perkinsozoa)? Eur. J. Protistol. 43, 163–167 (2007)

    Article  Google Scholar 

  27. Dodge, J. D. & Crawford, R. M. Fine structure of the dinoflagellate Oxyrrhis marina. Part 1: The general structure of the cell. Protistologica 7, 295–304 (1971)

    Google Scholar 

  28. Lang-Unnasch, N., Reith, M. E., Munholland, J. & Barta, J. R. Plastids are widespread and ancient in parasites of the phylum Apicomplexa. Int. J. Parasitol. 28, 1743–1754 (1998)

    Article  CAS  Google Scholar 

  29. Leander, B. S., Clopton, R. E. & Keeling, P. J. Phylogeny of gregarines (Apicomplexa) as inferred from small-subunit rDNA and beta-tubulin. Int. J. Syst. Evol. Microbiol. 53, 345–354 (2003)

    Article  CAS  Google Scholar 

  30. Saldarriaga, J. F. et al. Multiple protein phylogenies show that Oxyrrhis marina and Perkinsus marinus are early branches of the dinoflagellate lineage. Int. J. Syst. Evol. Microbiol. 53, 355–365 (2003)

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by an ARC grant to D.A.C. and O.H.-G.; an ABRS grant to D.A.C.; grants from the Czech Science Foundation, Academy of Sciences of the Czech Republic and Czech Ministry of Education to M.O.; University of Iowa start-up funds and an NSF grant to J.M.L.; and a University of Tasmania Institutional Research grant to C.J.S.B. We thank A. McMinn for pulse amplitude modulation data, A. Simpson for analytical suggestions, R. Andersen for culture backup, and A. Polaszek and M. Garland for taxonomic opinions.

Author Contributions R.B.M. isolated the strain while in the D.A.C. laboratory, then while in the J.M.L. laboratory designed the AToL SSU primers and the psbA primers, cloned and sequenced multiple copies of the SSU rRNA gene, a copy of the plastid SSU rRNA gene and initial sections of the psbA and LSU rRNA genes, then assigned precedented methods for culture fixation, and wrote and finalized the draft of the paper; M.O. led and performed phylogenetic analyses of the sequence data, cloned and sequenced a copy of the plastid SSU rDNA gene using different primers than R.B.M., and co-wrote the draft of the paper; M.O. and M.V. performed the TEM and SEM data collection; J.J. and T.C. cloned and sequenced near full-length LSU rDNA and psbA genes and undertook extensive phylogenetic analysis; T.C. performed mito-red staining; S.W.W. and N.W.D. performed pigment analysis and interpreted pigment data; R.B.M., K.H., C.J.S.B. and J.S. interpreted TEM data and assigned taxonomy; K.H. and R.B.M. performed light microscopy; R.B.M., M.O., T.C., K.H., D.H.G. and C.J.S.B. maintained cultures. D.H.G. cloned and sequenced the LSU rRNA gene, using different PCR primers than T.C. and J.J.; R.B.M., M.O., D.H.G., K.H., J.S., O.H.-G., J.M.L., C.J.S.B. and D.A.C. designed research, interpreted evolutionary, ecological and microbiological data, and performed extensive editing and revision.

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Correspondence to Dee A. Carter.

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The file contains Supplementary Notes with additional references, Supplementary Tables S1-S3 and Supplementary Figures S1-S22 with Legends. (PDF 3207 kb)

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Moore, R., Oborník, M., Janouškovec, J. et al. A photosynthetic alveolate closely related to apicomplexan parasites. Nature 451, 959–963 (2008). https://doi.org/10.1038/nature06635

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