1887

Abstract

and are two alveolate species of key taxonomic position with respect to the divergence of apicomplexans and dinoflagellates. New sequences from , and a number of dinoflagellates were added to datasets of small-subunit (SSU) rRNA, actin, α-tubulin and β-tubulin sequences, as well as to a combined dataset of all three protein-coding genes, and phylogenetic trees were inferred. The parasitic branches at the base of the dinoflagellate clade with high support in most of the individual gene trees and in the combined analysis, strongly confirming the position originally suggested in previous SSU rRNA and actin phylogenies. The SSU rRNA from is extremely divergent, and it typically branches with members of the Gonyaulacales, a dinoflagellate order where SSU rRNA sequences are also divergent. Conversely, none of the three protein-coding genes of is noticeably divergent and, in trees based on all three proteins individually and in combination, branches at the base of the dinoflagellate clade, typically with high bootstrap support. In some trees, and are sisters, but most analyses indicate that diverged prior to . Morphological characters have previously pointed to as an early branch in the dinoflagellate lineage; our data support this suggestion and significantly bolster the molecular data that support a relationship between and dinoflagellates. Together, these two organisms can be instrumental in reconstructing the early evolution of dinoflagellates and apicomplexans by helping to reveal aspects of the ancestors of both groups.

Keyword(s): SSU, small-subunit
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2003-01-01
2024-03-28
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References

  1. Baldauf S. L., Roger A. J., Wenk-Siefert I., Doolittle W. F. 2000; A kingdom-level phylogeny of eukaryotes based on combined protein data. Science 290:972–977 [CrossRef]
    [Google Scholar]
  2. Bruno W. J., Socci N. D., Halpern A. L. 2000; Weighted neighbor joining: a likelihood-based approach to distance-based phylogeny reconstruction. Mol Biol Evol 17:189–197 [CrossRef]
    [Google Scholar]
  3. Cavalier-Smith T. 1998; A revised six-kingdom system of life. Biol Rev Camb Philos Soc 73:203–266 [CrossRef]
    [Google Scholar]
  4. Clarke K. J., Pennick N. C. 1976; The occurrence of body scales in Oxyrrhis marina . Br Phycol J 11:345–348 [CrossRef]
    [Google Scholar]
  5. Diez B., Pedros-Alio C., Massana R. 2001; Study of genetic diversity of eukaryotic picoplankton in different oceanic regions by small-subunit rRNA gene cloning and sequencing. Appl Environ Microbiol 67:2932–2941 [CrossRef]
    [Google Scholar]
  6. Dodge J. D. 1984; Dinoflagellate taxonomy. In Dinoflagellates pp 17–42Edited by Spector D. L. Orlando: Academic Press;
    [Google Scholar]
  7. Dodge J. D., Crawford R. M. 1971; Fine structure of the dinoflagellate Oxyrrhis marina . Part 2: the flagellar system. Protistologica 7:399–409
    [Google Scholar]
  8. Fast N. M., Kissinger J. C., Roos D. S., Keeling P. J. 2001; Nuclear-encoded, plastid-targeted genes suggest a single common origin for apicomplexan and dinoflagellate plastids. Mol Biol Evol 18:418–426 [CrossRef]
    [Google Scholar]
  9. Fast N. M., Xue L., Bingham S., Keeling P. J. 2002; Re-examining alveolate evolution using multiple protein molecular phylogenies. J Eukaryot Microbiol 49:30–37 [CrossRef]
    [Google Scholar]
  10. Felsenstein J. 1993 phylip (Phylogeny Inference Package). Distributed by the author Department of Genetics, University of Washington; Seattle, USA:
    [Google Scholar]
  11. Fensome R. A., Taylor F. J. R., Norris G., Sarjeant W. A. S., Wharton D. I., Williams G. L. 1993; A Classification of Living and Fossil Dinoflagellates . Micropaleontology Special Publication no. 7: New York: American Museum of Natural History;
    [Google Scholar]
  12. Gao X. P., Li J. Y. 1986; Nuclear division in the marine dinoflagellate Oxyrrhis marina . J Cell Sci 85:161–175
    [Google Scholar]
  13. Goggin C. L., Barker S. C. 1993; Phylogenetic position of the genus Perkinsus (Protista, Apicomplexa) based on small subunit ribosomal RNA. Mol Biochem Parasitol 60:65–70 [CrossRef]
    [Google Scholar]
  14. Harrison P. J., Waters R. E., Taylor F. J. R. 1980; A broad spectrum artificial sea water medium for coastal and open ocean phytoplankton. J Phycol 16:28–35
    [Google Scholar]
  15. Höhfeld I., Melkonian M. 1998; Lifting the curtain? The microtubular cytoskeleton of Oxyrrhis marina (Dinophyceae) and its rearrangement during phagocytosis. Protist 149:75–88 [CrossRef]
    [Google Scholar]
  16. Kato K. H., Moriyama A., Huitorel P., Cosson J., Cachon M., Sato H. 1997; Isolation of the major basic nuclear protein and its localization on chromosomes of the dinoflagellate, Oxyrrhis marina . Biol Cell 89:43–52 [CrossRef]
    [Google Scholar]
  17. Keeling P. J. 2001; Foraminifera and Cercozoa are related in actin phylogeny: two orphans find a home? Mol Biol Evol 18. 1551–1557 [CrossRef]
  18. Kofoid C. A., Swezy O. 1921; The Free-living Unarmored Dinoflagellata . University of California Memoirs vol 5: Berkeley, CA: University of California Press;
    [Google Scholar]
  19. Kubai D. F., Ris H. 1969; Division in the dinoflagellate Gyrodinium cohnii (Schiller). A new type of nuclear reproduction. J Cell Biol 40:508–528 [CrossRef]
    [Google Scholar]
  20. Leadbeater B., Dodge J. D. 1967; An electron microscope study of nuclear and cell division in a dinoflagellate. Arch Mikrobiol 57:239–254 [CrossRef]
    [Google Scholar]
  21. Leander B. L., Clopton R. E., Keeling P. J. 2003; Phylogeny of gregarines (Apicomplexa) as inferred from small-subunit rDNA and β-tubulin. Int J Syst Evol Microbiol 53:345–354 [CrossRef]
    [Google Scholar]
  22. Lenaers G., Scholin C., Bhaud Y., Saint-Hilaire D., Herzog M. 1991; A molecular phylogeny of dinoflagellate protists (pyrrophyta) inferred from the sequence of 24S rRNA divergent domains D1 and D8. J Mol Evol 32:53–63 [CrossRef]
    [Google Scholar]
  23. Levine N. D. 1978; Perkinsus gen. n. and other new taxa in the protozoan phylum Apicomplexa. J Parasitol 64:549
    [Google Scholar]
  24. Levine N. D. 1985; Phylum Apicomplexa Levine 1970. In An Illustrated Guide to the Protozoa pp 322–374Edited by Lee J. J., Hutner S. H., Bovee E. C. Lawrence, KS: Society of Protozoologists;
    [Google Scholar]
  25. López-García P., Rodríguez-Valera F., Pedrós-Alió C., Moreira D. 2001; Unexpected diversity of small eukaryotes in deep-sea Antarctic plankton. Nature 409:603–607 [CrossRef]
    [Google Scholar]
  26. Maruyama K., Sugano S. 1994; Oligo-capping: a simple method to replace the cap structure of eukaryotic mRNAs with oligoribonucleotides. Gene 138:171–174 [CrossRef]
    [Google Scholar]
  27. Moon-van der Staay S. Y., De Wachter R., Vaulot D. 2001; Oceanic 18S rDNA sequences from picoplankton reveal unsuspected eukaryotic diversity. Nature 409:607–610 [CrossRef]
    [Google Scholar]
  28. Norén F., Moestrup Ø., Rehnstam-Holm A.-S. 1999; Parvilucifera infectans Norén et Moestrup gen. et sp. nov. (Perkinsozoa phylum nov.): a parasitic flagellate capable of killing toxic microalgae. Eur J Protistol 35:233–254 [CrossRef]
    [Google Scholar]
  29. Perkins F. O. 1976; Zoospores of the oyster pathogen, Dermocystidium marinum . I. Fine structure of the conoid and other aporozoan-like organelles. J Parasitol 20:959–974
    [Google Scholar]
  30. Perkins F. O. 1996; The structure of Perkinsus marinus (Mackin, Owen and Collier, 1950) Levine, 1978 with comments on taxonomy and phylogeny of Perkinsus spp. J Shellfish Res 15:67–87
    [Google Scholar]
  31. Popovský J., Pfiester L. A. 1990 Dinophyceae (Dinoflagellida). Süßwasserflora von Mitteleuropa Band 6 Stuttgart & Jena: Gustav Fischer;
    [Google Scholar]
  32. Reece K. S., Siddall M. E., Burreson E. M., Graves J. E. 1997; Phylogenetic analysis of Perkinsus based on actin gene sequences. J Parasitol 83:417–423 [CrossRef]
    [Google Scholar]
  33. Ris H., Kubai D. F. 1974; An unusual mitotic mechanism in the parasitic protozoan Syndinium sp. J Cell Biol 60:702–720 [CrossRef]
    [Google Scholar]
  34. Roberts K. R. 1985; The flagellar apparatus of Oxyrrhis marina Pyrrophyta. J Phycol 21:641–655
    [Google Scholar]
  35. Roberts K. R. 1991; The flagellar apparatus and cytoskeleton of dinoflagellates: organization and use in systematics. In The Biology of Free-Living Heterotrophic Flagellates pp 285–302 Systematics Association Special Volume 45Edited by Patterson D. J., Larsen J. Oxford: Clarendon Press;
    [Google Scholar]
  36. Sala-Rovira M., Geraud M. L., Caput D., Jacques F., Soyer-Gobillard M. O., Vernet G., Herzog M. 1991; Molecular cloning and immunolocalization of two variants of the major basic nuclear protein (HCc) from the histone-less eukaryote Crypthecodinium cohnii (Pyrrhophyta). Chromosoma 100:510–518 [CrossRef]
    [Google Scholar]
  37. Saldarriaga J. F., Taylor F. J. R., Keeling P. J., Cavalier-Smith T. 2001; Dinoflagellate nuclear SSU rRNA phylogeny suggests multiple plastid losses and replacements. J Mol Evol 53:204–213 [CrossRef]
    [Google Scholar]
  38. Saunders G. W., Hill D. R. A., Sexton J. P., Andersen R. A. 1997; Small-subunit ribosomal RNA sequences from selected dinoflagellates: testing classical evolutionary hypotheses with molecular systematic methods. In Origins of Algae and their PlastidsPlant Systematics and Evolution Supplement pp 237–259Edited by Bhattacharya D. Vienna: Springer Verlag;
    [Google Scholar]
  39. Siddall M. E., Reece K. S., Graves J. E., Burreson E. M. 1997; ‘Total evidence’ refutes the inclusion of Perkinsus species in the phylum Apicomplexa. Parasitology 115:165–176 [CrossRef]
    [Google Scholar]
  40. Siddall M. E., Reece K. S., Nerad T. A., Burreson E. M. 2001; Molecular determination of the phylogenetic position of a species in the genus Colpodella (Alveolata. Am Mus Novit 3314:1–10 [CrossRef]
    [Google Scholar]
  41. Simpson A. G. B., Patterson D. J. 1996; Ultrastructure and identification of the predatory flagellate Colpodella pugnax Cienkowski (Apicomplexa) with a description of Colpodella turpis n. sp. and a review of the genus. Syst Parasitol 33:187–198 [CrossRef]
    [Google Scholar]
  42. Sournia A. 1986 Atlas du Phytoplankton Marin vol IIntroduction, Cyanophycees, Dictyochophycees, Dinophycees et Raphidophycees Paris: Editions du Centre National de la Recherche Scientifique;
    [Google Scholar]
  43. Strimmer K., Von Haeseler A. 1996; Quartet puzzling: a quartet maximum-likelihood method for reconstructing tree topologies. Mol Biol Evol 13:964–969 [CrossRef]
    [Google Scholar]
  44. Suzuki Y., Yoshitomo-Nakagawa K., Maruyama K., Suyama A., Sugano S. 1997; Construction and characterization of a full length-enriched and a 5′-end-enriched cDNA library. Gene 200:149–156 [CrossRef]
    [Google Scholar]
  45. Swofford D. L. 1999; Phylogenetic Analysis using Parsimony (and other Methods PAUP*) 4.0 (test version). Sunderland, MA: Sinauer;
    [Google Scholar]
  46. Triemer R. E. 1982; A unique mitotic variation in the marine dinoflagellate Oxyrrhis marina Pyrrophyta. J Phycol 18:399–411 [CrossRef]
    [Google Scholar]
  47. Van de Peer Y., Caers A., De Rijk P., De Wachter R. 1998; Database on the structure of small ribosomal subunit RNA. Nucleic Acids Res 26:179–182 [CrossRef]
    [Google Scholar]
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