ALGAE

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

DOI QR Code

Lack of mixotrophy in three Karenia species and the prey spectrum of Karenia mikimotoi (Gymnodiniales, Dinophyceae)

  • Jin Hee Ok (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University) ;
  • Hae Jin Jeong (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University) ;
  • An Suk Lim (Division of Life Science, Gyeongsang National University) ;
  • Hee Chang Kang (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University) ;
  • Ji Hyun You (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University) ;
  • Sang Ah Park (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University) ;
  • Se Hee Eom (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University)
  • Received : 2023.01.10
  • Accepted : 2023.02.28
  • Published : 2023.03.15
Download PDF
⟨ Previous Next ⟩

Abstract

Exploring mixotrophy of dinoflagellate species is critical to understanding red-tide dynamics and dinoflagellate evolution. Some species in the dinoflagellate genus Karenia have caused harmful algal blooms. Among 10 Karenia species, the mixotrophic ability of only two species, Karenia mikimotoi and Karenia brevis, has been investigated. These species have been revealed to be mixotrophic; however, the mixotrophy of the other species should be explored. Moreover, although K. mikimotoi was previously known to be mixotrophic, only a few potential prey species have been tested. We explored the mixotrophic ability of Karenia bicuneiformis, Karenia papilionacea, and Karenia selliformis and the prey spectrum of K. mikimotoi by incubating them with 16 potential prey species, including a cyanobacterium, diatom, prymnesiophyte, prasinophyte, raphidophyte, cryptophytes, and dinoflagellates. Cells of K. bicuneiformis, K. papilionacea, and K. selliformis did not feed on any tested potential prey species, indicating a lack of mixotrophy. The present study newly discovered that K. mikimotoi was able to feed on the common cryptophyte Teleaulax amphioxeia. The phylogenetic tree based on the large subunit ribosomal DNA showed that the mixotrophic species K. mikimotoi and K. brevis belonged to the same clade, but K. bicuneiformis, K. papilionacea, and K. selliformis were divided into different clades. Therefore, the presence or lack of a mixotrophic ability in this genus may be partially related to genetic characterizations. The results of this study suggest that Karenia species are not all mixotrophic, varying from the results of previous studies.

Keywords

Acknowledgement

This research was supported by the National Research Foundation funded by the Ministry of Education (NRF-2022R1A6A3A01086348) award to JHO and the National Research Foundation by the Ministry of Science and ICT (NRF-2021M3I6A1091272; NRF-2021R1A2C1093379) award to HJJ.

References

  1. Adolf, J. E., Bachvaroff, T. & Place, A. R. 2008. Can cryptophyte abundance trigger toxic Karlodinium veneficum blooms in eutrophic estuaries? Harmful Algae 8:119-128. https://doi.org/10.1016/j.hal.2008.08.003
  2. Baden, D. G. 1989. Brevetoxins: unique polyether dinoflagellate toxins. FASEB J. 3:1807-1817. https://doi.org/10.1096/fasebj.3.7.2565840
  3. Baohong, C., Kang, W., Huige, G. & Hui, L. 2021. Karenia mikimotoi blooms in coastal waters of China from 1998 to 2017. Estuar. Coast. Shelf Sci. 249:107034.
  4. Benico, G., Takahashi, K., Lum, W. M. & Iwataki, M. 2019. Morphological variation, ultrastructure, pigment composition and phylogeny of the star-shaped dinoflagellate Asterodinium gracile (Kareniaceae, Dinophyceae). Phycologia 58:405-418. https://doi.org/10.1080/00318884.2019.1601948
  5. Bergholtz, T., Daugbjerg, N., Moestrup, O. & Fernandez-Tejedor, M. 2006. On the identity of Karlodinium veneficum and description of Karlodinium armiger sp. nov. (Dinophyceae), based on light and electron microscopy, nuclear-encoded LSU rDNA, and pigment composition. J. Phycol. 42:170-193. https://doi.org/10.1111/j.1529-8817.2006.00172.x
  6. Bockstahler, K. R. & Coats, D. W. 1993. Spatial and temporal aspects of mixotrophy in Chesapeake Bay dinoflagellates. J. Eukaryot. Microbiol. 40:49-60. https://doi.org/10.1111/j.1550-7408.1993.tb04881.x
  7. Boraas, M. E., Estep, K. W., Johnson, P. W. & Sieburth, J. M. 1988. Phagotrophic phototrophs: the ecological significance of mixotrophy. J. Protozool. 35:249-252. https://doi.org/10.1111/j.1550-7408.1988.tb04336.x
  8. Botes, L., Sym, S. D. & Pitcher, G. C. 2003. Karenia cristata sp. nov. and Karenia bicuneiformis sp. nov. (Gymnodiniales, Dinophyceae): two new Karenia species from the South African coast. Phycologia 42:563-571. https://doi.org/10.2216/i0031-8884-42-6-563.1
  9. Boudriga, I., Abdennadher, M., Khammeri, Y., Mahfoudi, M., Quemeneur, M., Hamza, A., Bel Haj Hmida, N., Zouari, A. B. & Hassen, M. B. 2023. Karenia selliformis bloom dynamics and growth rate estimation in the Sfax harbour (Tunisia), by using automated flow cytometry equipped with image in flow, during autumn 2019. Harmful Algae 121:102366.
  10. Brand, L. E., Campbell, L. & Bresnan, E. 2012. Karenia: the biology and ecology of a toxic genus. Harmful Algae 14:156-178. https://doi.org/10.1016/j.hal.2011.10.020
  11. Burkholder, J. M., Glibert, P. M. & Skelton, H. M. 2008. Mixotrophy, a major mode of nutrition for harmful algal species in eutrophic waters. Harmful Algae 8:77-93. https://doi.org/10.1016/j.hal.2008.08.010
  12. Calbet, A., Bertos, M., Fuentes-Grunewald, C., Alacid, E., Figueroa, R., Renom, B. & Garces, E. 2011. Intraspecific variability in Karlodinium veneficum: growth rates, mixotrophy, and lipid composition. Harmful Algae 10:654-667. https://doi.org/10.1016/j.hal.2011.05.001
  13. Cloern, J. E. 2018. Why large cells dominate estuarine phytoplankton. Limnol. Oceanogr. 63:S392-S409. https://doi.org/10.1002/lno.10749
  14. 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
  15. Davidson, K., Miller, P., Wilding, T. A., Shutler, J., Bresnan, E., Kennington, K. & Swan, S. 2009. A large and prolonged bloom of Karenia mikimotoi in Scottish waters in 2006. Harmful Algae 8:349-361. https://doi.org/10.1016/j.hal.2008.07.007
  16. de Salas, M. F., Bolch, C. J. S., Botes, L., Nash, G., Wright, S. W. & Hallegraeff, G. M. 2003. Takayama gen. nov. (Gymnodiniales, Dinophyceae), a new genus of unarmored dinoflagellates with sigmoid apical grooves, including the description of two new species. J. Phycol. 39:1233-1246. https://doi.org/10.1111/j.0022-3646.2003.03-019.x
  17. 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. https://doi.org/10.4490/algae.2021.36.2.22
  18. Fowler, N., Tomas, C., Baden, D., Campbell, L. & Bourdelais, A. 2015. Chemical analysis of Karenia papilionacea. Toxicon 101:85-91. https://doi.org/10.1016/j.toxicon.2015.05.007
  19. 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
  20. Gran-Stadniczenko, S., Egge, E., Hostyeva, V., Logares, R., Eikrem, W. & Edvardsen, B. 2019. Protist diversity and seasonal dynamics in Skagerrak plankton communities as revealed by metabarcoding and microscopy. J. Eukaryot. Microbiol. 66:494-513. https://doi.org/10.1111/jeu.12700
  21. Guillard, R. R. L. & Hargraves, P. E. 1993. Stichochrysis immobilis is a diatom, not a chrysophyte. Phycologia 32:234-236. https://doi.org/10.2216/i0031-8884-32-3-234.1
  22. 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. https://doi.org/10.1139/m62-029
  23. Guiry, M. D. & Guiry, G. M. 2023. AlgaeBase. World-wide electronic publication, National University of Ireland, Galway. Available from: http://www.algaebase.org. Accessed Jan 28, 2023.
  24. Haywood, A. J., Steidinger, K. A., Truby, E. W., Bergquist, P. R., Bergquist, P. L., Adamson, J. & Mackenzie, L. 2004. Comparative morphology and molecular phylogenetic analysis of three new species of the genus Karenia (Dinophyceae) from New Zealand. J. Phycol. 40:165-179. https://doi.org/10.1111/j.0022-3646.2004.02-149.x
  25. He, D., Liu, J., Hao, Q., Ran, L., Zhou, B. & Tang, X. 2016. Interspecific competition and allelopathic interaction between Karenia mikimotoi and Dunaliella salina in laboratory culture. Chin. J. Oceanol. Limnol. 34:301-313. https://doi.org/10.1007/s00343-016-4320-1
  26. Jang, S. H. & Jeong, H. J. 2020. Spatio-temporal distributions of the newly described mixotrophic dinoflagellate Yihiella yeosuensis (Suessiaceae) in Korean coastal waters and its grazing impact on prey populations. Algae 35:45-59. https://doi.org/10.4490/algae.2020.35.2.24
  27. Jang, S. H., Jeong, H. J., Kwon, J. E. & Lee, K. H. 2017. Mixotrophy in the newly described dinoflagellate Yihiella yeosuensis: a small, fast dinoflagellate predator that grows mixotrophically, but not autotrophically. Harmful Algae 62:94-103. https://doi.org/10.1016/j.hal.2016.12.007
  28. Jeong, H. J., Ha, J. H., Park, J. Y., Kim, J. H., Kang, N. S., Kim, S., Kim, J. S., Yoo, Y. D. & Yih, W. H. 2006. Distribution of the heterotrophic dinoflagellate Pfiesteria piscicida in Korean waters and its consumption of mixotrophic dinoflagellates, raphidophytes and fish blood cells. Aquat. Microb. Ecol. 44:263-278. https://doi.org/10.3354/ame044263
  29. Jeong, H. J., Ha, J. H., Yoo, Y. D., Park, J. Y., Kim, J. H., Kang, N. S., Kim, T. H., Kim, H. S. & Yih, W. H. 2007. Feeding by the Pfiesteria-like heterotrophic dinoflagellate Luciella masanensis. J. Eukaryot. Microbiol. 54:231-241. https://doi.org/10.1111/j.1550-7408.2007.00259.x
  30. 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.
  31. Jeong, H. J., Lee, K. H., Yoo, Y. D., Kang, N. S. & Lee, K. 2011. Feeding by the newly described, nematocyst-bearing heterotrophic dinoflagellate Gyrodiniellum shiwhaense. J. Eukaryot. Microbiol. 58:511-524. https://doi.org/10.1111/j.1550-7408.2011.00580.x
  32. 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 generation: nutrition, behavior, and biological interactions. Harmful Algae 47:97-115. https://doi.org/10.1016/j.hal.2015.06.004
  33. Jeong, H. J., Ok, J. H., Lim, A. S., Kwon, J. E., Kim, S. J. & Lee, S. Y. 2016. Mixotrophy in the phototrophic dinoflagellate Takayama helix (family Kareniaceae): predator of diverse toxic and harmful dinoflagellates. Harmful Algae 60:92-106. https://doi.org/10.1016/j.hal.2016.10.008
  34. Jeong, H. J., Park, J. Y., Nho, J. H., Park, M. O., Ha, J. H., Seong, K. A., Jeng, C., Seong, C. N., Lee, K. Y. & Yih, W. H. 2005a. Feeding by red-tide dinoflagellates on the cyanobacterium Synechococcus. Aquat. Microb. Ecol. 41:131-143. https://doi.org/10.3354/ame041131
  35. 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. https://doi.org/10.1073/pnas.1204302109
  36. Jeong, H. J., Yoo, Y. D., Kang, N. S., Rho, J. R., Seong, K. A., Park, J. W., Nam, G. S. & Yih, W. 2010a. Ecology of Gymnodinium aureolum. I. Feeding in western Korean waters. Aquat. Microb. Ecol. 59:239-255. https://doi.org/10.3354/ame01394
  37. Jeong, H. J., Yoo, Y. D., Kim, J. S., Kim, T. H., Kim, J. H., Kang, N. S. & Yih, W. 2004. Mixotrophy in the phototrophic harmful alga Cochlodinium polykrikoides (Dinophycean): prey species, the effects of prey concentration, and grazing impact. J. Eukaryot. Microbiol. 51:563-569. https://doi.org/10.1111/j.1550-7408.2004.tb00292.x
  38. Jeong, H. J., Yoo, Y. D., Kim, J. S., Seong, K. A., Kang, N. S. & Kim, T. H. 2010b. 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
  39. 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
  40. Jeong, H. J., Yoo, Y. D., Park, J. Y., Song, J. Y., Kim, S. T., Lee, S. H., Kim, K. W. & Yih, W. H. 2005b. Feeding by phototrophic red-tide dinoflagellates: five species newly revealed and six species previously known to be mixotrophic. Aquat. Microb. Ecol. 40:133-150. https://doi.org/10.3354/ame040133
  41. Jeong, H. J., Yoo, Y. D., Seong, K. A., Kim, J. H., Park, J. Y., Kim, S., Lee, S. H., Ha, J. H. & Yih, W. H. 2005c. Feeding by the mixotrophic dinoflagellate Gonyaulax polygramma: mechanisms, prey species, effects of prey concentration, and grazing impact. Aquat. Microb. Ecol. 38:249-257. https://doi.org/10.3354/ame038249
  42. Johnson, M. D. 2015. Inducible mixotrophy in the dinoflagellate Prorocentrum minimum. J. Eukaryot. Microbiol. 62:431-443. https://doi.org/10.1111/jeu.12198
  43. Johnson, M. D., Stoecker, D. K. & Marshall, H. G. 2013. Seasonal dynamics of Mesodinium rubrum in Chesapeake Bay. J. Plankton Res. 35:877-893. https://doi.org/10.1093/plankt/fbt028
  44. Jones, R. I. 2000. Mixotrophy in planktonic protists: an overview. Freshw. Biol. 45:219-226. https://doi.org/10.1046/j.1365-2427.2000.00672.x
  45. 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
  46. Kang, N. S., Jeong, H. J., Yoo, Y. D., Yoon, E. Y., Lee, K. H., Lee, K. & Kim, G. 2011. 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
  47. Kempton, J. W., Lewitus, A. J., Deeds, J. R., Law, J. M. & Place, A. R. 2002. Toxicity of Karlodinium micrum (Dinophyceae) associated with a fish kill in a South Carolina brackish retention pond. Harmful Algae 1:233-241. https://doi.org/10.1016/S1568-9883(02)00015-X
  48. Kim, S., Yoon, J. & Park, M. G. 2015. Obligate mixotrophy of the pigmented dinoflagellate Polykrikos lebourae (Dinophyceae, Dinoflagellata). Algae 30:35-47. https://doi.org/10.4490/algae.2015.30.1.035
  49. Lee, K. H., Jeong, H. J., Jang, T. Y., Lim, A. S., Kang, N. S., Kim, J. -H., Kim, K. Y., Park, K. -T. & Lee, K. 2014. Feeding by the newly described mixotrophic dinoflagellate Gymnodinium smaydae: feeding mechanism, prey species, and effect of prey concentration. J. Exp. Mar. Biol. Ecol. 459:114-125. https://doi.org/10.1016/j.jembe.2014.05.011
  50. Lee, K. H., Jeong, H. J., Kwon, J. E., Kang, H. C., Kim, J. H., Jang, S. H., Park, J. Y., Yoon, E. Y. & Kim, J. S. 2016. Mixotrophic ability of the phototrophic dinoflagellates Alexandrium andersonii, A. affine, and A. fraterculus. Harmful Algae 59:67-81. https://doi.org/10.1016/j.hal.2016.09.008
  51. Li, A., Stoecker, D. K. & Adolf, J. E. 1999. Feeding, pigmentation, photosynthesis and growth of the mixotrophic dinoflagellate Gyrodinium galatheanum. Aquat. Microb. Ecol. 19:163-176. https://doi.org/10.3354/ame019163
  52. Li, X., Yan, T., Yu, R. & Zhou, M. 2019. A review of Karenia mikimotoi: bloom events, physiology, toxicity and toxic mechanism. Harmful Algae 90:101702.
  53. Lim, A. S. & Jeong, H. J. 2021. Benthic dinoflagellates in Korean waters. Algae 36:91-109. https://doi.org/10.4490/algae.2021.36.5.31
  54. Lim, A. S., Jeong, H. J. & Ok, J. H. 2019. Five Alexandrium species lacking mixotrophic ability. Algae 34:289-301. https://doi.org/10.4490/algae.2019.34.11.21
  55. Lin, C. -H. M., Lyubchich, V. & Glibert, P. M. 2018. Time series models of decadal trends in the harmful algal species Karlodinium veneficum in Chesapeake Bay. Harmful Algae 73:110-118. https://doi.org/10.1016/j.hal.2018.02.002
  56. Liu, C., Zhang, X. & Wang, X. 2022. DNA metabarcoding data reveals harmful algal-bloom species undescribed previously at the northern Antarctic Peninsula region. Polar Biol. 45:1495-1512. https://doi.org/10.1007/s00300-022-03084-7
  57. Lopez-Cortes, D. J., Nunez Vazquez, E. J., Dorantes-Aranda, J. J., Band-Schmidt, C. J., Hernandez-Sandoval, F. E., Bustillos-Guzman, J. J., Leyva-Valencia, I. & FernandezHerrera, L. J. 2019. The state of knowledge of harmful algal blooms of Margalefidinium polykrikoides (aka Cochlodinium polykrikoides) in Latin America. Front. Mar. Sci. 6:463.
  58. Mansour, J. S. & Anestis, K. 2021. Eco-evolutionary perspectives on mixoplankton. Front. Mar. Sci. 8:666160.
  59. Miles, C. O., Wilkins, A. L., Stirling, D. J. & MacKenzie, A. L. 2003. Gymnodimine C, an isomer of gymnodimine B, from Karenia selliformis. J. Agric. Food Chem. 51:4838-4840. https://doi.org/10.1021/jf030101r
  60. Ok, J. H., Jeong, H. J., Kang, H. C., Park, S. A., Eom, S. H., You, J. H. & Lee, S. Y. 2021a. Ecophysiology of the kleptoplastidic dinoflagellate Shimiella gracilenta: I. spatiotemporal distribution in Korean coastal waters and growth and ingestion rates. Algae 36:263-283. https://doi.org/10.4490/algae.2021.36.11.28
  61. Ok, J. H., Jeong, H. J., Kang, H. C., Park, S. A., Eom, S. H., You, J. H. & Lee, S. Y. 2022. Ecophysiology of the kleptoplastidic dinoflagellate Shimiella gracilenta: II. Effects of temperature and global warming. Algae 37:49-62. https://doi.org/10.4490/algae.2022.37.3.2
  62. Ok, J. H., Jeong, H. J., Lee, S. Y., Park, S. A. & Noh, J. H. 2021b. Shimiella gen. nov. and Shimiella gracilenta sp. nov. (Dinophyceae, Kareniaceae), a kleptoplastidic dinoflagellate from Korean waters and its survival under starvation. J. Phycol. 57:70-91. https://doi.org/10.1111/jpy.13067
  63. Ok, J. H., Jeong, H. J., Lim, A. S. & Lee, K. H. 2017. Interactions between the mixotrophic dinoflagellate Takayama helix and common heterotrophic protists. Harmful Algae 68:178-191. https://doi.org/10.1016/j.hal.2017.08.006
  64. Ok, J. H., Jeong, H. J., Lim, A. S., You, J. H., Kang, H. C., Kim, S. J. & Lee, S. Y. 2019. Effects of light and temperature on the growth of Takayama helix (Dinophyceae): mixotrophy as a survival strategy against photoinhibition. J. Phycol. 55:1181-1195. https://doi.org/10.1111/jpy.12907
  65. Ok, J. H., Jeong, H. J., Lim, A. S., You, J. H., Yoo, Y. D., Kang, H. C., Park, S. A., Lee, M. J. & Eom, S. H. 2023. Effects of intrusion and retreat of deep cold waters on the causative species of red tides offshore in the South Sea of Korea. Mar. Biol. 170:6.
  66. Ok, J. H., Jeong, H. J., You, J. H., Kang, H. C., Park, S. A., Lim, A. S., Lee, S. Y. & Eom, S. H. 2021c. Phytoplankton bloom dynamics in incubated natural seawater: predicting bloom magnitude and timing. Front. Mar. Sci. 8:681252.
  67. Orlova, T. Y., Aleksanin, A. I., Lepskaya, E. V., Efimova, K. V., Selina, M. S., Morozova, T. V., Stonik, I. V., Kachur, V. A., Karpenko, A. A., Vinnikov, K. A., Adrianov, A. V. & Iwataki, M. 2022. A massive bloom of Karenia species (Dinophyceae) off the Kamchatka coast, Russia, in the fall of 2020. Harmful Algae 120:102337.
  68. Park, M. G., Kim, S., Kim, H. S., Myung, G., Kang, Y. G. & Yih, W. 2006. First successful culture of the marine dinoflagellate Dinophysis acuminata. Aquat. Microb. Ecol. 45:101-106. https://doi.org/10.3354/ame045101
  69. Park, S. A., Jeong, H. J., Ok, J. H., Kang, H. C., You, J. H., Eom, S. H., Yoo, Y. D. & Lee, M. J. 2021. Bioluminescence capability and intensity in the dinoflagellate Alexandrium species. Algae 36:299-314. https://doi.org/10.4490/algae.2021.36.12.6
  70. Pierce, R. H., Henry, M. S., Blum, P. C., Lyons, J., Cheng, Y. S., Yazzie, D. & Zhou, Y. 2003. Brevetoxin concentrations in marine aerosol: human exposure levels during a Karenia brevis harmful algal bloom. Bull. Environ. Contam. Toxicol. 70:161-165. https://doi.org/10.1007/s00128-002-0170-y
  71. Rublee, P. A. & Gallegos, C. L. 1989. Use of fluorescently labelled algae (FLA) to estimate microzooplankton grazing. Mar. Ecol. Prog. Ser. 51:221-227. https://doi.org/10.3354/meps051221
  72. Sakamoto, S., Lim, W. A., Lu, D., Dai, X., Orlova, T. & Iwataki, M. 2021. Harmful algal blooms and associated fisheries damage in East Asia: current status and trends in China, Japan, Korea and Russia. Harmful Algae 102:101787.
  73. Selosse, M. -A., Charpin, M. & Not, F. 2017. Mixotrophy everywhere on land and in water: the grand ecart hypothesis. Ecol. Lett. 20:246-263. https://doi.org/10.1111/ele.12714
  74. Sengco, M. R. 2009. Prevention and control of Karenia brevis blooms. Harmful Algae 8:623-628. https://doi.org/10.1016/j.hal.2008.11.005
  75. Shen, A., Xing, X. & Li, D. 2015. Allelopathic effects of Prorocentrum donghaiense and Karenia mikimotoi on each other under different temperature. Thalassas 31:33-49.
  76. Siswanto, E., Ishizaka, J., Tripathy, S. C. & Miyamura, K. 2013. Detection of harmful algal blooms of Karenia mikimotoi using MODIS measurements: a case study of SetoInland Sea, Japan. Remote Sens. Environ. 129:185-196. https://doi.org/10.1016/j.rse.2012.11.003
  77. Skovgaard, A. 1998. Role of chloroplast retention in a marine dinoflagellate. Aquat. Microb. Ecol. 15:293-301. https://doi.org/10.3354/ame015293
  78. Steidinger, K. A. 2009. Historical perspective on Karenia brevis red tide research in the Gulf of Mexico. Harmful Algae 8:549-561. https://doi.org/10.1016/j.hal.2008.11.009
  79. Stoecker, D. K. 1999. Mixotrophy among Dinoflagellates. J. Eukaryot. Microbiol. 46:397-401. https://doi.org/10.1111/j.1550-7408.1999.tb04619.x
  80. Stoecker, D. K., Hansen, P. J., Caron, D. A. & Mitra, A. 2017. Mixotrophy in the marine plankton. Annu. Rev. Mar. Sci. 9:311-335. https://doi.org/10.1146/annurev-marine-010816-060617
  81. Stoecker, D. K., Li, A., Coats, D. W., Gustafson, D. E. & Nannen, M. K. 1997. Mixotrophy in the dinoflagellate Prorocentrum minimum. Mar. Ecol. Prog. Ser. 152:1-12. https://doi.org/10.3354/meps152001
  82. Takahashi, K., Benico, G., Lum, W. M. & Iwataki, M. 2019. Gertia stigmatica gen. et sp. nov. (Kareniaceae, Dinophyceae), a new marine unarmored dinoflagellate possessing the peridinin-type chloroplast with an eyespot. Protist 170:125680.
  83. Tamura, K., Dudley, J., Nei, M. & Kumar, S. 2007. MEGA4: molecular evolutionary genetics analysis (MEGA) software v. 4.0. Mol. Biol. Evol. 24:1596-1599. https://doi.org/10.1093/molbev/msm092
  84. Uchida, T., Toda, S., Matsuyama, Y., Yamaguchi, M., Kotani, Y. & Honjo, T. 1999. Interactions between the red tide dinoflagellates Heterocapsa circularisquama and Gymnodinium mikimotoi in laboratory culture. J. Exp. Mar. Biol. Ecol. 241:285-299. https://doi.org/10.1016/S0022-0981(99)00088-X
  85. Van Dolah, F. M., Lidie, K. B., Monroe, E. A., Bhattacharya, D., Campbell, L., Doucette, G. J. & Kamykowski, D. 2009. The Florida red tide dinoflagellate Karenia brevis: new insights into cellular and molecular processes underlying bloom dynamics. Harmful Algae 8:562-572. https://doi.org/10.1016/j.hal.2008.11.004
  86. Yniguez, A. T., Lim, P. T., Leaw, C. P., Jipanin, S. J., Iwataki, M., Benico, G. & Azanza, R. V. 2021. Over 30 years of HABs in the Philippines and Malaysia: what have we learned? Harmful Algae 102:101776.
  87. Yoo, Y. D., Jeong, H. J., Kang, N. S., Song, J. Y., Kim, K. Y., Lee, G. & Kim, J. 2010. Feeding by the newly described mixotrophic dinoflagellate Paragymnodinium shiwhaense: feeding mechanism, prey species, and effect of prey concentration. J. Eukaryot. Microbiol. 57:145-158. https://doi.org/10.1111/j.1550-7408.2009.00448.x
  88. Zhang, Q. -C., Wang, Y. -F., Song, M. -J., Wang, J. -X., Ji, N. -J., Liu, C., Kong, F, -Z., Yan, T. & Yu, R. -C. 2022. First record of a Takayama bloom in Haizhou Bay in response to dissolved organic nitrogen and phosphorus. Mar. Pollut. Bull. 178:113572.
  89. Zhang, Q., Yu, R., Song, J., Yan, T., Wang, Y. & Zhou, M. 2011. Will harmful dinoflagellate Karenia mikimotoi grow phagotrophically? Chin. J. Oceanol. Limnol. 29:849-859. https://doi.org/10.1007/s00343-011-0513-9
  90. Zheng, J. -W., Mao, X. -T., Ye, M. -H., Li, H. -Y., Liu, J. -S. & Yang, W. -D. 2021. Allelopathy and underlying mechanism of Karenia mikimotoi on the diatom Thalassiosira pseudonana under laboratory condition. Algal Res. 54: 102229.