Advertisement

Systematic Parasitology

, Volume 74, Issue 1, pp 65–74 | Cite as

The crustacean parasites Ellobiopsis Caullery, 1910 and Thalassomyces Niezabitowski, 1913 form a monophyletic divergent clade within the Alveolata

  • Fernando Gómez
  • Purificación López-García
  • Antoine Nowaczyk
  • David Moreira
Article

Abstract

The Ellobiopsidae are enigmatic parasites of crustaceans that have been grouped together exclusively on the basis of morphological similarities. Ultrastructural studies have revealed their affiliation within the alveolates, which was confirmed by the phylogenetic analysis of the ribosomal RNA gene (SSU rDNA) sequences of two species of Thalassomyces Niezabitowski, 1913. However, their precise systematic position within this group remains unresolved, since they could not be definitively allied with any particular alveolate group. To better determine the systematic position of ellobiopsids by molecular phylogeny, we sequenced the SSU rDNA from the type-species of the Ellobiopsidae, Ellobiopsis chattoni Caullery, 1910. We found E. chattoni infecting various copepod hosts, Acartia clausi Giesbrecht, Centropages typicus Kröyer and Clausocalanus sp., in the Bay of Marseille, NW Mediterranean Sea, which allowed us to study several stages of the parasite development. A single unicellular multinucleate specimen provided two different sequences of the SSU rDNA gene, indicating the existence of polymorphism at this locus within single individuals. Ellobiopsis Caullery, 1910 and Thalassomyces formed a very divergent and well-supported clade in phylogenetic analyses. This clade appears to be more closely related to the dinoflagellates (including the Syndiniales/Marine Alveolate Group II and the Dinokaryota) and Marine Alveolate Group I than to the other alveolates (Ciliophora, Perkinsozoa and Apicomplexa).

Keywords

Copepod Species Accession EF539153 Infected Copepod Parasitic Dinoflagellate Hematodinium 
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

This is a contribution to the project DIVERPLAN-MED supported by a post-doctoral grant to F.G. of the Ministerio Español de Educación y Ciencia No. 2007-0213. P.L.G. and D.M. acknowledge financial support from the French CNRS and the ANR Biodiversity project ‘Aquaparadox’. This is a part of SOMLIT (Service d’Observation en Milieu LITtoral) national grid.

References

  1. Albaina, A., & Irigoien, X. (2006). Fecundity limitation of Calanus helgolandicus, by the parasite Ellobiopsis sp. Journal of Plankton Research, 28, 413–418.CrossRefGoogle Scholar
  2. Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J., Zhang, Z., et al. (1997). Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Research, 25, 3389–3402.PubMedCrossRefGoogle Scholar
  3. Alverson, A. J., & Kolnick, L. (2005). Intragenomic nucleotide polymorphism among small subunit (18S) rDNA paralogs in the diatom genus Skeletonema (Bacillariophyta). Journal of Phycology, 41, 1248–1257.CrossRefGoogle Scholar
  4. Boschma, H. (1949). Ellobiopsidae. Discovery Report, 25, 281–314.Google Scholar
  5. Boschma, H. (1959). Ellobiopsidae from the tropical West Africa. Atlantide Report, 5, 145–175.Google Scholar
  6. Burreson, E. M., Dungan, C. F., & Reece, K. S. (2005). Molecular, morphological, and experimental evidence support the synonymy of Perkinsus chesapeaki and Perkinsus andrewsi. Journal of Eukaryotic Microbiology, 52, 258–270.PubMedGoogle Scholar
  7. Cachon, J., & Cachon, M. (1987). Parasitic dinoflagellates. In F. J. R. Taylor (Ed.), The biology of dinoflagellates (pp. 571–610). Oxford: Blackwell.Google Scholar
  8. Caullery, M. (1910). Ellobiopsis chattoni, n. g., n. sp., parasite de Calanus helgolandicus Claus, appartenant probablement aux Péridiniens. Bulletin Scientifique de la France et la Belgique, 44, 201–214.Google Scholar
  9. Cavalier-Smith, T. (1993). Kingdom Protozoa and its 18 phyla. Microbiological Reviews, 57, 953–994.PubMedGoogle Scholar
  10. Cavalier-Smith, T., & Chao, E. E. (2004). Protalveolae phylogeny and systematics and the origins of Sporozoa and dinoflagellates (phylum Myzozoa nom nov.). European Journal of Protistology, 40, 185–212.CrossRefGoogle Scholar
  11. Chatton, E. (1920). Les Péridiniens parasites. Morphologie, reproduction, éthologie. Archives de Zoologie Experimentale et Générale, 59, 1–475.Google Scholar
  12. Chatton, E. (1952). Classe des Dinoflagellés ou Péridiniens. In P. Grassé (Ed.), Traité de Zoologie (Vol. 1, pp. 1309–1406). Paris: Masson et Cie.Google Scholar
  13. Collin, B. (1913). Sur un Ellobiopside nouveau parasite des Nebalies (Parallobiopsis coutieri n. g., n. sp.). Comptes Rendus de l’Academie des Sciences, 156, 1332–1333.Google Scholar
  14. Dick, M. W. (2001). Straminipilous fungi: Systematics of the peronosporomycetes, including accounts of the marine straminipilous protists, the plasmodiophorids, and similar organisms. Dordrecht: Kluwer, 654 pp.Google Scholar
  15. Edgar, R. C. (2004). MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32, 1792–1797.PubMedCrossRefGoogle Scholar
  16. Fukuda, Y., & Endoh, H. (2008). Phylogenetic analyses of the dinoflagellate Noctiluca scintillans based on β-tubulin and Hsp90 genes. European Journal of Protistology, 44, 27–33.PubMedCrossRefGoogle Scholar
  17. Galt, J. H., & Whisler, H. C. (1970). Differentiation of flagellate spores in Thalassomyces Ellobiopsid parasite of marine Crustacea. Archiv für Mikrobiologie, 71, 295–303.CrossRefGoogle Scholar
  18. Grassé, P. P. (1952). Les Ellobiopsidae. In P. Grassé (Ed.), Traité de Zoologie (Vol. 1, pp. 1023–1030). Paris: Masson et Cie.Google Scholar
  19. Gribble, K. E., & Anderson, D. M. (2007). High intraindividual, intraspecific, and interspecific variability in large-subunit ribosomal DNA in the heterotrophic dinoflagellates Protoperidinium, Diplopsalis, and Preperidinium (Dinophyceae). Phycologia, 46, 315–324.CrossRefGoogle Scholar
  20. Guillou, L., Viprey, M., Chambouvet, A., Welsh, R. M., Kirkham, A. R., Massana, R., et al. (2008). Widespread occurrence and genetic diversity of marine parasitoids belonging to Syndiniales (Alveolata). Environmental Microbiology, 10, 3349–3365.PubMedCrossRefGoogle Scholar
  21. Harada, A., Ohtsuka, S., & Horiguchi, T. (2007). Species of the parasitic genus Duboscquella are members of the enigmatic marine alveolate Group I. Protist, 158, 337–347.PubMedCrossRefGoogle Scholar
  22. Hovasse, R. (1926). “Parallobiopsis coutieri” Collin. Morphologie, cytologie, évolution, affinités des Ellobiopsidés. Bulletin Scientifique de la France et la Belgique, 60, 409–446.Google Scholar
  23. Hovasse, R. (1952). Ellobiopsis fagei Hovasse, Ellobiopsidé parasite, en Méditerranée, de Clausocalanus arcuicornis Dana. Bulletin de l’Institut Océanographique, Monaco, 1016, 1–12.Google Scholar
  24. Huelsenbeck, J. P., & Ronquist, F. (2001). MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics, 17, 754–755.PubMedCrossRefGoogle Scholar
  25. Jepps, M. W. (1937). On the protozoan parasites of Calanus finmarchicus in the Cycle Sea area. Quarterly Journal of Microscopical Science, 79, 589–658.Google Scholar
  26. Jobb, G., von Haeseler, A., & Strimmer, K. (2004). TREEFINDER: A powerful graphical analysis environment for molecular phylogenetics. BMC Evolutionary Biology, 4, 18.PubMedCrossRefGoogle Scholar
  27. Kim, S., Park, M. G., Kim, K. Y., Kim, C. H., Yih, W., Park, J. S., et al. (2008). Genetic diversity of parasitic dinoflagellates in the genus Amoebophrya and its relationship to parasite biology and biogeography. Journal of Eukaryotic Microbiology, 55, 1–8.PubMedCrossRefGoogle Scholar
  28. Lanave, C., Preparata, G., Saccone, C., & Serio, G. (1984). A new method for calculating evolutionary substitution rates. Journal of Molecular Evolution, 20, 86–93.PubMedCrossRefGoogle Scholar
  29. Lartillot, N., & Philippe, H. (2004). A Bayesian mixture model for across-site heterogeneities in the amino-acid replacement process. Molecular Biology and Evolution, 21, 1095–1109.PubMedCrossRefGoogle Scholar
  30. Leander, B. S., & Hoppenrath, M. (2008). Ultrastructure of a novel tube-forming, intracellular parasite of dinoflagellates: Parvilucifera prorocentri sp. nov. (Alveolata, Myzozoa). European Journal of Protistology, 44, 55–70.PubMedCrossRefGoogle Scholar
  31. 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
  32. Mauchline, J. (1998). The biology of calanoid copepods. Advances in Marine Biology, 33, 1–710.CrossRefGoogle Scholar
  33. Moreira, D., & López-García, P. (2002). The molecular ecology of microbial eukaryotes unveils a hidden world. Trends in Microbiology, 10, 31–38.PubMedCrossRefGoogle Scholar
  34. Mori, K., Yamamoto, K., Teruya, K., Shiozawa, S., Yoseda, K., Sugaya, T., et al. (2007). Endoparasitic dinoflagellate of the genus Ichthyodinium infecting fertilized eggs and hatched larvae observed in the seed production of leopard coral grouper Plectropomus leopardus. Fish Pathology, 42, 49–57.CrossRefGoogle Scholar
  35. Niezabitowski, E. L. (1913). Die pfianzlichen Parasiten der Tiefsee-Decapoden-Gattung Pasiphaea. Kosmos, 38, 1563–1572.Google Scholar
  36. Norén, F., Moestrup, O., & Rehnstam-Holm, A.-S. (1999). Parvilucifera infectans Norén et Moestrup sp. nov. (Perkinsozoa phylum nov.): A parasitic flagellate capable of killing toxic microalgae. European Journal of Protistology, 35, 233–254.Google Scholar
  37. Philippe, H. (1993). MUST, a computer package of management utilities for sequences and trees. Nucleic Acids Research, 21, 5264–5272.PubMedCrossRefGoogle Scholar
  38. Reichenow, E. (1930). Parasitische Peridinea (einschließlich Ellobiopsidae). Die Tierwelt der Nord- und Ostsee, 19(2.d3), 85–100.Google Scholar
  39. Rodríguez, F., Oliver, J. L., Marín, A., & Medina, J. R. (1990). The general stochastic model of nucleotide substitution. Journal of Theoretical Biology, 142, 485–501.PubMedCrossRefGoogle Scholar
  40. Rose, M. (1933). Copépodes pélagiques. Faune France, 26, 1–374.Google Scholar
  41. Saitou, N., & Nei, M. (1987). The neighbor-joining method: A new method for reconstructing phylogenetic trees. Molecular Biology and Evolution, 4, 406–425.PubMedGoogle Scholar
  42. Schweikert, M., & Elbrächter, M. (2006). First ultrastructural investigations on Ellobiopsis spec. (incertae sedis) a parasite of copepods. Endocytobiosis Cell Research, 17, 73.Google Scholar
  43. Shields, J. D. (1994). The parasitic dinoflagellates of marine crustaceans. Annual Review of Fish Diseases, 4, 241–271.CrossRefGoogle Scholar
  44. Silberman, J. D., Collins, A. G., Gershwin, L. A., Johnson, P. J., & Roger, A. J. (2004). Ellobiopsids of the genus Thalassomyces are alveolates. Journal of Eukaryotic Microbiology, 52, 246–252.CrossRefGoogle Scholar
  45. Skovgaard, A., Massana, R., Balague, V., & Saiz, E. (2005). Phylogenetic position of the copepod-infesting parasite Syndinium turbo (Dinoflagellata, Syndinea). Protist, 156, 413–423.PubMedCrossRefGoogle Scholar
  46. Théodoridès, J. (1989). Parasitology of marine zooplankton. Advances in Marine Biology, 25, 117–177.CrossRefGoogle Scholar
  47. Whisler, H. C. (1990). Incertae Sedis Ellobiopsida. In L. Margulis, J. O. Corliss, M. Melkonian, & D. J. Chapman (Eds.), Handbook of Protoctista (pp. 715–719). Boston: Jones & Bartlett.Google Scholar
  48. Yamaguchi, A., Kawamura, H., & Horiguchi, T. (2006). A further phylogenetic study of the heterotrophic dinoflagellate genus, Protoperidinium (Dinophyceae) based on small and large subunit ribosomal RNA gene sequences. Phycological Research, 54, 317–329.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • Fernando Gómez
    • 1
  • Purificación López-García
    • 2
  • Antoine Nowaczyk
    • 3
  • David Moreira
    • 2
  1. 1.Observatoire Océanologique de Banyuls sur MerUniversité Pierre et Marie Curie, CNRS-INSU UMR 7621Banyuls sur MerFrance
  2. 2.Unité d’Ecologie, Systématique et Evolution, CNRS UMR 8079Université Paris-SudOrsay CedexFrance
  3. 3.Laboratoire d’Océanographie Physique et de BiogéochimieCNRS UMR 6535, Aix-Marseille II UniversitéMarseilleFrance

Personalised recommendations