Development of an automatic system for cultivating the bioluminescent heterotrophic dinoflagellate Noctiluca scintillans on a 100-liter scale |
You, Ji Hyun
(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) Park, Sang Ah (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University) Ok, Jin Hee (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University) Kang, Hee Chang (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University) Eom, Se Hee (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University) Lim, An Suk (Division of Life Science & Plant Molecular Biology and Biotechnology Research Center, Gyeongsang National University) |
1 | Rohr, J., Latz, M. I., Fallon, S., Nauen, J. C. & Hendricks, E. 1998. Experimental approaches towards interpreting dolphin-stimulated bioluminescence. J. Exp. Biol. 201: 1447-1460. DOI |
2 | Spilling, K., Olli, K., Lehtoranta, J., Kremp, A., Tedesco, L., Tamelander, T., Klais, R., Peltonen, H. & Tamminen, T. 2018. Shifting diatom: dinoflagellate dominance during spring bloom in the Baltic Sea and its potential effects on biogeochemical cycling. Front. Mar. Sci. 5:327. DOI |
3 | Stauffer, B. A., Gellene, A. G., Rico, D., Sur, C. & Caron, D. A. 2017. Grazing of the heterotrophic dinoflagellate Noctiluca scintillans on dinoflagellate and raphidophyte prey. Aquat. Microb. Ecol. 80:193-207. DOI |
4 | Kimor, B. 1979. Predation by Noctiluca miliaris Souriray on Acartia tonsa Dana eggs in the inshore waters of southern California. Limnol. Oceanogr. 24:568-572. DOI |
5 | Sellers, C. G., Gast, R. J. & Sanders, R. W. 2014. Selective feeding and foreign plastid retention in an Antarctic dinoflagellate. J. Phycol. 50:1081-1088. DOI |
6 | Bityukov, E. P. 1971. Bioluminescence in the wake current in the Atlantic Ocean and Mediterranean Sea. Okean 11:127-133. |
7 | Coats, D. W. 1999. Parasitic life styles of marine dinoflagellates. J. Eukaryot. Microbiol. 46:402-409. DOI |
8 | Kiorboe, T. & Titelman, J. 1998. Feeding, prey selection and prey encounter mechanisms in the heterotrophic dinoflagellate Noctiluca scintillans. J. Plankton Res. 20:1615-1636. DOI |
9 | Lee, S. Y., Jeong, H. J., Kang, H. C., Ok, J. H., You, J. H., Park, S. A. & Eom, S. H. 2021. Comparison of the spatial-temporal distributions of the heterotrophic dinoflagellates Gyrodinium dominans, G. jinhaense, and G. moestrupii in Korean coastal waters. Algae 36:37-50. DOI |
10 | Lim, A. S., Jeong, H. J., Jang, T. Y., Yoo, Y. D., Kang, N. S., Yoon, E. Y. & Kim, G. H. 2014. Feeding by the newly described heterotrophic dinoflagellate Stoeckeria changwonensis: a comparison with other species in the family Pfiesteriaceae. Harmful Algae 36:11-21. DOI |
11 | Sugawara, T., Yamashita, K., Sakai, S., Asai, A., Nagao, A., Shiraishi, T., Imai, I. & Hirata, T. 2007. Induction of apoptosis in DLD-1 human colon cancer cells by peridinin isolated from the dinoflagellate, Heterocapsa triquetra. Biosci. Biotechnol. Biochem. 71:1069-1072. DOI |
12 | Sweeney, B. M. 1971. Laboratory studies of a green Noctiluca from New Guinea. J. Phycol. 7:53-58. |
13 | Tada, K., Pithakpol, S. & Montani, S. 2004. Seasonal variation in the abundance of Noctiluca scintillans in the Seto Inland Sea, Japan. Plankton Biol. Ecol. 51:7-14. |
14 | Tarasov, N. I. 1956. Marine luminescence. Naval Oceanographic Office, Report No. NOOT-21. National Space Technology Laboratories Station, Bay St. Louis, MO, 183 pp. |
15 | Uhlig, G. & Sahling, G. 1990. Long-term studies on Noctiluca scintillans in the German Bight population dynamics and red tide phenomena 1968-1988. Neth. J. Sea Res. 25:101-112. DOI |
16 | Tett, P. B. 1971. The relation between dinoflagellates and the bioluminescence of sea water. J. Mar. Biol. Assoc. U. K. 51:183-206. DOI |
17 | Thomas, W. H. & Gibson, C. H. 1990. Quantified small-scale turbulence inhibits a red tide dinoflagellate, Gonyaulax polyedra Stein. Deep Sea Res. Part A Oceanogr. Res. Pap. 37:1583-1593. DOI |
18 | Turkoglu, M. 2013. Red tides of the dinoflagellate Noctiluca scintillans associated with eutrophication in the Sea of Marmara (the Dardanelles, Turkey). Oceanologia 55:709-732. DOI |
19 | Valiadi, M., de Rond, T., Amorim, A., Gittins, J. R., Gubili, C., Moore, B. S., Iglesias-Rodriguez, D. & Latz, M. I. 2019. Molecular and biochemical basis for the loss of bioluminescence in the dinoflagellate Noctiluca scintillans along the west coast of the USA. Limnol. Oceanogr. 64:2709-2724. DOI |
20 | Valiadi, M. & Iglesias-Rodriguez, D. 2013. Understanding bioluminescence in dinoflagellates: how far have we come? Microorganisms 1:3-25. DOI |
21 | Valiadi, M. & Iglesias-Rodriguez, M. D. 2014. Diversity of the luciferin binding protein gene in bioluminescent dinoflagellates: insights from a new gene in Noctiluca scintillans and sequences from Gonyaulacoid genera. J. Eukaryot. Microbiol. 61:134-145. DOI |
22 | Loder, M. G. J., Kraberg, A. C., Aberle, N., Peters, S. & Wiltshire, K. H. 2012. Dinoflagellates and ciliates at Helgoland roads, North Sea. Helgol. Mar. Res. 66:11-23. DOI |
23 | Williams, T. M. & Kooyman, G. L. 1985. Swimming performance and hydrodynamic characteristics of harbor seals Phoca vitulina. Physiol. Zool. 58:576-589. DOI |
24 | Wynn, J. P. & Ratledge, C. 2005. Oils from microorganisms. In Shahidi, F. (Ed.) Bailey's Industrial Oil and Fat Products. John Wiley & Sons, Hoboken, NJ, pp. 121-153. |
25 | 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. DOI |
26 | Johnson, K. B. & Shanks, A. L. 2003. Low rates of predation on planktonic marine invertebrate larvae. Mar. Ecol. Prog. Ser. 248:125-139. DOI |
27 | Lee, K. H., Jeong, H. J., Yoon, E. Y., Jang, S. H., Kim, H. S. & Yih, W. 2014. Feeding by common heterotrophic dinoflagellates and a ciliate on the red-tide ciliate Mesodinium rubrum. Algae 29:153-163. DOI |
28 | Lim, A. S., Jeong, H. J., Kim, S. J. & Ok, J. H. 2018. Amino acids profiles of six dinoflagellate species belonging to diverse families: possible use as animal feeds in aquaculture. Algae 33:279-290. DOI |
29 | Lim, A. S., Jeong, H. J., You, J. H. & Park, S. A. 2020. Semicontinuous cultivation of the mixotrophic dinoflagellate Gymnodinium smaydae, a new promising microalga for omega-3 production. Algae 35:277-292. DOI |
30 | Miyaguchi, H., Fujiki, T., Kikuchi, T., Kuwahara, V. S. & Toda, T. 2006. Relationship between the bloom of Noctiluca scintillans and environmental factors in the coastal waters of Sagami Bay, Japan. J. Plankton Res. 28:313-324. DOI |
31 | Morin, J. G. 1983. Coastal bioluminescence: patterns and functions. Bull. Mar. Sci. 33:787-817. |
32 | Nakamura, Y. 1998. Growth and grazing of a large heterotrophic dinoflagellate, Noctiluca scintillans, in laboratory cultures. J. Plankton Res. 20:1711-1720. DOI |
33 | Glibert, P. M., Burkholder, J. M. & Kana, T. M. 2012. Recent insights about relationships between nutrient availability, forms, and stoichiometry, and the distribution, ecophysiology, and food web effects of pelagic and benthic Prorocentrum species. Harmful Algae 14:231-259. DOI |
34 | Davy, S. K., Allemand, D. & Weis, V. M. 2012. Cell biology of cnidarian-dinoflagellate symbiosis. Microbiol. Mol. Biol. Rev. 76:229-261. DOI |
35 | Berdalet, E. 1992. Effects of turbulence on the marine dinoflagellate Gymnodinium nelsonii. J. Phycol. 28:267-272. DOI |
36 | Buskey, E. J. 1995. Growth and bioluminescence of Noctiluca scintillans on varying algal diets. J. Plankton Res. 17:29-40. DOI |
37 | Buskey, E. J., Strom, S. & Coulter, C. 1992. Biolumiscence of heterotrophic dinoflagellates from Texas coastal waters. J. Exp. Mar. Biol. Ecol. 159:37-49. DOI |
38 | Jeong, H. J. & Lim, A. S. 2020. Method and system for continuous mass culture for mixotrophic dinoflagellates. Patent no. KR102064718B1. Korean Intellectual Property Office, Daejeon. |
39 | Harrison, P. J., Furuya, K., Glibert, P. M., Xu, J., Liu, H. B., Yin, K., Lee, J. H. W., Anderson, D. M., Gowen, R., Al-Azri, A. R. & Ho, A. Y. T. 2011. Geographical distribution of red and green Noctiluca scintillans. Chin. J. Oceanol. Limnol. 29:807-831. DOI |
40 | Jang, S. H., Jeong, H. J. & Kwon, J. E. 2017. High contents of eicosapentaenoic acid and docosahexaenoic acid in the mixotrophic dinoflagellate Paragymnodinium shiwhaense and identification of putative omega-3 biosynthetic genes. Algal Res. 25:525-537. DOI |
41 | Jacobson, D. M. & Anderson, D. M. 1996. Widespread phagocytosis of ciliates and other protists by marine mixotrophic and heterotrophic thecate dinoflagellates. J. Phycol. 32:279-285. DOI |
42 | Eom, S. H., Jeong, H. J., Ok, J. H., Park, S. A., Kang, H. C., You, J. H., Lee, S. Y., Yoo, Y. D., Lim, A. S. & Lee, M. J. 2021. Interactions between common heterotrophic protists and the dinoflagellate Tripos furca: implication on the long duration of its red tides in the South Sea of Korea in 2020. Algae 36:25-36. DOI |
43 | Guillard, R. R. & Ryther, J. H. 1962. Studies of marine planktonic diatoms: I. Cyclotella nana Hustedt, and Detonula confervacea (Cleve) Gran. Can. J. Microbiol. 8:229-239. DOI |
44 | Gupta, P. L., Lee, S. -M. & Choi, H. -J. 2015. A mini review: photobioreactors for large scale algal cultivation. World J. Microbiol. Biotechnol. 31:1409-1417. DOI |
45 | You, J. H., Jeong, H. J., Kang, H. C., Ok, J. H., Park, S. A. & Lim, A. S. 2020. Feeding by common heterotrophic protist predators on seven Prorocentrum species. Algae 35:61-78. DOI |
46 | Hastings, J. W. 1975. Dinoflagellate bioluminescence: molecular mechanisms and circadian control. In Lo Cicero, V. R. (Ed.) Proc. First Int. Conf. Toxic Dinoflagellate Blooms, The Massachusetts Science and Technology Foundation, Wakefield, pp. 235-248. |
47 | Jeong, H. J. 1995. The interactions between microzooplanktonic grazers and dinoflagellates causing red tides in the open coastal waters off southern California. Ph.D. dissertation, University of California, San Diego, CA, USA, 139 pp. |
48 | Jeong, H. J., Kang, H. C., Lim, A. S., Jang, S. H., Lee, K., Lee, S. Y., Ok, J. H., You, J. H., Kim, J. H., Lee, K. H., Park, S. A., Eom, S. H., Yoo, Y. D. & Kim, K. Y. 2021. Feeding diverse prey as an excellent strategy of mixotrophic dinoflagellates for global dominance. Sci. Adv. 7:eabe4214. DOI |
49 | Jeong, H. J., Yoo, Y. D., Kang, N. S., Lim, A. S., Seong, K. A., Lee, S. Y., Lee, M. J., Lee, K. H., Kim, H. S., Shin, W., Nam, S. W., Yih, W. & Lee, K. 2012. Heterotrophic feeding as a newly identified survival strategy of the dinoflagellate Symbiodinium. Proc. Natl. Acad. Sci. U. S. A. 109:12604-12609. DOI |
50 | 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. DOI |
51 | Park, S. A., Jeong, H. J., Ok, J. H., Kang, H. C., You, J. H., Eom, S. H., Yoo, Y. D. & Lee, M. J. 2021b. Bioluminescence capability and intensity in the dinoflagellate Alexandrium species. Algae 36:299-314. DOI |
52 | Zhang, S., Liu, H., Guo, C. & Harrison, P. J. 2016. Differential feeding and growth of Noctiluca scintillans on monospecific and mixed diets. Mar. Ecol. Prog. Ser. 549:27-40. DOI |
53 | Ok, J. H., Jeong, H. J., Kang, H. C., Park, S. A., Eom, S. H., You, J. H. & Lee, S. Y. 2021. Ecophysiology of the kleptoplastidic dinoflagellate Shimiella gracilenta: I. spatiotemporal distribution in Korean coastal waters and growth and ingestion rates. Algae 36:263-283. DOI |
54 | Onodera, K. -I., Konishi, Y., Taguchi, T., Kiyoto, S. & Tominaga, A. 2014. Peridinin from the marine symbiotic dinoflagellate, Symbiodinium sp., regulates eosinophilia in mice. Mar. Drugs 12:1773-1787. DOI |
55 | 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. DOI |
56 | Park, S. A., Jeong, H. J., Ok, J. H., Kang, H. C., You, J. H., Eom, S. H. & Park, E. C. 2021a. Interactions between the kleptoplastidic dinoflagellate Shimiella gracilenta and several common heterotrophic protists. Front. Mar. Sci. 8:738547. DOI |
57 | Jerney, J. & Spilling, K. 2018. Large scale cultivation of microalgae: open and closed systems. In Spilling, K. (Ed.) Biofuels from Algae: Methods and Protocols. Humana Press, New York, NY, pp. 1-8. |
58 | Jeong, H. J., You, J. H., Lee, K. H., Kim, S. J. & Lee, S. Y. 2018. Feeding by common heterotrophic protists on the mixotrophic alga Gymnodinium smaydae (Dinophyceae), one of the fastest growing dinoflagellates. J. Phycol. 54:734-743. DOI |