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The Korean Society of Phycology (한국조류학회(藻類))
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Ansanella granifera gen. et sp. nov. (Dinophyceae), a new dinoflagellate from the coastal waters of Korea

  • Jeong, Hae Jin (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University) ;
  • Jang, Se Hyeon (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University) ;
  • Moestrup, Ojvind (Biological Institute, Section of Marine Biology, University of Copenhagen) ;
  • Kang, Nam Seon (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University) ;
  • Lee, Sung Yeon (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University) ;
  • Potvin, Eric (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University) ;
  • Noh, Jae Hoon (Marine Resources Research Department, KIOST)
  • Received : 2014.04.29
  • Accepted : 2014.05.30
  • Published : 2014.06.15
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Abstract

A small dinoflagellate, Ansanella granifera gen. et sp. nov., was isolated from estuarine and marine waters, and examined by light microscopy, scanning electron microscopy, and transmission electron microscopy. In addition, the identity of the sequences (3,663-bp product) of the small subunit (SSU), internal transcribed spacer (ITS) region (ITS1, 5.8S, ITS2), and D1-D3 large subunit (LSU) rDNA were determined. This newly isolated, thin-walled dinoflagellate has a type E eyespot and a single elongated apical vesicle, and it is closely related to species belonging to the family Suessiaceae. A. granifera has 10-14 horizontal rows of amphiesmal vesicles, comparable to Biecheleria spp. and Biecheleriopsis adriatica, but greater in number than in other species of the family Suessiaceae. Unlike Biecheleria spp. and B. adriatica, A. granifera has grana-like thylakoids. Further, A. granifera lacks a nuclear fibrous connective, which is present in B. adriatica. B. adriatica and A. granifera also show a morphological difference in the shape of the margin of the cingulum. In A. granifera, the cingular margin formed a zigzag line, and in B. adriatica a straight line, especially on the dorsal side of the cell. The episome is conical with a round apex, whereas the hyposome is trapezoidal. Cells growing photosynthetically are $10.0-15.0{\mu}m$ long and $8.5-12.4{\mu}m$ wide. The cingulum is descending, the two ends displaced about its own width. Cells of A. granifera contain 5-8 peripheral chloroplasts, stalked pyrenoids, and a pusule system, but lack nuclear envelope chambers, a nuclear fibrous connective, lamellar body, rhizocysts, and a peduncle. The main accessory pigment is peridinin. The SSU, ITS regions, and D1-D3 LSU rDNA sequences differ by 1.2-7.4%, >8.8%, and >2.5%, respectively, from those of the other known genera in the order Suessiales. Moreover, the SSU rDNA sequence differed by 1-2% from that of the three most closely related species, Polarella glacialis, Pelagodinium bei, and Protodinium simplex. In addition, the ITS1-5.8S-ITS2 rDNA sequence differed by 16-19% from that of the three most closely related species, Gymnodinium corii, Pr. simplex, and Pel. bei, and the LSU rDNA sequence differed by 3-4% from that of the three most closely related species, Protodinium sp. CCMP419, B. adriatica, and Gymnodinium sp. CCMP425. A. granifera had a 51-base pair fragment in domain D2 of the large subunit of ribosomal DNA, which is absent in the genus Biecheleria. In the phylogenetic tree based on the SSU and LSU sequences, A. granifera is located in the large clade of the family Suessiaceae, but it forms an independent clade.

Keywords

References

  1. Biecheler, B. 1952. Recherches sur les Peridiniens. Bull. Biol. Fr. Belg. 36(Suppl.):1-149.
  2. Butschli, O. 1885. Erster Band. Protozoa. In Bronn, H. G. (Ed.) Klassen und Ordnungen des Thier-Reichs, wissenschaftlich dargestellt in Wort und Bild. Wintersche Verlagsbuchhandlung, Leipzig, pp. 865-1088.
  3. Calado, A. J., Craveiro, S. C. & Moestrup, O. 1998. Taxonomy and ultrastructure of a freshwater, heterotrophic Amphidinium (Dinophyceae) that feeds on unicellular protists. J. Phycol. 34:536-554. https://doi.org/10.1046/j.1529-8817.1998.340536.x
  4. Craveiro, S. C., Pandeirada, M. S., Daugbjerg, N., Moestrup, O. & Calado, A. J. 2013. Ultrastructure and phylogeny of Theleodinium calcisporum gen. et sp. nov., a freshwater dinoflagellate that produces calcareous cysts. Phycologia 52:488-507. https://doi.org/10.2216/13-152.1
  5. Deeds, J. R., Terlizzi, D. E., Adolf, J. E., Stoecker, D. K. & Place, A. R. 2002. Toxic activity from cultures of Karlodinium micrum (=Gyrodinium galatheanum) (Dinophyceae): a dinoflagellate associated with fish mortalities in an estuarine aquaculture facility. Harmful Algae 1:169-189. https://doi.org/10.1016/S1568-9883(02)00027-6
  6. Dodge, J. D. 1967. Fine structure of the dinoflagellate Aureo-sysdinium pigmentosum gen. et sp. nov. Br. Phycol. Bull. 3:327-336. https://doi.org/10.1080/00071616700650211
  7. Dodge, J. D. 1968. The fine structure of chloroplasts and pyrenoids in some marine dinoflagellates. J. Cell. Sci. 3:41-48.
  8. Dodge, J. D. 1974. A redescription of the dinoflagellate Gymnodinium simplex with the aid of electron microscopy. J. Mar. Biol. Assoc. U. K. 54:171-177. https://doi.org/10.1017/S0025315400022141
  9. Dodge, J. D. 1975. A survey of chloroplast ultrastructure in the Dinophyceae. Phycologia 14:253-263. https://doi.org/10.2216/i0031-8884-14-4-253.1
  10. Fensome, R. A., Taylor, F. J. R., Norris, G., Sarjeant, W. A. S., Wharton, D. I. & William, G. L. 1993. A classification of living and fossil dinoflagellates: micropaleontology. special publication. No. 7. Sheridan Press, Hanover, pp. 56-57.
  11. Foster, K. W. & Smyth, R. D. 1980. Light antennas in phototactic algae. Microbiol. Rev. 44:572-630.
  12. Freudenthal, H. D. 1962. Symbiodinium gen. nov. and Symbiodinium microadriaticum sp. nov., a zooxanthella: taxonomy, life cycle, and morphology. J. Protozool. 9:45-52. https://doi.org/10.1111/j.1550-7408.1962.tb02579.x
  13. Glibert, P. M., Burkholder, J. M., Kana, T. M., Alexander, J., Skelton, H. & Shilling, C. 2009. Grazing by Karenia brevis on Synechococcus enhances its growth rate and may help to sustain blooms. Aquat. Microb. Ecol. 55:17-30. https://doi.org/10.3354/ame01279
  14. Gomez, F. 2012a. A checklist and classification of living dinoflagellates (Dinoflagellata, Alveolata). CICIMAR Oceanides 27:65-140.
  15. Gomez, F. 2012b. A quantitative review of the lifestyle, habitat and trophic diversity of dinoflagellates (Dinoflagellata, Alveolata). Syst. Biodivers. 10:267-275. https://doi.org/10.1080/14772000.2012.721021
  16. 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
  17. Hansen, G. & Daugbjerg, N. 2009. Symbiodinium natans sp. nov.: a "free-living" dinoflagellate from Tenerife (northeast-Atlantic Ocean). J. Phycol. 45:251-263. https://doi.org/10.1111/j.1529-8817.2008.00621.x
  18. Hansen, G., Daugbjerg, N. & Henriksen, P. 2007. Baldinia anauniensis gen. et sp. nov.: a 'new' dinoflagellate from Lake Tovel, N. Italy. Phycologia 46:86-108. https://doi.org/10.2216/0031-8884(2007)46[86:BAGESN]2.0.CO;2
  19. Hansen, G., Moestrup, O. & Roberts, K. R. 1996. Fine structural observations on Gonyaulax spinifera (Dinophyceae), with special emphasis on the flagellar apparatus. Phycologia 35:354-366. https://doi.org/10.2216/i0031-8884-35-4-354.1
  20. Hansen, P. J. 2011. The role of photosynthesis and food uptake for the growth of marine mixotrophic dinoflagellates. J. Eukaryot. Microbiol. 58:203-214. https://doi.org/10.1111/j.1550-7408.2011.00537.x
  21. Horiguchi, T. & Pienaar, R. N. 1994a. Gymnodinium natalense sp. nov. (Dinophyceae), a new tide pool dinoflagellate from South Africa. Jpn. J. Phycol. 42:21-28.
  22. Horiguchi, T. & Pienaar, R. N. 1994b. Ultrastructure and ontogeny of a new type of eyespot in dinoflagellates. Protoplasma 179:142-150. https://doi.org/10.1007/BF01403952
  23. Horiguchi, T. & Sukigara, C. 2005. Pyramidodinium atrofuscum gen. et sp. nov. (Dinophyceae), a new marine sanddwelling coccoid dinoflagellate from tropical waters. Phycol. Res. 53:247-254. https://doi.org/10.1111/j.1440-183.2005.00392.x
  24. Huelsenbeck, J. P. & Ronquist, F. 2001. MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 17:754-755. https://doi.org/10.1093/bioinformatics/17.8.754
  25. Jeong, H. J., Lee, S. Y., Kang, N. S., Yoo, Y. D., Lim, A. S., Lee, M. J., Kim, H. S., Yih, W., Yamashita, H. & LaJeunesse, T. C. 2014. Genetics and morphology characterize the dinoflagellate Symbiodinium voratum, n. sp., (Dinophyceae) as the sole representative of Symbiodinium clade E. J. Eukaryot. Microbiol. 61:75-94. https://doi.org/10.1111/jeu.12088
  26. Jeong, H. J., Shim, J. H., Kim, J. S., Park, J. Y., Lee, C. W. & Lee. Y. 1999. Feeding by the mixotrophic thecate dinoflagellate Fragilidium cf. mexicanum on red-tide and toxic dinoflagellates. Mar. Ecol. Prog. Ser. 176:263-277. https://doi.org/10.3354/meps176263
  27. Jeong, H. J., Yoo, Y. D., Kim, J. S., Seong, K. A., Kang, N. S. & Kim, T. H. 2010. Growth, feeding, and ecological roles of the mixotrophic and heterotrophic dinoflagellates in marine planktonic food webs. Ocean. Sci. J. 45:65-91. https://doi.org/10.1007/s12601-010-0007-2
  28. Jeong, H. J., Yoo, Y. D., Lee, K. H., Kim, T. H., Seong, K. A., Kang, N. S., Lee, S. Y., Kim, J. S., Kim, S. & Yih, W. H. 2013. Red tides in Masan Bay, Korea in 2004-2005: I. Daily variations in the abundance of red-tide organisms and environmental factors. Harmful Algae 30(Suppl. 1):S75-S88. https://doi.org/10.1016/j.hal.2013.10.008
  29. Kang, N. S., Jeong, H. J., Moestrup, O. & Park, T. G. 2011a. Gyrodiniellum shiwhaense n. gen., n. sp., a new planktonic heterotrophic dinoflagellate from the coastal waters of western Korea: morphology and ribosomal DNA gene sequence. J. Eukaryot. Microbiol. 58:284-309. https://doi.org/10.1111/j.1550-7408.2011.00544.x
  30. Kang, N. S., Jeong, H. J., Moestrup, O., Shin, W., Nam, S. W., Park, J. Y., de Salas, M. F., Kim, K. W. & Noh, J. H. 2010. Description of a new planktonic mixotrophic dinoflagellate Paragymnodinium shiwhaense n. gen., n. sp. from the coastal waters off western Korea: morphology, pigments, and ribosomal DNA gene sequence. J. Eukaryot. Microbiol. 57:121-144. https://doi.org/10.1111/j.1550-7408.2009.00462.x
  31. Kang, N. S., Jeong, H. J., Yoo, Y. D., Yoon, E. Y., Lee, K. H., Lee, K. & Kim, G. 2011b. Mixotrophy in the newly described phototrophic dinoflagellate Woloszynskia cincta from western Korean waters: feeding mechanism, prey species, and effect of prey concentration. J. Eukaryot. Microbiol. 58:152-170. https://doi.org/10.1111/j.1550-7408.2011.00531.x
  32. Kang, N. S., Lee, K. H., Jeong, H. J., Yoo, Y. D., Seong, K. A., Potvin, E., Hwang, Y. J. & Yoon, E. Y. 2013. Red tides in Shiwha Bay, western Korea: a huge dike and tidal power plant established in a semi-enclosed embayment system. Harmful Algae 30(Suppl. 1):S114-S130. https://doi.org/10.1016/j.hal.2013.10.011
  33. Kremp, A., Elbrachter, M., Schweikert, M., Wolny, J. L. & Gottschling, M. 2005. Woloszynskia halophila (Biecheler) comb. nov.: a bloomforming cold-water dinoflagellate co-occurring with Scrippsiella hangoei (Dinophyceae) in the Baltic Sea. J. Phycol. 41:629-642. https://doi.org/10.1111/j.1529-8817.2005.00070.x
  34. Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., Lopez, R., Thompson, J. D., Gibson, T. J. & Higgins, D. G. 2007. Clustal W and clustal X version 2.0. Bioinformatics 23:2947-2948. https://doi.org/10.1093/bioinformatics/btm404
  35. Lee, H., Park, K. T., Lee, K., Jeong, H. J. & Yoo, Y. D. 2012. Prey-dependent retention of dimethylsulfoniopropionate (DMSP) by mixotrophic dinoflagellates. Environ. Microbiol. 14:605-616. https://doi.org/10.1111/j.1462-2920.2011.02600.x
  36. 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. J. Parasitol. 93:1006-1015. https://doi.org/10.1645/GE-3585.1
  37. Loeblich, A. R. & Sherley, J. L. 1979. Observations on the theca of the motile phase of free-living and symbiotic isolates of Zooxanthella microadriatica (Freudenthal) comb. nov. J. Mar. Biol. Assoc. U. K. 59:195-205. https://doi.org/10.1017/S0025315400046270
  38. Logares, R., Shalchian-Tabrizi, K., Boltovskoy, A. & Rengefors, K. 2007. Extensive dinoflagellate phylogenies indicate infrequent marine-freshwater transitions. Mol. Phylogenet. Evol. 45:887-903. https://doi.org/10.1016/j.ympev.2007.08.005
  39. Lohmann, H. 1908. Untersuchungen zur Feststellung des vollstandigen Gehaltes des Meeres an Plankton. Druck von Schmidt & Klaunig, Kiel, 370 pp.
  40. Lom, J. 1981. Fish invading dinoflagellates: a synopsis of existing and newly proposed genera. Folia Parasitol. 28:3-11.
  41. Lom, J. & Schubert, G. 1983. Ultrastructural study of Piscinoodinium pillulare (Schaperclaus, 1954) Lom, 1981 with special emphasis on its attachment to the fish host. J. Fish Dis. 6:411-428. https://doi.org/10.1111/j.1365-2761.1983.tb00096.x
  42. Luo, Z., Yang, W., Xu, B. & Gu, H. 2013. First record of Biecheleria cincta (Dinophyceae) from Chinese coasts, with morphological and molecular characterization of the strains. Chin. J. Oceanol. Limnol. 31:835-845. https://doi.org/10.1007/s00343-013-2315-8
  43. McNeill, J., Barrie, F. R., Buck, W. R., Demoulin, V., Greuter, W., Hawksworth, D. L., Herendeen, P. S., Knapp, S., Marhold, K., Prado, J., Prud'homme van Reine, W. F., Smith, G. F., Wiersema, J. H. & Turland, N. J. 2012. International code of nomenclature for algae, fungi, and plants (Melbourne code). Koeltz Scientific Books, Konigstein, 208 pp.
  44. Moestrup, O. & Daugbjerg, N. 2007. On dinoflagellate phylogeny and classification. In Brodie, J. & Lewis, J. (Eds.) Unravelling the Algae: The Past, Present, and Future of Algae Systematics. Systematics Association Special Volumes 75. CRC Press, Boca Raton, FL, pp. 215-230.
  45. Moestrup, O., Hansen, G. & Daugbjerg, N. 2008. Studies on woloszynskioid dinoflagellates III: on the structure and phylogeny of Borghiella dodgei gen. et sp. nov., a cold-water species from Lake Tovel, N. Italy, and on B. tenuissima comb. nov. (syn. Woloszynskia tenuissima). Phycologia 47:54-78. https://doi.org/10.2216/07-32.1
  46. Moestrup, O., Lindberg, K. & Daugbjerg, N. 2009a. Studies on woloszynskioid dinoflagellates. IV. The genus Biecheleria gen. nov. Phycol. Res. 57:203-220. https://doi.org/10.1111/j.1440-1835.2009.00540.x
  47. Moestrup, O., Lindberg, K. & Daugbjerg, N. 2009b. Studies on woloszynskioid dinoflagellates. V. Ultrastructure of Biecheleriopsis gen. nov., with description of Biecheleriopsis adriatica sp. nov. Phycol. Res. 57:221-237. https://doi.org/10.1111/j.1440-1835.2009.00541.x
  48. Montresor, M., Procaccini, G. & Stoecker, D. K. 1999. Polarella glacialis gen. nov., sp. nov. (Dinophyceae): Suessiaceae are still alive!. J. Phycol. 35:186-197. https://doi.org/10.1046/j.1529-8817.1999.3510186.x
  49. Park, J., Jeong, H. J., Yoo, Y. D. & Yoon, E. Y. 2013. Mixotrophic dinoflagellate red tides in Korean waters: distribution and ecophysiology. Harmful Algae 30(Suppl. 1):S28-S40. https://doi.org/10.1016/j.hal.2013.10.004
  50. Pascher, A. 1914. Uber Flagellaten und Algen. Berichte der Deutschen Botanischen Gesellschaft 32:136-160.
  51. Ronquist, F. & Huelsenbeck, J. P. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572-1574. https://doi.org/10.1093/bioinformatics/btg180
  52. Sanders, R. W. 2011. Alternative nutritional strategies in protists: symposium introduction and a review of freshwater protists that combine photosynthesis and heterotrophy. J. Eukaryot. Microbiol. 58:181-184. https://doi.org/10.1111/j.1550-7408.2011.00543.x
  53. Seong, K. A. & Jeong, H. J. 2013. Interactions between marine bacteria and red tide organisms in Korean waters. Algae 28:297-305. https://doi.org/10.4490/algae.2013.28.4.297
  54. Siano, R., Kooistra, W. H. C. F., Montresor, M. & Zingone, A. 2009. Unarmoured and thin-walled dinoflagellates from the Gulf of Naples, with the description of Woloszynskia cincta sp. nov. (Dinophyceae, Suessiales). Phycologia 48:44-65. https://doi.org/10.2216/08-61.1
  55. Siano, R., Montresor, M., Probert, I., Not, F. & de Vargas, C. 2010. Pelagodinium gen. nov. and P. beii comb. nov., a dinoflagellate symbiont of planktonic foraminifera. Protist 161:385-399. https://doi.org/10.1016/j.protis.2010.01.002
  56. Spurr, A. R. 1969. A low-viscosity epoxy resin embedding medium for electron microscopy. J. Ultrastruct. Res. 26:31-43. https://doi.org/10.1016/S0022-5320(69)90033-1
  57. Stamatakis, A. 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688-2690. https://doi.org/10.1093/bioinformatics/btl446
  58. Stoecker, D., Tillmann, U. & Graneli, E. 2006. Phagotrophy in harmful algae. In Graneli, E. & Turner, J. T. (Eds.) Ecology of Harmful Algae: Ecological Studies. Vol. 189. Springer Verlag, Heidelberg, pp. 177-187.
  59. Takahashi, K., Sarai, C. & Iwataki, M. 2014. Morphology of two marine woloszynskioid dinoflagellates, Biecheleria brevisulcata sp. nov. and Biecheleriopsis adriatica (Suessiaceae, Dinophyceae), from Japanese coasts. Phycologia 53:52-65. https://doi.org/10.2216/13-192.1
  60. Tamura, K., Dudley, J., Nei, M. & Kumar, S. 2007. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24:1596-1599. https://doi.org/10.1093/molbev/msm092
  61. Yoo, Y. D., Jeong, H. J., Kim, J. S., Kim, T. H., Kim, J. H., Seong, K. A., Lee, S. H., Kang, N. S., Park, J. W., Park, J., Yoon, E. Y. & Yih, W. H. 2013. Red tides in Masan Bay, Korea in 2004-2005: II. Daily variations in the abundance of heterotrophic protists and their grazing impact on red-tide organisms. Harmful Algae 30(Suppl. 1):S89-S101. https://doi.org/10.1016/j.hal.2013.10.009
  62. Zapata, M., Rodriguez, F. & Garrido, J. L. 2000. Separation of chlorophylls and carotenoids from marine phytoplankton: a new HPLC method using a reversed phase C8 column and pyridine-containing mobile phases. Mar. Ecol. Prog. Ser. 195:29-45. https://doi.org/10.3354/meps195029

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