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Revisiting the Parvilucifera infectans / P. sinerae (Alveolata, Perkinsozoa) species complex, two parasitoids of dinoflagellates

  • Jeon, Boo Seong (LOHABE, Department of Oceanography, Chonnam National University) ;
  • Nam, Seung Won (LOHABE, Department of Oceanography, Chonnam National University) ;
  • Kim, Sunju (Department of Oceanography, Pukyong National University) ;
  • Park, Myung Gil (LOHABE, Department of Oceanography, Chonnam National University)
  • 투고 : 2018.01.04
  • 심사 : 2018.03.06
  • 발행 : 2018.03.15

초록

Members of the family Parviluciferaceae (Alveolata, Perkinsozoa) are the well-known dinoflagellate parasitoids along with Amoebophrya ceratii species complex and parasitic chytrid Dinomyces arenysensis and contain six species across three genera (i.e., Parvilucifera infectans, P. sinerae, P. rostrata, and P. corolla, Dinovorax pyriformis, and Snorkelia prorocentri) so far. Among Parvilucifera species, the two species, P. infectans and P. sinerae, are very similar or almost identical each other morphologically and genetically, thereby make it difficult to distinguish between the two. The only main difference between the two species known so far is the number of sporangium wall (i.e., 2 layers in P. infectans vs. 3 layers in P. sinerae). During sampling in Masan bay, Korea during the spring season of 2015, the dinoflagellate Akashiwo sanguinea cells infected by the parasite Parvilucifera were observed and this host-parasite system was established in culture. Using this culture, its morphological and ultrastructural features with special emphasis on the variation in the number of sporangium wall over developmental times, were investigated. In addition, the sequences of rDNA regions and ${\beta}-tubulin$ genes were determined. The result clearly demonstrated that the trophocyte at 36 h was covered with 4 layers, and then outer layer of the sporocyte gradually degraded over time, resulting in wall structure consisting of two layers, with even processes being detached from 7-day-old sporangium with smooth surface, indicating that the difference in the number of layers seems not to be an appropriate ultrastructural character for distinguishing P. infectans and P. sinerae. While pairwise comparison of the large subunit rDNA sequences showed 100% identity among P. infectans / P. sinerae species complex, genetic differences were found in the small subunit (SSU) rDNA sequences but the differences were relatively small (11-13 nucleotides) compared with those (190-272 nucleotides) found among the rest of Parvilucifera species (P. rostrata and P. corolla). Those small differences in SSU rDNA sequences of P. infectans / P. sinerae species complex may reflect the variations within inter- strains of the same species from different geographical areas. Taken together, all morphological, ultrastructural, and molecular data from the present study suggest that they are the same species.

키워드

참고문헌

  1. Alacid, E., Rene, A. & Garces, E. 2015. New insights into the parasitoid Parvilucifera sinerae life cycle: the development and kinetics of infection of a bloom-forming dinoflagellate host. Protist 166:677-699. https://doi.org/10.1016/j.protis.2015.09.001
  2. Azevedo, C. 1989. Fine structure of Perkinsus atlanticus n. sp.(Apicomplexa, Perkinsea) parasite of the clam Ruditapes decussatus from Portugal. J. parasitol. 75:627-635.
  3. Coats, D. W. 1999. Parasitic life styles of marine dinoflagellates. J. Eukaryot. Microbiol. 46:402-409. https://doi.org/10.1111/j.1550-7408.1999.tb04620.x
  4. Coats, D. W., Bachvaroff, T. R. & Delwiche, C. F. 2012. Revision of the family Duboscquellidae with description of Euduboscquella crenulata n. gen., n. sp. (Dinoflagellata, Syndinea), an intracellular parasite of the ciliate Favella panamensis Kofoid & Campbell, 1929. J. Eukaryot. Microbiol. 59:1-11. https://doi.org/10.1111/j.1550-7408.2011.00588.x
  5. Coats, D. W. & Bockstahler, K. R. 1994. Occurrence of the parasitic dinoflagellate Amoebophrya ceratii in Chesapeake Bay populations of Gymnodinium sanguineum. J. Eukaryot. Microbiol. 41:586-593. https://doi.org/10.1111/j.1550-7408.1994.tb01520.x
  6. Coats, D. W. & Park, M. G. 2002. Parasitism of photosynthetic dinoflagellates by three strains of Amoebophrya (Dinophyta): parasite survival, infectivity, generation time, and host specificity. J. Phycol. 38:520-528. https://doi.org/10.1046/j.1529-8817.2002.01200.x
  7. Daugbjerg, N., Hansen, G., Larsen, J. & Moestrup, O. 2000. Phylogeny of some of the major genera of dinoflagellates based on ultrastructure and partial LSU rDNA sequence data, including the erection of three new genera of unarmoured dinoflagellates. Phycologia 39:302-317. https://doi.org/10.2216/i0031-8884-39-4-302.1
  8. Figueroa, R. I., Garcés, E., Massana, R. & Camp, J. 2008. Description, host-specificity, and strain selectivity of the dinoflagellate parasite Parvilucifera sinerae sp. nov. (Perkinsozoa). Protist 159:563-578. https://doi.org/10.1016/j.protis.2008.05.003
  9. Garces, E., Alacid, E., Bravo, I., Fraga, S. & Figueroa, R. I. 2013. Parvilucifera sinerae (Alveolata, Myzozoa) is a generalist parasitoid of dinoflagellates. Protist 164:245-260. https://doi.org/10.1016/j.protis.2012.11.004
  10. Garces, E. & Hoppenrath, M. 2010. Ultrastructure of the intracellular parasite Parvilucifera sinerae (Alveolata, Myzozoa) infecting the marine toxic planktonic dinoflagellate Alexandrium minutum (Dinophyceae). Harmful Algae 10:64-70. https://doi.org/10.1016/j.hal.2010.07.001
  11. Guillard, R. R. L. & Ryther, J. H. 1962. Studies of marine planktonic diatoms: I. Cyclotella nana Hustedt, and Detonula confervacea (CLEVE) Gran. Can. J. Microbiol. 8:229-239. https://doi.org/10.1139/m62-029
  12. Jephcott, T. G., Alves-De-Souza, C., Gleason, F. H., Van Ogtrop, F. F., Sime-Ngando, T., Karpov, S. A. & Guillou, L. 2016. Ecological impacts of parasitic chytrids, syndiniales and perkinsids on populations of marine photosynthetic dinoflagellates. Fungal Ecol. 19:47-58. https://doi.org/10.1016/j.funeco.2015.03.007
  13. Kim, S. 2006. Patterns in host range for two strains of Amoebophrya (Dinophyta) infecting thecate dinoflagellates: Amoebophyra spp. ex Alexandrium affine and ex Gonyaulax polygramma. J. Phycol. 42:1170-1173. https://doi.org/10.1111/j.1529-8817.2006.00277.x
  14. Leander, B. S. & Hoppenrath, M. 2008. Ultrastructure of a novel tube-forming, intracellular parasite of dinoflagellates: Parvilucifera prorocentri sp. nov. (Alveolata, Myzozoa). Eur. J. Protistol. 44:55-70. https://doi.org/10.1016/j.ejop.2007.08.004
  15. Lepelletier, F., Karpov, S. A., Alacid, E., Le Panse, S., Bigeard, E., Garces, E., Jeanthon, C. & Guillou, L. 2014a. Dinomyces arenysensis gen. et sp. nov. (Rhizophydiales, Dinomycetaceae fam. nov.), a chytrid infecting marine dinoflagellates. Protist 165:230-244. https://doi.org/10.1016/j.protis.2014.02.004
  16. Lepelletier, F., Karpov, S. A., Le Panse, S., Bigeard, E., Skovgaard, A., Jeanthon, C. & Guillou, L. 2014b. Parvilucifera rostrata sp. nov. (Perkinsozoa), a novel parasitoid that infects planktonic dinoflagellates. Protist 165:31-49.
  17. Linton, E. W. 2005. MacGDE: genetic data environment for MacOS X. Software available from: http://www.msu.edu/- lintone/macgde.
  18. 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. https://doi.org/10.1016/0378-1119(88)90066-2
  19. Noren, F., Moestrup, O. & Rehnstam-Holm, A. -S. 1999. Parvilucifera infectans Noren et Moestrup gen. et sp. nov. (Perkinsozoa phylum nov.): a parasitic flagellate capable of killing toxic microalgae. Eur. J. Protistol. 35:233-254. https://doi.org/10.1016/S0932-4739(99)80001-7
  20. Noren, F., Moestrup, O., Rehnstam-Holm, A. -S. & Larsen, J. 2001. Worldwide occurrence and host specificity of Parvilucifera infectans: a parasitic flagellate capable of killing toxic dinoflagellates. In Hallegraeff, G. M., Blackburn, S. I., Bolch, C. J. & Lewis, R. J. (Eds.) Harmful Algal Blooms. Intergovernmental Oceanographic Commission of UNESCO, Paris, pp. 481-483.
  21. Park, M. G., Kim, S., Shin, E. -Y., Yih, W. & Coats, D. W. 2013. Parasitism of harmful dinoflagellates in Korean coastal waters. Harmful Algae 30(Suppl. 1):S62-S74. https://doi.org/10.1016/j.hal.2013.10.007
  22. Park, M. G., Yih, W. & Coats, D. W. 2004. Parasites and phytoplankton, with special emphasis on dinoflagellate infections. J. Eukaryot. Microbiol. 51:145-155. https://doi.org/10.1111/j.1550-7408.2004.tb00539.x
  23. Posada, D. & Crandall, K. A. 1998. Modeltest: testing the model of DNA substitution. Bioinformatics 14:817-818. https://doi.org/10.1093/bioinformatics/14.9.817
  24. Rene, A., Alacid, E., Ferrera, I. & Garces, E. 2017a. Evolutionary trends of Perkinsozoa (Alveolata) characters based on observations of two new genera of parasitoids of dinoflagellates, Dinovorax gen. nov. and Snorkelia gen. nov. Front. Microbiol. 8:1594. https://doi.org/10.3389/fmicb.2017.01594
  25. Rene, A., Alacid, E., Figueroa, R. I., Rodriguez, F. & Garces, E. 2017b. Life-cycle, ultrastructure, and phylogeny of Parvilucifera corolla sp. nov. (Alveolata, Perkinsozoa), a parasitoid of dinoflagellates. Eur. J. Protistol 58:9-25. https://doi.org/10.1016/j.ejop.2016.11.006
  26. Ronquist, F., Teslenko, M., Van Der Mark, P., Ayres, D. L., Darling, A., Hohna, S., Larget, B., Liu, L., Suchard, M. A. & Huelsenbeck, J. P. 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61:539-542. https://doi.org/10.1093/sysbio/sys029
  27. Scholin, C. A., Herzog, M., Sogin, M. & Anderson, D. M. 1994. Identification of group‐and strain‐specific genetic markers for globally distributed Alexandrium (Dinophyceae). II. Sequence analysis of a fragment of the LSUrRNA gene. J. Phycol. 30:999-1011. https://doi.org/10.1111/j.0022-3646.1994.00999.x
  28. Skovgaard, A. 2014. Dirty tricks in the plankton: diversity and role of marine parasitic protists. Acta Protozool. 53:51-62
  29. Stamatakis, A. 2006. RAxML-VI-HPC: maximum likelihoodbased phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688-2690. https://doi.org/10.1093/bioinformatics/btl446
  30. Thompson, J. D., Higgins, D. G. & Gibson, T. J. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680. https://doi.org/10.1093/nar/22.22.4673
  31. Turon, M., Alacid, E., Figueroa, R. I., Rene, A., Ferrera, I., Bravo, I., Ramilo, I. & Garces, E. 2015. Genetic and phenotypic diversity characterization of natural populations of the parasitoid Parvilucifera sinerae. Aquat. Microb. Ecol. 76:117-132. https://doi.org/10.3354/ame01771
  32. White, T. J., Bruns, T., Lee, S. & Taylor, J. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In Innis, M. A., Gelfand, D. H., Sninsky, J. J. & White, T. J. (Eds.) PCR Protocols: A Guide to Methods and Applications. Academic Press Inc., New York, pp. 315-322.

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