Advertisement

Systematic Parasitology

, Volume 90, Issue 2, pp 125–135 | Cite as

The molecular phylogeny of the type-species of Oodinium Chatton, 1912 (Dinoflagellata: Oodiniaceae), a highly divergent parasitic dinoflagellate with non-dinokaryotic characters

  • Fernando Gómez
  • Alf Skovgaard
Article

Abstract

Oodinium pouchetii (Lemmermann, 1899) Chatton, 1912, the first described parasitic dinoflagellate, is the type of the Oodiniaceae Chatton, 1920. In the taxonomical schemes, this family of metazoan parasites includes Amyloodinium Brown & Hovasse, 1946 and Piscinoodinium Lom, 1981 that are responsible of important damages in fish aquaculture. Species of Oodinium Chatton, 1912 have unique characteristics such as the possession of both non-dinokaryotic and dinokaryotic nuclei within the life-cycle, and the absence of the transversal (cingulum) and longitudinal (sulcus) surface grooves in the parasitic stage. We provide the first molecular data for the genus Oodinium from specimens of O. pouchetii infecting the chordate Oikopleura sp. (Tunicata: Appendicularia) off the coasts of Brazil. Although O. pouchetii lacks dinokaryotic characters in the parasitic stage, the SSU rDNA phylogeny revealed that it forms a distinct fast-evolved clade that branches among the dinokaryotic dinoflagellates. However, there is no clear relationship with other dinoflagellates. Hence, the taxonomic affinity of the family Oodiniaceae is unclear at the moment.

Keywords

Settling Chamber Environmental Sequence Environmental Clone Thecal Plate Bayesian Consensus Tree 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

F.G. was supported by the Brazilian Conselho Nacional de Desenvolvimento Científico e Tecnológico (grant no. BJT 370646/2013-14). A.S. was supported through the project IMPAQ - IMProvement of AQuaculture high quality fish fry production, funded by the Danish Council for Strategic Research (Grant No. 10-093522).

Supplementary material

11230_2014_9538_MOESM1_ESM.pdf (500 kb)
Supplementary material 1 (PDF 499 kb)

References

  1. Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J., Zhang, Z., Miller, W., & Lipman, D. J. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research, 25, 3389–3402.PubMedCentralPubMedCrossRefGoogle Scholar
  2. Brown, E. M. (1934). On Oodinium ocellatum Brown, a parasitic dinoflagellate causing epidemic disease in marine fish. Proceedings of the Zoological Society of London, Part, 3, 583–607.Google Scholar
  3. Brown, E. M., & Hovasse, R. (1946). Amyloodinium ocellatum (Brown), a peridinian parasitic on marine fishes. A complementary study. Proceedings of the Zoological Society of London, 116, 33–46.CrossRefGoogle Scholar
  4. Cachon, J., & Cachon, M. (1971). Ultrastructures du genre Oodinium Chatton. Différentiations cellulaires en rapport avec la vie parasitaire. Protistologica, 7, 153–169.Google Scholar
  5. Cachon, J., & Cachon, M. (1977). Observations on the mitosis and on the chromosome evolution during the life-cycle of Oodinium, a parasitic dinoflagellate. Chromosoma, 60, 237–251.PubMedCrossRefGoogle Scholar
  6. Cachon, J., & Cachon, M. (1987). Parasitic dinoflagellates. In: Taylor, F. J. R. (Ed.) The Biology of Dinoflagellates. Botanical Monographs, Vol. 21. Oxford: Blackwell, pp. 571–610.Google Scholar
  7. Castresana, J. (2000). Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution, 17, 540–552.PubMedCrossRefGoogle Scholar
  8. Chatton, É. (1912). Diagnoses préliminaires de Péridiniens parasites nouveaux. Bulletin de la Société zoologique de France, 37, 85–93.Google Scholar
  9. Chatton, É. (1920). Les Péridiniens parasites. Morphologie, reproduction, éthologie. Archives de Zoologie Expérimentale et Générale, 59, 1–475.Google Scholar
  10. Cheung, M. K., Chu, K. H., Li, C. P., Kwan, H. S., & Wong, C. K. (2008). Genetic diversity of picoeukaryotes in a semi-enclosed harbour in the subtropical western Pacific. Aquatic Microbial Ecology, 53, 295–305.CrossRefGoogle Scholar
  11. Coats, D. W., Bachvaroff, T. R., Handy, S. M., Kim, S. Y., Gárate-Lizárraga, I., & Delwiche, C. F. (2008). Prevalence and phylogeny of parasitic dinoflagellates (genus Blastodinium) infecting copepods in the Gulf of California. CICIMAR Oceánides, 23, 67–77.Google Scholar
  12. Coats, D. W., Kim, S., Bachvaroff, T. R., Handy, S. M., & Delwiche, C. F. (2010). Tintinnophagus acutus n. g., n. sp. (Phylum Dinoflagellata), an ectoparasite of the ciliate Tintinnopsis cylindrica Daday 1887, and its relationship to Duboscquodinium collini Grassé 1952. Journal of Eukaryotic Microbiology, 57, 468–682.PubMedCrossRefGoogle Scholar
  13. Ekelund, F., Daugbjerg, N., & Fredslund, K. (2004). Phylogeny of Heteromita, Cercomonas and Thaumatomonas based on SSU rDNA sequences, including the description of Neocercomonas jutlandica sp. nov., gen. nov. European Journal of Protistology, 40, 119–135.CrossRefGoogle Scholar
  14. Elwood, H. J., Olsen, G. J., & Sogin, M. L. (1985). The small-subunit ribosomal RNA gene sequences from the hypotrichous ciliates Oxytricha nova and Stylonychia pustulata. Molecular Biology and Evolution, 2, 399–410.PubMedGoogle Scholar
  15. 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 number, 7, 1–351.Google Scholar
  16. Fukuda, Y., & Endoh, H. (2006). New details from the complete life cycle of the red-tide dinoflagellate Noctiluca scintillans (Ehrenberg) McCartney. European Journal of Protistology, 42, 209–219.PubMedCrossRefGoogle Scholar
  17. Giovannoni, S. J., DeLong, E. F., Olsen, G. J., & Pace, N. R. (1988). Phylogenetic group-specific oligodeoxynucleotide probes for identification of single microbial cells. Journal of Bacteriology, 170, 720–726.PubMedCentralPubMedGoogle Scholar
  18. Gómez, F. (2012). A quantitative review of the lifestyle, habitat and trophic diversity of dinoflagellates (Dinoflagellata, Alveolata). Systematics and Biodiversity, 10, 267–275.CrossRefGoogle Scholar
  19. Gómez, F. (2014). Problematic biases in the availability of molecular markers in protists: The example of the dinoflagellates. Acta Protozoologica, 53, 63–75.Google Scholar
  20. Gómez, F., López-García, P., Nowaczyk, A., & Moreira, D. (2009a). The crustacean parasites Ellobiopsis Caullery, 1910 and Thalassomyces Niezabitowski, 1913 form a monophyletic divergent clade within the Alveolata. Systematic Parasitology, 74, 65–74.PubMedCrossRefGoogle Scholar
  21. Gómez, F., Moreira, D., & López-García, P. (2009b). Life cycle and molecular phylogeny of the dinoflagellates Chytriodinium and Dissodinium, ectoparasites of copepod eggs. European Journal of Protistology, 45, 260–270.PubMedCrossRefGoogle Scholar
  22. Gómez, F., Moreira, D., & López-García, P. (2010). Molecular phylogeny of noctilucoid dinoflagellates (Noctilucales, Dinophyta). Protist, 161, 466–478.PubMedCrossRefGoogle Scholar
  23. Gómez, F., & Skovgaard, A. (2014). Molecular phylogeny of the parasitic dinoflagellate Chytriodinium within the Gymnodinium clade (Gymnodiniales, Dinophyceae). Journal of Eukaryotic Microbiology (in press) doi: 10.1111/jeu.12180.
  24. Guillou, L., Viprey, M., Chambouvet, A., Welsh, R. M., Kirkham, A. R., Massana, R., Scanlan, D. J., & Worden, A. Z. (2008). Widespread occurrence and genetic diversity of marine parasitoids belonging to Syndiniales (Alveolata). Environmental Microbiology, 10, 3349–3365.PubMedCrossRefGoogle Scholar
  25. Horiguchi, T., & Ohtsuka, S. (2001). Oodinium inlandicum sp. nov. (Blastodiniales, Dinophyta), a new ectoparastic dinoflagellate infecting a chaetognath. Sagitta crassa. Plankton Biology and Ecology, 48, 85–95.Google Scholar
  26. Hovasse, R. (1935). Deux Péridiniens parasites convergents: Oodinium poucheti (Lemm.), Protoodinium chattoni gen. nov. sp. nov. Bulletin Scientifique de la France et de la Belgique, 69, 59–86.Google Scholar
  27. Huelsenbeck, J. P., & Ronquist, F. (2001). MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics, 17, 754–755.PubMedCrossRefGoogle Scholar
  28. Kühn, S. F., & Medlin, L. K. (2005). The systematic position of the parasitoid marine dinoflagellate Paulsenella vonstoschii (Dinophyceae) inferred from nuclear-encoded small subunit ribosomal DNA. Protist, 156, 393–398.PubMedCrossRefGoogle Scholar
  29. Landsberg, J. H., Steidinger, K. A., Blakesley, B. A., & Zondervan, R. L. (1994). Scanning electron microscope study of dinospores of Amyloodinium cf. ocellatum, a pathogenic dinoflagellate parasite of marine fish, and comments on its relationship to the peridiniales. Diseases of Aquatic Organisms, 20, 23–32.CrossRefGoogle Scholar
  30. Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., López, R., Thompson, J. D., Gibson, T. J., & Higgins, D. G. (2007). Clustal W and Clustal X version 2.0. Bioinformatics, 23, 2947–2948.PubMedCrossRefGoogle Scholar
  31. Lauckner, G. (1984). Diseases caused by protophytans (algae). In Kinne, O. (Ed.) Diseases of marine animals, Vol. IV, Part 1, Pisces. Hamburg: Biologische Anstalt Helgoland, pp. 169–179.Google Scholar
  32. Levy, M. G., Litaker, R. W., Goldstein, R. J., Dykstra, M. J., Vandersea, M. W., & Noga, E. J. (2007). Piscinoodinium, a fish-ectoparasitic dinoflagellate, is a member of the class Dinophyceae, subclass Gymnodiniphycidae: convergent evolution with Amyloodinium. Journal of Parasitology, 93, 1006–1015.PubMedCrossRefGoogle Scholar
  33. Lie, A. A., Liu, Z., Hu, S. K., Jones, A. C., Kim, D. Y., Countway, P. D., Amaral-Zettler, L. A., Cary, S. C., Sherr, E. B., Sherr, B. F., Gast, R. J., & Caron, D. A. (2014). Investigating microbial eukaryotic diversity from a global census: Insights from a comparison of Pyrotag and full-length sequences of 18S rRNA genes. Applied Environmental Microbiology, 80, 4363–4373.PubMedCentralPubMedCrossRefGoogle Scholar
  34. Litaker, R. W., Tester, P. A., Haugen, E. M., Colorni, A., Levy, M. G., & Noga, E. J. (1999). The phylogenetic relationship of Pfiesteria piscicida, cryptoperidiniopsoid sp., Amyloodinium ocellatum and a Pfiesteria-like dinoflagellate to other dinoflagellates and apicomplexans. Journal of Phycology, 35, 1379–1389.CrossRefGoogle Scholar
  35. Lom, J. (1981). Fish invading dinoflagellates: A synopsis of existing and newly proposed genera. Folia Parasitologica, 28, 3–11.PubMedGoogle Scholar
  36. Lom, J., Rohde, K., & Dykova, I. (1993). Crepidoodinium australe n. sp., an ectocommensal dinoflagellate from the gills of Sillago ciliata, an estuarine fish from the New South Wales coast of Australia. Diseases of Aquatic Organisms, 15, 63–72.CrossRefGoogle Scholar
  37. 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.PubMedCrossRefGoogle Scholar
  38. McLean, N., & Nielsen, C. (1989). Oodinium jordani n. sp., a dinoflagellate (Dinoflagellata: Oodinida) ectoparasitic on Sagitta elegans (Chaetognatha). Diseases of Aquatic Organisms, 7, 61–66.CrossRefGoogle Scholar
  39. Medlin, L., Elwood, H. J., Stickel, S., & Sogin, M. L. (1988). The characterization of enzymatically amplified eukaryotic 16S-like rRNA-coding regions. Gene, 71, 491–499.PubMedCrossRefGoogle Scholar
  40. Mills, C. E., & McLean, N. (1991). Ectoparasitism by a dinoflagellate (Dinoflagellata: Oodinidae) on 5 ctenophores (Ctenophora) and a hydromedusa (Cnidaria). Diseases of Aquatic Organisms, 10, 211–216.CrossRefGoogle Scholar
  41. 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.PubMedCrossRefGoogle Scholar
  42. Nylander, J. A. A. (2004). MrModeltest v2. Program distributed by the author. http://www.abc.se/~nylander/mrmodeltest2/mrmodeltest2.html.
  43. Pouchet, G. (1884). Sur un Péridinien parasite. Comptes Rendus de l’Académie des Sciences, Paris, 98, 1345–1346.Google Scholar
  44. Pouchet, G. (1885). Contribution à l’histoire des Péridiniens marins. Journal de l’Anatomie et de la Physiologie Normales et Pathologiques de l’Homme et des Animaux, Paris, 21, 28–88.Google Scholar
  45. Rueckert, S., & Leander, B. S. (2008). Morphology and molecular phylogeny of Haplozoon praxillellae n. sp. (Dinoflagellata): a novel intestinal parasite of the maldanid polychaete Praxillella pacifica Berkeley. European Journal of Protistology, 44, 299–307.PubMedCrossRefGoogle Scholar
  46. 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. Journal of Molecular Evolution, 53, 204–213.PubMedCrossRefGoogle Scholar
  47. Shields, J. D. (1994). The parasitic dinoflagellates of marine crustaceans. Annual Review of Fish Diseases, 4, 241–271.CrossRefGoogle Scholar
  48. Siano, P., Montresor, M., Not, F., & Vargas, C. (2010). Pelagodinium gen. nov. and P. béii comb. nov., a dinoflagellate symbiont of planktonic Foraminifera. Protist, 161, 385–399.PubMedCrossRefGoogle Scholar
  49. Skovgaard, A., & Saiz, E. (2006). Seasonal occurrence and role of protistan parasites in coastal marine zooplankton. Marine Ecology Progress Series, 327, 37–49.CrossRefGoogle Scholar
  50. Skovgaard, A., Massana, R., & Saiz, E. (2007). Parasitic species of the genus Blastodinium (Blastodiniphyceae) are peridinioid dinoflagellates. Journal of Phycology, 43, 553–560.CrossRefGoogle Scholar
  51. Skovgaard, A., & Salomonsen, X. M. (2009). Blastodinium galatheanum sp. nov. (Dinophyceae) a parasite of the planktonic copepod Acartia negligens (Crustacea, Calanoida) in the central Atlantic Ocean. European Journal of Phycology, 44, 425–438.CrossRefGoogle Scholar
  52. Skovgaard, A., Karpov, S. A., & Guillou, L. (2012). The parasitic dinoflagellates Blastodinium spp. inhabiting the gut of marine, planktonic copepods: morphology, ecology, and unrecognized species diversity. Frontiers in Microbiology, 3, 305.PubMedCentralPubMedCrossRefGoogle Scholar
  53. Taylor, F. J. R. (2004). Illumination or confusion? Dinoflagellate molecular phylogenetic data viewed from a primarily morphological standpoint. Phycological Research, 52, 308–324.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  1. 1.Laboratory of Plankton Systems, Oceanographic InstituteUniversity of São PauloButantãBrazil
  2. 2.Department of Veterinary Disease Biology, Faculty of Health and Medical SciencesUniversity of CopenhagenFrederiksberg CDenmark
  3. 3.Department of Environmental, Social and Spatial ChangeUniversity of RoskildeRoskildeDenmark

Personalised recommendations