ALGAE

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

DOI QR Code

Protists in hypoxic waters of Jinhae Bay and Masan Bay, Korea, based on metabarcoding analyses: emphasizing surviving dinoflagellates

  • 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) ;
  • 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) ;
  • Jin Kyeong Kang (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University) ;
  • Yeong Du Yoo (Department of Marine Biotechnology, Kunsan National University)
  • Received : 2023.09.25
  • Accepted : 2023.12.06
  • Published : 2023.12.21
Download PDF
⟨ Previous Next ⟩

Abstract

Hypoxia can indeed impact the survival of protists, which play a crucial role in marine ecosystems. To better understand the protistan community structure and species that can thrive in hypoxic waters, we collected samples from both the surface and bottom waters during the hypoxic period in Jinhae and Masan Bays and the non-hypoxic period in Jinhae Bay. Subsequently, we utilized metabarcoding techniques to identify the protistan species. During hypoxia, with dissolved oxygen concentrations of 0.8 mg L-1 in Jinhae Bay and 1.8 mg L-1 in Masan Bay within the bottom waters, the phylum Dinoflagellata exhibited the highest amplicon sequence variants richness among the identified protist phyla. Following the Dinoflagellata, Ochrophyta and Ciliophora also displayed notable presence. In hypoxic waters of Jinhae and Masan Bays, we identified a total of 36 dinoflagellate species that exhibited various trophic modes. These included one autotrophic species, 14 mixotrophic species, 9 phototrophic species with undetermined trophic modes (either autotrophic or mixotrophic), 2 kleptoplastidic species, and 10 heterotrophic species. Furthermore, the hypoxic bottom water exhibited a greater number of heterotrophic dinoflagellate species compared to the non-hypoxic surface water within the same water column or the non-hypoxic bottom water. Therefore, feeding by mixotrophic and heterotrophic dinoflagellates may be partially responsible for their dominance in terms of the number of species surviving in hypoxic waters. This study not only introduces the initial documentation of 26 dinoflagellate species surviving in hypoxic conditions but also establishes a foundation for a more comprehensive understanding of the ecophysiology of dinoflagellates in hypoxic marine environments.

Keywords

Acknowledgement

We thank Prof. Chung Yeon Hwang at Seoul National University for valuable comments. 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-2021R1A2C1093379; NRF-RS-2023-00291696) and Korea Institute of Marine Science & Technology Promotion (KIMST) by the Ministry of Oceans and Fisheries (20230018) award to HJJ.

References

  1. Azam, F., Fenchel, T., Field, J. G., Gray, J. S., Meyer-Reil, L. A. & Thingstad, F. 1983. The ecological role of water-column microbes in the sea. Mar. Ecol. Prog. Ser. 10:257-263.  https://doi.org/10.3354/meps010257
  2. Bendtsen, J. & Hansen, J. L. S. 2013. Effects of global warming on hypoxia in the Baltic Sea-North Sea transition zone. Ecol. Modell. 264:17-26.  https://doi.org/10.1016/j.ecolmodel.2012.06.018
  3. Blossom, H. E., Daugbjerg, N. & Hansen, P. J. 2012. Toxic mucus traps: a novel mechanism that mediates prey uptake in the mixotrophic dinoflagellate Alexandrium pseudogonyaulax. Harmful Algae 17:40-53.  https://doi.org/10.1016/j.hal.2012.02.010
  4. Bockstahler, K. R. & Coats, D. W. 1993. Grazing of the mixotrophic dinoflagellate Gymnodinium sanguineum on ciliate populations of Chesapeake Bay. Mar. Biol. 116:477-487.  https://doi.org/10.1007/BF00350065
  5. Breitburg, D., Levin, L. A., Oschlies, A., Gregoire, M., Chavez, F. P., Conley, D. J., Garcon, V., Gilbert, D., Gutierrez, D., Isensee, K., Jacinto, G. S., Limburg, K. E., Montes, I., Naqvi, S. W. A., Pitcher, G. C., Rabalais, N. N., Roman, M. R., Rose, K. A., Seibel, B. A., Telszewski, M., Yasuhara, M. & Zhang, J. 2018. Declining oxygen in the global ocean and coastal waters. Science 359:eaam7240. 
  6. Buskey, E. J. 1997. Behavioral components of feeding selectivity of the heterotrophic dinoflagellate Protoperidinium pellucidum. Mar. Ecol. Prog. Ser. 153:77-89.  https://doi.org/10.3354/meps153077
  7. Buskey, E. J., Strom, S. & Coulter, C. 1992. Biolumiscence of heterotrophic dinoflagellates from Texas coastal waters. J. Exp. Mar. Biol. Ecol. 159:37-49.  https://doi.org/10.1016/0022-0981(92)90256-A
  8. Callahan, B. J., McMurdie, P. J., Rosen, M. J., Han, A. W., Johnson, A. J. A. & Holmes, S. P. 2016. DADA2: high-resolution sample inference from Illumina amplicon data. Nat. Methods 13:581-583.  https://doi.org/10.1038/nmeth.3869
  9. Camacho, C., Coulouris, G., Avagyan, V., Ma, N., Papadopoulos, J., Bealer, K. & Madden, T. L. 2009. BLAST+: architecture and applications. BMC Bioinform. 10:1-9.  https://doi.org/10.1186/1471-2105-10-1
  10. Caporaso, J. G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F. D., Costello, E. K., Fierer, N., Pena, A. G., Goodrich, J. K., Gordon, J. I., Huttley, G. A., Kelley, S. T., Knights, D., Koenig, J. E., Ley, R. E., Lozupone, C. A., McDonald, D., Muegge, B. D., Pirrung, M., Reeder, J., Sevinsky, J. R., Turnbaugh, P. J., Walters, W. A., Widmann, J., Yatsumenko, T., Zaneveld, J. & Knight, R. 2010. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7:335-336.  https://doi.org/10.1038/nmeth.f.303
  11. Caron, D. A., Countway, P. D., Jones, A. C., Kim, D. Y. & Schnetzer, A. 2012. Marine protistan diversity. Ann. Rev. Mar. Sci. 4:467-493.  https://doi.org/10.1146/annurev-marine-120709-142802
  12. Caroppo, C., Congestri, R. & Bruno, M. 1999. On the presence of Phalacroma rotundatum in the southern Adriatic Sea (Italy). Aquat. Microb. Ecol. 17:301-310.  https://doi.org/10.3354/ame017301
  13. Chen, C.-C., Shiah, F.-K., Gong, G.-C. & Chen, T.-Y. 2021. Impact of upwelling on phytoplankton blooms and hypoxia along the Chinese coast in the East China Sea. Mar. Pollut. Bull. 167:112288. 
  14. 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
  15. 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. J. Eukaryot. Microbiol. 59:1-11.  https://doi.org/10.1111/j.1550-7408.2011.00588.x
  16. Coats, D. W. & Moon, E. 2022. Ultrastructure of selected life history stages of the parasitic dinoflagellate Euduboscquella cachoni. J. Eukaryot. Microbiol. 69:e12921. 
  17. Dias, A. & Kurian, S. 2022. Characterization of colored dissolved organic matter along the western continental shelf of India during the seasonal hypoxia. Estuar. Coast. Shelf Sci. 265:107714. 
  18. Diaz, R. J. 2001. Overview of hypoxia around the world. J. Environ. Qual. 30:275-281.  https://doi.org/10.2134/jeq2001.302275x
  19. Edgcomb, V. P. 2016. Marine protist associations and environmental impacts across trophic levels in the twilight zone and below. Curr. Opin. Microbiol. 31:169-175.  https://doi.org/10.1016/j.mib.2016.04.001
  20. Eom, S. H., Jeong, H. J., Ok, J. H., Park, S. A., Kang, H. C. & You, J. H. 2024. Combined effects of hypoxia and starvation on the survival and growth rates of autotrophic, mixotrophic, and heterotrophic dinoflagellates. Mar. Biol. In press. 
  21. 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
  22. 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
  23. Hallegraeff, G. M. 2004. Harmful algal blooms: a global overview. In Hallegraeff, G. M., Anderson, D. M. & Cembella, A. D. (Eds.) Manual on Harmful Marine Microalgae. UNESCO, Paris, pp. 25-49. 
  24. Hansen, P. J. 1991. Dinophysis: a planktonic dinoflagellate genus which can act both as a prey and a predator of a ciliate. Mar. Ecol. Prog. Ser. 69:201-204.  https://doi.org/10.3354/meps069201
  25. Hansen, P. J. 1992. Prey size selection, feeding rates and growth dynamics of heterotrophic dinoflagellates with special emphasis on Gyrodinium spirale. Mar. Biol. 114:327-334.  https://doi.org/10.1007/BF00349535
  26. Hoppenrath, M. 2000. Morphology and taxonomy of Sinophysis (Dinophyceae, Dinophysiales) including two new marine sand-dwelling species from the North German Wadden Sea. Eur. J. Phycol. 35:153-162.  https://doi.org/10.1080/09670260010001735741
  27. 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.  https://doi.org/10.1111/j.0022-3646.1996.00279.x
  28. 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
  29. Jang, S. H., Lim, P., Torano, O., Neave, E. F., Seim, H. & Marchetti, A. 2022. Protistan communities within the Galapagos archipelago with an emphasis on micrograzers. Front. Mar. Sci. 9:811979. 
  30. Jeong, H. J. 1994. Predation by the heterotrophic dinoflagellate Protoperidinium cf. divergens on copepod eggs and early naupliar stages. Mar. Ecol. Prog. Ser. 114:203-208.  https://doi.org/10.3354/meps114203
  31. Jeong, H. J. 1999. The ecological roles of heterotrophic dinoflagellates in marine planktonic community. J. Eukaryot. Microbiol. 46:390-396.  https://doi.org/10.1111/j.1550-7408.1999.tb04618.x
  32. 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. 
  33. Jeong, H. J., Kim, J. S., Kim, J. H., Kim, S. T., Seong, K. A., Kim, T. H., Song, J. Y. & Kim, S. K. 2005a. Feeding and grazing impact of the newly described heterotrophic dinoflagellate Stoeckeria algicida on the harmful alga Heterosigma akashiwo. Mar. Ecol. Prog. Ser. 295:69-78.  https://doi.org/10.3354/meps295069
  34. Jeong, H. J., Kim, J. S., Yoo, Y. D., Kim, S. T., Kim, T. H., Park, M. G., Lee, C. H., Seong, K. A., Kang, N. S. & Shim, J. H. 2003. Feeding by the heterotrophic dinoflagellate Oxyrrhis marina on the red-tide raphidophyte Heterosigma akashiwo: a potential biological method to control red tides using mass-cultured grazers. J. Eukaryot. Microbiol. 50:274-282.  https://doi.org/10.1111/j.1550-7408.2003.tb00134.x
  35. Jeong, H. J., Kim, S. K., Kim, J. S., Kim, S. T., Yoo, Y. D. & Yoon, J. Y. 2001. Growth and grazing rates of the heterotrophic dinoflagellate Polykrikos kofoidii on red-tide and toxic dinoflagellates. J. Eukaryot. Microbiol. 48:298-308.  https://doi.org/10.1111/j.1550-7408.2001.tb00318.x
  36. 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
  37. 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
  38. 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. 2005b. Feeding by red-tide dinoflagellates on the cyanobacterium Synechococcus. Aquat. Microb. Ecol. 41:131-143.  https://doi.org/10.3354/ame041131
  39. Jeong, H. J., Seong, K. A., Yoo, Y. D., Kim, T. H., Kang, N. S., Kim, S., Park, J. Y., Kim, J. S., Kim, G. H. & Song, J. Y. 2008. Feeding and grazing impact by small marine heterotrophic dinoflagellates on heterotrophic bacteria. J. Eukaryot. Microbiol. 55:271-288.  https://doi.org/10.1111/j.1550-7408.2008.00336.x
  40. 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
  41. Jeong, H. J., Yoo, Y. D., Kim, S. T. & Kang, N. S. 2004. Feeding by the heterotrophic dinoflagellate Protoperidinium bipes on the diatom Skeletonema costatum. Aquat. Microb. Ecol. 36:171-179.  https://doi.org/10.3354/ame036171
  42. 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:S75-S88.  https://doi.org/10.1016/j.hal.2013.10.008
  43. Jeong, H. J., Yoo, Y. D., Park, J. Y., Song, J. Y., Kim, S. T., Lee, S. H., Kim, K. Y. & Yih, W. H. 2005c. 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
  44. 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. 2005d. Feeding by the mixotrophic red-tide 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
  45. Kang, H. C., Jeong, H. J., Lim, A. S., Ok, J. H., You, J. H., Park, S. A. & Eom, S. H. 2023. Feeding by common heterotrophic protists on the mixotrophic dinoflagellate Ansanella granifera (Suessiaceae, Dinophyceae). Algae 38:57-70.  https://doi.org/10.4490/algae.2023.38.2.24
  46. Kang, H. C., Jeong, H. J., Park, S. A., Eom, S. H., Ok, J. H., You, J. H., Jang, S. H. & Lee, S. Y. 2020. Feeding by the newly described heterotrophic dinoflagellate Gyrodinium jinhaense: comparison with G. dominans and G. moestrupii. Mar. Biol. 167:156. 
  47. Kawami, H., Van Wezel, R., Koeman, R. P. T. & Matsuoka, K. 2009. Protoperidinium tricingulatum sp. nov. (Dinophyceae), a new motile form of a round, brown, and spiny dinoflagellate cyst. Phycol. Res. 57:259-267.  https://doi.org/10.1111/j.1440-1835.2009.00545.x
  48. Kemp, W. M., Testa, J. M., Conley, D. J., Gilbert, D. & Hagy, J. D. 2009. Temporal responses of coastal hypoxia to nutrient loading and physical controls. Biogeosciences 6:2985-3008.  https://doi.org/10.5194/bg-6-2985-2009
  49. Kim, J. S. & Jeong, H. J. 2004. Feeding by the heterotrophic dinoflagellates Gyrodinium dominans and G. spirale on the red-tide dinoflagellate Prorocentrum minimum. Mar. Ecol. Prog. Ser. 280:85-94.  https://doi.org/10.3354/meps280085
  50. Kim, S. & Park, M. G. 2017. Feeding characteristics and molecular phylogeny of the thecate mixotrophic dinoflagellate Fragilidium mexicanum. Harmful Algae 63:154-163.  https://doi.org/10.1016/j.hal.2017.02.007
  51. Kim, Y. H., Seo, H. J., Yang, H. J., Lee, M.-Y., Kim, T.-H., Yoo, D., Choi, B.-J. & Jang, S. H. 2023. Protistan community structure and the influence of a branch of Kuroshio in the northeastern East China Sea during the late spring. Front. Mar. Sci. 10:1192529. 
  52. Kiϕrboe, T. & Titelman, J. 1998. Feeding, prey selection and prey encounter mechanisms in the heterotrophic dinoflagellate Noctiluca scintillans. J. Plankton Res. 20:1615-1636.  https://doi.org/10.1093/plankt/20.8.1615
  53. Lee, J., Park, K.-T., Lim, J.-H., Yoon, J.-E. & Kim, I.-N. 2018. Hypoxia in Korean coastal waters: a case study of the natural Jinhae Bay and artificial Shihwa Bay. Front. Mar. Sci. 5:70. 
  54. 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
  55. Lee, M. J., Jeong, H. J., Lee, K. H., Jang, S. H., Kim, J. H. & Kim, K. Y. 2015. Mixotrophy in the nematocyst-taeniocyst complex-bearing phototrophic dinoflagellate Polykrikos hartmannii. Harmful Algae 49:124-134.  https://doi.org/10.1016/j.hal.2015.08.006
  56. Lee, S. K., Jeong, H. J., Jang, S. H., Lee, K. H., Kang, N. S., Lee, M. J. & Potvin, E. 2014. Mixotrophy in the newly described dinoflagellate Ansanella granifera: feeding mechanism, prey species, and effect of prey concentration. Algae 29:137-152.  https://doi.org/10.4490/algae.2014.29.2.137
  57. 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.  https://doi.org/10.4490/algae.2021.36.3.4
  58. Lee, S. Y., Jeong, H. J., Ok, J. H., Kang, H. C. & You, J. H. 2020. Spatial-temporal distributions of the newly described mixotrophic dinoflagellate Gymnodinium smaydae in Korean coastal waters. Algae 35:225-236.  https://doi.org/10.4490/algae.2020.35.8.25
  59. Lewitus, A. J., Glasgow, H. B. Jr. & Burkholder, J. M. 1999. Kleptoplastidy in the toxic dinoflagellate Pfiesteria piscicida (Dinophyceae). J. Phycol. 35:303-312.  https://doi.org/10.1046/j.1529-8817.1999.3520303.x
  60. 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
  61. 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
  62. Lim, H.-S., Diaz, R. J., Hong, J.-S. & Schaffner, L. C. 2006. Hypoxia and benthic community recovery in Korean coastal waters. Mar. Pollut. Bull. 52:1517-1526.  https://doi.org/10.1016/j.marpolbul.2006.05.013
  63. Martin, M. 2011. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J. 17:10-12.  https://doi.org/10.14806/ej.17.1.200
  64. Martinez, E., Velez, S. M., Mayo, M. & Sastre, M. P. 2016. Acute toxicity assessment of N,N-diethyl-m-toluamide (DEET) on the oxygen flux of the dinoflagellate Gymnodinium instriatum. Ecotoxicology 25:248-252.  https://doi.org/10.1007/s10646-015-1564-z
  65. Massana, R. 2015. Protistan diversity in environmental molecular surveys. In Ohtsuka, S., Suzaki, T., Horiguchi, T., Suzuki, N. & Not, F. (Eds.) Marine Protists: Diversity and Dynamics. Springer, Tokyo, pp. 3-21. 
  66. Min, J. & Kim, K. Y. 2023. Diversity and assembly of planktonic protist communities in the Jeju Strait, Korea. Front. Mar. Sci. 10:1225640. 
  67. Mitra, A., Flynn, K. J., Burkholder, J. M., Berge, T., Calbet, A., Raven, J. A., Graneli, E., Glibert, P. M., Hansen, P. K., Stoecker, D. K., Thingstad, F., Tillmann, U., Vage, S., Wilken, S. & Zubkov, M. V. 2014. The role of mixotrophic protists in the biological carbon pump. Biogeosciences 11:995-1005.  https://doi.org/10.5194/bg-11-995-2014
  68. Moestrup, O., Lindberg, K. & Daugbjerg, N. 2009. 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
  69. Nakamura, Y. & Hirata, A. 2006. Plankton community structure and trophic interactions in a shallow and eutrophic estuarine system, Ariake Sound, Japan. Aquat. Microb. Ecol. 44:45-57.  https://doi.org/10.3354/ame044045
  70. Nilsson, H. C. & Rosenberg, R. 1994. Hypoxic response of two marine benthic communities. Mar. Ecol. Prog. Ser. 115:209-217.  https://doi.org/10.3354/meps115209
  71. Ohtsuka, S., Suzaki, T., Horiguchi, T., Suzuki, N. & Not, F. 2015. Marine protists: diversity and dynamics. Springer, Tokyo, 637 pp. 
  72. 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
  73. 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
  74. Ok, J. H., Jeong, H. J., Lim, A. S., Kang, H. C., You, J. H., Park, S. A. & Eom, S. H. 2023a. Lack of mixotrophy in three Karenia species and the prey spectrum of Karenia mikimotoi (Gymnodiniales, Dinophyceae). Algae 38:39-55.  https://doi.org/10.4490/algae.2023.38.2.28
  75. Ok, J. H., Jeong, H. J., Lim, A. S., Lee, S. Y. & Kim, S. J. 2018. Feeding by the heterotrophic nanoflagellate Katablepharis remigera on algal prey and its nationwide distribution in Korea. Harmful Algae 74:30-45.  https://doi.org/10.1016/j.hal.2018.03.011
  76. 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. 2023b. 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. 
  77. Ok, J. H., Jeong, H. J., You, J. H., Kang, H. C., Park, S. A., Lim, A. S., Lee, S. Y. & Eom, S. H. 2021b. Phytoplankton bloom dynamics in incubated natural seawater: predicting bloom magnitude and timing. Front. Mar. Sci. 8:681252. 
  78. Piredda, R., Tomasino, M. P., D'Erchia, A. M., Manzari, C., Pesole, G., Montresor, M., Kooistra, W. H. C. F., Sarno, D. & Zingone, A. 2017. Diversity and temporal patterns of planktonic protist assemblages at a Mediterranean Long Term Ecological Research site. FEMS Microbiol. Ecol. 93:fiw200. 
  79. Rabalais, N. N., Turner, R. E., Diaz, R. J. & Justic, D. 2009. Global change and eutrophication of coastal waters. ICES J. Mar. Sci. 66:1528-1537.  https://doi.org/10.1093/icesjms/fsp047
  80. Rajan, A., Thankamony, R., Othman, Y., Khan, S. A. & Jamali, E. A. 2021. Massive bloom of Cochlodinium polykrikoides and its impacts in the United Arab Emirates' waters. Int. J. Ecol. Environ. Sci. 3:341-347. 
  81. Ratmaya, W., Laverman, A. M., Rabouille, C., Akbarzadeh, Z., Andrieux-Loyer, F., Barille, L., Barille, A.-L., Merrer, Y. L. & Souchu, P. 2022. Temporal and spatial variations in benthic nitrogen cycling in a temperate macro-tidal coastal ecosystem: observation and modeling. Cont. Shelf Res. 235:104649. 
  82. Rene, A., Camp, J. & Garces, E. 2014. Polykrikos tanit sp. nov., a new mixotrophic unarmoured pseudocolonial dinoflagellate from the NW Mediterranean Sea. Protist 165:81-92.  https://doi.org/10.1016/j.protis.2013.12.001
  83. Riedel, B., Zuschin, M. & Stachowitsch, M. 2012. Tolerance of benthic macrofauna to hypoxia and anoxia in shallow coastal seas: a realistic scenario. Mar. Ecol. Prog. Ser. 458:39-52.  https://doi.org/10.3354/meps09724
  84. Rocke, E., Jing, H. & Liu, H. 2013. Phylogenetic composition and distribution of picoeukaryotes in the hypoxic northwestern coast of the Gulf of Mexico. Microbiologyopen 2:130-143.  https://doi.org/10.1002/mbo3.57
  85. Rocke, E., Jing, H., Xia, X. & Liu, H. 2016. Effects of hypoxia on the phylogenetic composition and species distribution of protists in a subtropical harbor. Microb. Ecol. 72:96-105.  https://doi.org/10.1007/s00248-016-0751-7
  86. Rodriguez, F., Escalera, L., Reguera, B., Rial, P., Riobo, P. & da Silva, T. D. J. 2012. Morphological variability, toxinology and genetics of the dinoflagellate Dinophysis tripos (Dinophysiaceae, Dinophysiales). Harmful Algae 13:26-33.  https://doi.org/10.1016/j.hal.2011.09.012
  87. 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. 
  88. Saldarriaga, J. F., Leander, B. S., "Max" Taylor, F. J. R. & Keeling, P. J. 2003. Lessardia elongata gen. et sp. nov. (Dinoflagellata, Peridiniales, Podolampaceae) and the taxonomic position of the genus Roscoffia. J. Phycol. 39:368-378.  https://doi.org/10.1046/j.1529-8817.2003.02113.x
  89. Sampaio, E., Santos, C., Rosa, I. C., Ferreira, V., Portner, H.-O., Duarte, C. M., Levin, L. A. & Rosa, R. 2021. Impacts of hypoxic events surpass those of future ocean warming and acidification. Nat. Ecol. Evol. 5:311-321.  https://doi.org/10.1038/s41559-020-01370-3
  90. Sampedro, N., Fraga, S., Penna, A., Casabianca, S., Zapata, M., Grunewald, C. F., Riobo, P. & Camp, J. 2011. Barrufeta bravensis gen. nov. sp. nov. (Dinophyceae): a new bloom-forming species from the Northwest Mediterranean sea. J. Phycol. 47:375-392.  https://doi.org/10.1111/j.1529-8817.2011.00968.x
  91. Santoferrara, L., Burki, F., Filker, S., Logares, R., Dunthorn, M. & McManus, G. B. 2020. Perspectives from ten years of protist studies by high-throughput metabarcoding. J. Eukaryot. Microbiol. 67:612-622.  https://doi.org/10.1111/jeu.12813
  92. Santoferrara, L. F., McManus, G. B., Greenfield, D. I. & Smith, S. A. 2022. Microbial communities (bacteria, archaea and eukaryotes) in a temperate estuary during seasonal hypoxia. Aquat. Microb. Ecol. 88:61-79.  https://doi.org/10.3354/ame01982
  93. Schmidtko, S., Stramma, L. & Visbeck, M. 2017. Decline in global oceanic oxygen content during the past five decades. Nature 542:335-339.  https://doi.org/10.1038/nature21399
  94. Schnepf, E. & Elbrachter, M. 1992. Nutritional strategies in dinoflagellates: a review with emphasis on cell biological aspects. Eur. J. Protistol. 28:3‒24. 
  95. Scully, M. E., Geyer, W. R., Borkman, D., Pugh, T. L., Costa, A. & Nichols, O. C. 2022. Unprecedented summer hypoxia in southern Cape Cod Bay: an ecological response to regional climate change? Biogeosciences 19:3523-3536.  https://doi.org/10.5194/bg-19-3523-2022
  96. Sherr, E. B. & Sherr, B. F. 2007. Heterotrophic dinoflagellates: a significant component of microzooplankton biomass and major grazers of diatoms in the sea. Mar. Ecol. Prog. Ser. 352:187-197.  https://doi.org/10.3354/meps07161
  97. Sinkko, H., Lukkari, K., Sihvonen, L. M., Sivonen, K., Leivuori, M., Rantanen, M., Paulin, L. & Lyra, C. 2013. Bacteria contribute to sediment nutrient release and reflect progressed eutrophication-driven hypoxia in an organicrich continental sea. PLoS ONE 8:e67061. 
  98. Smalley, G. W. & Coats, D. W. 2002. Ecology of the red-tide dinoflagellate Ceratium furca: distribution, mixotrophy, and grazing impact on ciliate populations of Chesapeake Bay. J. Eukaryot. Microbiol. 49:63-73.  https://doi.org/10.1111/j.1550-7408.2002.tb00343.x
  99. Smayda, T. J. 1997. Harmful algal blooms: their ecophysiology and general relevance to phytoplankton blooms in the sea. Limnol. Oceanogr. 42:1137-1153.  https://doi.org/10.4319/lo.1997.42.5_part_2.1137
  100. Stat, M., Morris, E. & Gates, R. D. 2008. Functional diversity in coral-dinoflagellate symbiosis. Proc. Natl. Acad. Sci. U. S. A. 105:9256-9261.  https://doi.org/10.1073/pnas.0801328105
  101. Stauffer, B. A., Schnetzer, A., Gellene, A. G., Oberg, C., Sukhatme, G. S. & Caron, D. A. 2013. Effects of an acute hypoxic event on microplankton community structure in a coastal harbor of Southern California. Estuar. Coasts 36:135-148.  https://doi.org/10.1007/s12237-012-9551-6
  102. Stoeck, T., Bass, D., Nebel, M., Christen, R., Jones, M. D. M., Breiner, H.-W. & Richards, T. A. 2010. Multiple marker parallel tag environmental DNA sequencing reveals a highly complex eukaryotic community in marine anoxic water. Mol. Ecol. 19:21-31.  https://doi.org/10.1111/j.1365-294X.2009.04480.x
  103. Stoecker, D. K., Hansen, P. J., Caron, D. A. & Mitra, A. 2017. Mixotrophy in the marine plankton. Annu. Rev. Mar. Sci. 9:311‒335. 
  104. Strom, S. L. & Buskey, E. J. 1993. Feeding, growth, and behavior of the thecate heterotrophic dinoflagellate Oblea rotunda. Limnol. Oceanogr. 38:965-977.  https://doi.org/10.4319/lo.1993.38.5.0965
  105. Takano, Y. & Horiguchi, T. 2004. Surface ultrastructure and molecular phylogenetics of four unarmored heterotrophic dinoflagellates, including the type species of the genus Gyrodinium (Dinophyceae). Phycol. Res. 52:107-116.  https://doi.org/10.1111/j.1440-1835.2004.tb00319.x
  106. Telesh, I., Schubert, H. & Skarlato, S. 2013. Life in the salinity gradient: discovering mechanisms behind a new biodiversity pattern. Estuar. Coast. Shelf Sci. 135:317-327.  https://doi.org/10.1016/j.ecss.2013.10.013
  107. Thimijan, R. W. & Heins, R. D. 1983. Photometric, radiometric, and quantum light units of measure: a review of procedures for interconversion. HortScience 18:818-822.  https://doi.org/10.21273/HORTSCI.18.6.818
  108. Yamaguchi, A., Hoppenrath, M., Pospelova, V., Horiguchi, T. & Leander, B. S. 2011. Molecular phylogeny of the marine sand-dwelling dinoflagellate Herdmania litoralis and an emended description of the closely related planktonic genus Archaeperidinium Jorgensen. Eur. J. Phycol. 46:98-112.  https://doi.org/10.1080/09670262.2011.564517
  109. 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
  110. Yoon, E. Y., Kang, N. S. & Jeong, H. J. 2012. Gyrodinium moestrupii n. sp., a new planktonic heterotrophic dinoflagellate from the coastal waters of western Korea: morphology and ribosomal DNA gene sequence. J. Eukaryot. Microbiol. 59:571-586.  https://doi.org/10.1111/j.1550-7408.2012.00632.x
  111. You, J. H., Ok, J. H., Kang, H. C., Park, S. A., Eom, S. H. & Jeong, H. J. 2023. Five phototrophic Scrippsiella species lacking mixotrophic ability and the extended prey spectrum of Scrippsiella acuminata (Thoracosphaerales, Dinophyceae). Algae 38:111-126.  https://doi.org/10.4490/algae.2023.38.6.6