ALGAE

The Korean Society of Phycology (한국조류학회(藻類))
권호 표지
DOI QR코드

DOI QR Code

Morphological and genetic characterization and the nationwide distribution of the phototrophic dinoflagellate Scrippsiella lachrymosa in the Korean waters

  • Lee, Sung Yeon (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University) ;
  • Jeong, Hae Jin (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University) ;
  • You, Ji Hyun (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University) ;
  • Kim, So Jin (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University)
  • Received : 2018.01.09
  • Accepted : 2018.03.04
  • Published : 2018.03.15
Download PDF
⟨ Previous Next ⟩

Abstract

The phototrophic dinoflagellate genus Scrippsiella is known to have a worldwide distribution. Here, we report for the first time, the occurrence of Scrippsiella lachrymosa in Korean waters. Unlike the other stains of S. lachrymosa whose cultures had been established from cysts in the sediments, the clonal culture of the Korean strain of S. lachrymosa was established from motile cells. When the sulcal plates of S. lachrymosa, which have not been fully described to date, were carefully examined using scanning electron microscopy, the Korean strain of S. lachrymosa clearly exhibited the anterior sulcal plate (s.a.), right sulcal plate (s.d.), left sulcal plate (s.s.), median sulcal plate (s.m.), and posterior sulcal plate (s.p.). When properly aligned, the large subunit (LSU) rDNA sequence of the Korean strain of S. lachrymosa was ca. 1% different from those of two Norwegian strains of S. lachrymosa, the only strains for which LSU sequences have been reported. The internal transcribed spacer (ITS) rDNA sequence of the Korean strain of S. lachrymosa was also ca. 1% different from those of the Scottish and Chinese strains and 3% different from those of the Canadian, German, Greek, and Portuguese strains. Thus, the Korean S. lachrymosa strain has unique LSU and ITS sequences. The abundances of S. lachrymosa in the waters of 28 stations, located in the East, West, and South Sea of Korea, were quantified in four seasons from January 2016 to October 2017, using quantitative real-time polymerase chain reaction method and newly designed specific primer-probe sets. Its abundances were >$0.1cells\;mL^{-1}$ at eight stations in January and March 2016 and March 2017, and its highest abundance in Korean waters was $26cells\;mL^{-1}$. Thus, S. lachrymosa has a nationwide distribution in Korean waters as motile cells.

Keywords

References

  1. Anderson, D. M., Alpermann, T. J., Cembella, A. D., Collos, Y., Masseret, E. & Montresor, M. 2012. The globally distributed genus Alexandrium: multifaceted roles in marine ecosystems and impacts on human health. Harmful Algae 14:10-35. https://doi.org/10.1016/j.hal.2011.10.012
  2. Balech, E. 1959. Two new genera of dinoflagellates from California. Biol. Bull. 116:195-203. https://doi.org/10.2307/1539204
  3. D'Onofrio, G., Marino, D., Bianco, L., Busico, E. & Montresor, M. 1999. Toward an assessment on the taxonomy of dinoflagellates that produce calcareous cysts (Calciodinelloideae, Dinophyceae): a morphological and molecular approach. J. Phycol. 35:1063-1078. https://doi.org/10.1046/j.1529-8817.1999.3551063.x
  4. 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. Sheridan Press, Hanover, PA, 351 pp.
  5. Giovannoni, S. J., DeLong, E. F., Olsen, G. J. & Pace, N. R. 1988. Phylogenetic group-specific oligodeoxynucleotide probes for identification of single microbial cells. J. Bacteriol. 170:720-726. https://doi.org/10.1128/jb.170.2.720-726.1988
  6. Glibert, P. M., Anderson, D. M., Gentein, P., Graneli, E. & Sellner, K. G. 2005. The global, complex phenomena of harmful algal blooms. Oceanography 18:136-147.
  7. Gomez, F. 2003. Checklist of Mediterranean free-living dinoflagellates. Bot. Mar. 46:215-242.
  8. Gottschling, M. & Kirsch, M. 2009. Annotated list of Scandinavian calcareous dinoflagellates collected in fall 2003. Berl. Palaobiologische Abh. 10:193-198.
  9. Gottschling, M., Knop, R., Plotner, J., Kirsch, M., Willems, H. & Keupp, H. 2005. A molecular phylogeny of Scrippsiella sensu lato (Calciodinellaceae, Dinophyta) with interpretations on morphology and distribution. Eur. J. Phycol. 40:207-220. https://doi.org/10.1080/09670260500109046
  10. 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
  11. Head, M. J., Lewis, J. & de Vernal, A. 2006. The cyst of the calcareous dinoflagellate Scrippsiella trifida: resolving the fossil record of its organic wall with that of Alexandrium tamarense. J. Paleontol. 80:1-18.
  12. Hoppenrath, M. 2004. A revised checklist of planktonic diatoms and dinoflagellates from Helgoland (North Sea,German Bight). Helgol. Mar. Res. 58:243-251. https://doi.org/10.1007/s10152-004-0190-6
  13. Jeong, H. J., Lim, A. S., Franks, P. J. S., Lee, K. H., Kim, J. H., Kang, N. S., Lee, M. J., Jang, S. H., Lee, S. Y., Yoon, E. Y., Park, J. Y., Yoo, Y. D., Seong, K. A., Kwon, J. E. & Jang, T. Y. 2015. A hierarchy of conceptual models of red-tide gentheration: nutrition, behavior, and biological interactions. Harmful Algae 47:97-115. https://doi.org/10.1016/j.hal.2015.06.004
  14. Jeong, H. J., Lim, A. S., Lee, K., Lee, M. J., Seong, K. A., Kang, N. S., Jang, S. H., Lee, K. H., Lee, S. Y., Kim, M. O., Kim, J. H., Kwon, J. E., Kang, H. C., Kim, J. S., Yih, W., Shin, K., Jang, P. K., Ryu, J. -H., Kim, S. Y., Park, J. Y. & Kim, K. W. 2017. Ichthyotoxic Cochlodinium polykrikoides red tides offshore in the South Sea, Korea in 2014: I. Temporal variations in three-dimensional distributions of red-tide organisms and environmental factors. Algae 32:101-130. https://doi.org/10.4490/algae.2017.32.5.30
  15. 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
  16. 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. 2013. Red tides in Masan Bay, Korea in 2004-2005, I. Daily variations in the abundance of red-tides organisms and environmental factors. Harmful Algae 30(Suppl. 1):S75-S88. https://doi.org/10.1016/j.hal.2013.10.008
  17. Joyce, L. B., Pitcher, G. C., Du Randt, A. & Monteiro, P. M. S. 2005. Dinoflagellate cysts from surface sediments of Saldanha Bay, South Africa: an indication of the potential risk of harmful algal blooms. Harmful Algae 4:309-318. https://doi.org/10.1016/j.hal.2004.08.001
  18. 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
  19. Kang, N. S., Lee, K. H., Jeong, H. J., Yoo, Y. D., Seong, K. A., Potvin, É., 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
  20. Kibbe, W. A. 2007. OligoCalc: an online oligonucleotide properties calculator. Nucleic Acids Res. 35(Suppl. 2):W43-W46. https://doi.org/10.1093/nar/gkm234
  21. Kuylenstierna, M. & Karlson, B. 2000. Checklist of phytoplankton in Skagerrak-Kattegat. Available from: http://www.smhi.se/oceanografi/oce_info_data/plankton_checklist/ssshome.htm. Accessed Feb 28, 2018.
  22. Lee, S. Y., Jeong, H. J., Seong, K. A., Lim, A. S., Kim, J. H., Lee, K. H., Lee, M. J. & Jang, S. H. 2017. Improved real-time PCR method for quantification of the abundance of all known ribotypes of the ichthyotoxic dinoflagellate Cochlodinium polykrikoides by comparing 4 different preparation methods. Harmful Algae 63:23-31. https://doi.org/10.1016/j.hal.2017.01.006
  23. Lewis, J. 1991. Cyst-theca relationships in Scrippsiella (Dino phyceae) and related orthoperidinioid genera. Bot. Mar. 34:91-106.
  24. Lim, A. S., Jeong, H. J., Seong, K. A., Lee, M. J., Kang, N. S., Jang, S. H., Lee, K. H., Park, J. Y., Jang, T. Y. & Yoo, Y. D. 2017. Ichthyotoxic Cochlodinium polykrikoides red tides offshore in the South Sea, Korea in 2014: II. Heterotrophic protists and their grazing impacts on redtide organisms. Algae 32:199-222. https://doi.org/10.4490/algae.2017.32.8.25
  25. Litaker, R. W., Vandersea, M. W., Kibler, S. R., Reece, K. S., Stokes, N. A., Steidinger, K. A., Millie, D. F., Bendis, B. J., Pigg, R. J. & Tester, P. A. 2003. Identification of Pfiesteria piscicida (Dinophyceae) and Pfiesteria-like organisms using internal transcribed spacer-specific PCR assays. J. Phycol. 39:754-761. https://doi.org/10.1046/j.1529-8817.2003.02112.x
  26. Loeblich, A. R. III. 1965. Dinoflagellate nomenclature. Taxon 14:15-18. https://doi.org/10.2307/1216704
  27. Luo, Z., Mertens, K. N., Bagheri, S., Aydin, H., Takano, Y., Matsuoka, K., McCarthy, F. M. G. & Gu, H. 2016. Cyst-theca relationship and phylogenetic positions of Scrippsiella plana sp. nov. and S. spinifera (Peridiniales, Dinophyceae). Eur. J. Phycol. 51:188-202. https://doi.org/10.1080/09670262.2015.1120348
  28. Meier, K. J. S., Janofske, D. & Willems, H. 2002. New calcareous dinoflagellates (Calciodinelloideae) from the Mediterranean Sea. J. Phycol. 38:602-615. https://doi.org/10.1046/j.1529-8817.2002.t01-1-01191.x
  29. Montero, P., Perez-Santos, I., Daneri, G., Gutierrez, M. H., Igor, G., Seguel, R., Purdie, D. & Crawford, D. W. 2017. A winter dinoflagellate bloom drives high rates of primary production in a Patagonian fjord ecosystem. Estuar. Coast. Shelf Sci. 199:105-116. https://doi.org/10.1016/j.ecss.2017.09.027
  30. Nehring, S. 1994. Scrippsiella spp. resting cysts from the German Bight (North Sea): a tool for more complete checklists of dinoflagellates. Neth. J. Sea Res. 33:57-63. https://doi.org/10.1016/0077-7579(94)90051-5
  31. Olli, K. & Anderson, D. M. 2002. High encystment success of the dinoflagellate Scrippsiella cf. lachrymosa in culture experiments. J. Phycol. 38:145-156. https://doi.org/10.1046/j.1529-8817.2002.01113.x
  32. Olli, K., Neubert, M. G. & Anderson, D. M. 2004. Encystment probability and encystment rate: new terms to quantitatively describe formation of resting cysts in planktonic microbial populations. Mar. Ecol. Prog. Ser. 273:43-48. https://doi.org/10.3354/meps273043
  33. Park, J., Jeong, H. J., Yoo, Y. D. & Yoon, E. Y. 2013a. 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
  34. Park, T. G., Lim, W. A., Park, Y. T., Lee, C. K. & Jeong, H. J. 2013b. Economic impact, management and mitigation of red tides in Korea. Harmful Algae 30(Suppl. 1):S131-S143. https://doi.org/10.1016/j.hal.2013.10.012
  35. Persson, A., Smith, B. C., Cyronak, T., Cooper, E. & DiTullio, G. R. 2016. Differences in pigmentation between life cycle stages in Scrippsiella lachrymosa (dinophyceae). J. Phycol. 52:64-74. https://doi.org/10.1111/jpy.12364
  36. Pitcher, G. C. & Joyce, L. B. 2009. Dinoflagellate cyst production on the southern Namaqua shelf of the Benguela upwelling system. J. Plankton Res. 31:865-875. https://doi.org/10.1093/plankt/fbp040
  37. 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
  38. Rozen, S. & Skaletsky, H. 2000. Primer3 on the WWW for general users and for biologist programmers. In Misener, S. & Krawetz, S. A. (Eds.) Bioinformatics Methods and Protocols. Methods in Molecular Biology. Humana Press, Totowa, NJ, pp. 365-386.
  39. Rubino, F., Belmonte, M., Caroppo, C. & Giacobbe, M. 2010. Dinoflagellate cysts from surface sediments of Syracuse Bay (Western Ionian Sea, Mediterranean). Deep-Sea Res. Part II Top. Stud. Oceanogr. 57:243-247. https://doi.org/10.1016/j.dsr2.2009.09.011
  40. Satta, C. T., Angles, S., Garcés, E., Luglie, A., Padedda, B. M. & Sechi, N. 2010. Dinoflagellate cysts in recent sediments from two semi-enclosed areas of the Western Mediterranean Sea subject to high human impact. Deep Sea Res. Part II Top. Stud. Oceanogr. 57:256-267. https://doi.org/10.1016/j.dsr2.2009.09.013
  41. 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 LSU rRNA gene. J. Phycol. 30:999-1011. https://doi.org/10.1111/j.0022-3646.1994.00999.x
  42. Shumway, S. E. & Cembella, A. D. 1993. The impact of toxic algae on scallop culture and fisheries. Rev. Fish. Sci. 1:121-150. https://doi.org/10.1080/10641269309388538
  43. Soehner, S., Zinssmeister, C., Kirsch, M. & Gottschling, M. 2012. Who am I-and if so, how many? Species diversity of calcareous dinophytes (Thoracosphaeraceae, Peridiniales) in the Mediterranean Sea. Org. Divers. Evol. 12:339-348. https://doi.org/10.1007/s13127-012-0109-z
  44. 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
  45. Stoeck, T., Schwarz, M. V. J., Boenigk, J., Schweikert, M., von der Heyden, S. & Behnke, A. 2005. Cellular identity of an 18S rRNA gene sequence clade within the class Kinetoplastea: the novel genus Actuariola gen. nov. (Neobodonida) with description of the type species Actuariola framvarensis sp. nov. Int. J. Syst. Evol. Microbiol. 55:2623-2635. https://doi.org/10.1099/ijs.0.63769-0
  46. 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
  47. Wang, Z., Qi, Y., Chen, J., Xu, N. & Yang, Y. 2006. Phytoplankton abundance, community structure and nutrients in cultural areas of Daya Bay, South China Sea. J. Mar. Syst. 62:85-94. https://doi.org/10.1016/j.jmarsys.2006.04.008
  48. Zinssmeister, C., Soehner, S., Facher, E., Kirsch, M., Meier, K. J. S. & Gottschling, M. 2011. Catch me if you can: the taxonomic identity of Scrippsiella trochoidea (F.Stein) A.R.Loebl. (Thoracosphaeraceae, Dinophyceae). Syst. Biodivers. 9:145-157. https://doi.org/10.1080/14772000.2011.586071

Cited by

  1. Scrippsiella masanensis sp. nov. (Thoracosphaerales, Dinophyceae), a phototrophic dinoflagellate from the coastal waters of southern Korea vol.58, pp.3, 2018, https://doi.org/10.1080/00318884.2019.1568794
  2. Differential feeding by common heterotrophic protists on four Scrippsiella species of similar size vol.55, pp.4, 2018, https://doi.org/10.1111/jpy.12864
  3. Feeding by common heterotrophic protist predators on seven Prorocentrum species vol.35, pp.1, 2018, https://doi.org/10.4490/algae.2020.35.2.28
  4. Structure and environmental drivers of phytoplanktonic resting stage assemblages in the central Mediterranean Sea vol.639, pp.None, 2018, https://doi.org/10.3354/meps13244
  5. Spatial-temporal distributions of the newly described mixotrophic dinoflagellate Gymnodinium smaydae in Korean coastal waters vol.35, pp.3, 2020, https://doi.org/10.4490/algae.2020.35.8.25
  6. Morphology and Phylogeny of Scrippsiella precaria Montresor & Zingone (Thoracosphaerales, Dinophyceae) from Korean Coastal Waters vol.9, pp.2, 2021, https://doi.org/10.3390/jmse9020154
  7. Comparison of the spatial-temporal distributions of the heterotrophic dinoflagellates Gyrodinium dominans, G. jinhaense, and G. moestrupii in Korean coastal waters vol.36, pp.1, 2018, https://doi.org/10.4490/algae.2021.36.3.4