ALGAE

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

DOI QR Code

Responses of protist communities to spatio-temporal changes in water masses in the northeastern East China Sea in 2023

  • Hye Jin Seo (Department of Oceanography, Chonnam National University) ;
  • Hyun Jun Yang (Department of Oceanography, Chonnam National University) ;
  • Yun Hee Kim (Department of Oceanography, Chonnam National University) ;
  • Dohyeop Yoo (Department of Oceanography, Chonnam National University) ;
  • Hyebin Kim (Department of Oceanography, Chonnam National University) ;
  • Jiae Yoo (Major of Oceanography, Pukyong National University) ;
  • Sunju Kim (Major of Oceanography, Pukyong National University) ;
  • Yoonja Kang (Department of Ocean Integrated Science, Chonnam National University) ;
  • Tae-Hoon Kim (Department of Oceanography, Chonnam National University) ;
  • Byoung-Ju Choi (Department of Oceanography, Chonnam National University) ;
  • Adrian Marchetti (Department of Earth, Marine and Environmental Sciences, University of North Carolina at Chapel Hill) ;
  • Se Hyeon Jang (Department of Oceanography, Chonnam National University)
  • Received : 2026.02.01
  • Accepted : 2026.06.09
  • Published : 2026.06.19
Download PDF
⟨ Previous Next ⟩

Abstract

This study explores the dynamics of protist communities in the northeastern East China Sea (ECS) focusing on their responses to changing water masses and oceanographic conditions during spring, summer, and autumn in 2023. Water masses were classified using K-means clustering based on physico-chemical parameters, revealing significant seasonal variation. Protist community spatial, temporal, and vertical distributions were analyzed using 18S rRNA gene amplicon sequencing and morphological identification along the 33° N latitude, a region characterized by the confluence of multiple water masses, including Kuroshio surface (KSW) and sub-surface (KSSW) waters, Yellow Sea water (YSW), Changjiang diluted water (CDW), and ECS Shelf water. Protist diversity, community structure, and cell abundance exhibited pronounced seasonal variations influenced by temperature, salinity, and nutrient availability. In spring, YSW, characterized by phosphate deficiencies and, consequently, increased N:P ratios, exhibited a prevalence of dinoflagellates, whose phagotrophic capabilities likely conferred a competitive advantage in such nutrient-fluctuating environments. During summer, diatoms were prevalent in the ECS Shelf water, underscoring the role this water plays in shaping seasonal community structure. In contrast, CDW exhibited low species diversities, likely due to unstable salinity. In autumn, water column mixing increased overall diversity and cell abundance, particularly in YSW, where Chaetoceros socialis and other diatoms thrived. Potential phosphorus limitation, especially in the western waters, may have further influenced the spatial structuring of communities across seasons. These findings highlight complex interactions between oceanographic factors and protistan communities in the northeastern ECS, contributing to a deeper understanding of their distributions and responses to environmental changes.

Keywords

Acknowledgement

This work was supported by a National Research Foundation of Korea (NRF) grant funded by the Korean government (MSIT) (Nos. RS-2022-NR071750 and RS-2022-NR068505) and by the Korea Institute of Marine Science & Technology (KIMST) funded by the Ministry of Oceans and Fisheries (No. RS-2023-00256330, Development of risk managing technology tackling ocean and fisheries crisis around Korean Peninsula by Kuroshio Current) awarded to SH Jang. We would like to thank Wordvice (https://wordvice.com) for English language editing.

References

  1. Abad, D., Albaina, A., Aguirre, M., et al. 2016. Is metabarcoding suitable for estuarine plankton monitoring? A comparative study with microscopy. Mar. Biol. 163:149. doi.org/10.1007/s00227-016-2920-0
  2. Anderson, S. R. & Harvey, E. L. 2020. Temporal variability and ecological interactions of parasitic marine Syndiniales in coastal protist communities. mSphere 5:e00209-20. doi.org/10.1128/mSphere.00209-20
  3. Arenovski, A. L., Lim, E. L. & Caron, D. A. 1995. Mixotrophic nanoplankton in oligotrophic surface waters of the Sargasso Sea may employ phagotrophy to obtain major nutrients. J. Plankton Res. 17:801–820. doi.org/10.1093/plankt/17.4.801
  4. Bolyen, E., Rideout, J. R., Dillon, M. R., et al. 2019. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat. Biotechnol. 37:852–857. doi.org/10.1038/s41587-019-0209-9
  5. 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. doi.org/10.1038/nmeth.3869
  6. Choi, Y., Kim, T.-H., Kim, D. & Kang, D.-J. 2022. Spatiotemporal variability of aragonite saturation state in the northern East China Sea. J. Geophys. Res. Oceans 127:e2021JC017593. doi.org/10.1029/2021JC017593
  7. Cui, Z., Xu, Q., Gibson, K., Liu, S. & Chen, N. 2021. Metabarcoding analysis of harmful algal bloom species in the Changjiang Estuary, China. Sci. Total Environ. 782:146823. doi.org/10.1016/j.scitotenv.2021.146823
  8. De Vargas, C., Audic, S., Henry, N., et al. 2015. Eukaryotic plankton diversity in the sunlit ocean. Science 348:1261605. doi.org/10.1126/science.1261605
  9. Dufrêne, M. & Legendre, P. 1997. Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecol. Monogr. 67:345–366. doi.org/10.1890/0012-9615(1997)067[0345:SAAIST]2.0.CO;2
  10. Eppley, R. W., Rogers, J. N. & McCarthy, J. J. 1969. Half-saturation constants for uptake of nitrate and ammonium by marine phytoplankton. Limnol. Oceanogr. 14:912–920. doi.org/10.4319/lo.1969.14.6.0912
  11. Gong, W. & Marchetti, A. 2019. Estimation of 18S gene copy number in marine eukaryotic plankton using a next-generation sequencing approach. Front. Mar. Sci. 6:219. doi.org/10.3389/fmars.2019.00219
  12. Guillou, L., Bachar, D., Audic, S., et al. 2013. The Protist Ribosomal Reference database (PR2): a catalog of unicellular eukaryote small sub-unit rRNA sequences with curated taxonomy. Nucleic Acids Res. 41:D597–D604. doi.org/10.1093/nar/gks1160
  13. Guo, X., Miyazawa, Y. & Yamagata, T. 2006. The Kuroshio onshore intrusion along the shelf break of the East China Sea: the origin of the Tsushima Warm Current. J. Phys. Oceanogr. 36:2205–2231. doi.org/10.1175/JPO2976.1
  14. Haraguchi, L., Jakobsen, H. H., Lundholm, N. & Carstensen, J. 2018. Phytoplankton community dynamic: a driver for ciliate trophic strategies. Front. Mar. Sci. 5:272. doi.org/10.3389/fmars.2018.00272
  15. Hur, H. B., Jacobs, G. A. & Teague, W. J. 1999. Monthly variations of water masses in the Yellow and East China Seas, November 6, 1998. J. Oceanogr. 55:171–184. doi.org/10.1023/A:1007885828278
  16. Ichikawa, H. & Beardsley, R. C. 2002. The current system in the Yellow and East China Seas. J. Oceanogr. 58:77–92. doi.org/10.1023/A:1015876701363
  17. Isobe, A. 2008. Recent advances in ocean-circulation research on the Yellow Sea and East China Sea shelves. J. Oceanogr. 64:569–584. doi.org/10.1007/s10872-008-0048-7
  18. Jang, S. H., Jeong, H. J. & Chon, J. K. 2019. De novo transcriptome of the newly described phototrophic dinoflagellate Yihiella yeosuensis: comparison between vegetative cells and cysts. Mar. Biol. 166:104. doi.org/10.1007/s00227-019-3554-9
  19. 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. doi.org/10.1016/j.hal.2016.12.007
  20. 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. doi.org/10.3389/fmars.2022.811979
  21. Jeong, H. J., Kang, H. C., Lim, A. S., et al. 2021. Feeding diverse prey as an excellent strategy of mixotrophic dinoflagellates for global dominance. Sci. Adv. 7:eabe4214. doi.org/10.1126/sciadv.abe4214
  22. 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.org/10.1007/s12601-010-0007-2
  23. Kang, H. C., Jeong, H. J., Park, S. A., et al. 2020. Feeding by the newly described heterotrophic dinoflagellate Gyrodinium jinhaense: comparison with G. dominans and G. moestrupii. Mar. Biol. 167:156. doi.org/10.1007/s00227-020-03769-9
  24. Kim, D., Choi, S. H., Kim, K. H., Shim, J., Yoo, S. & Kim, C. H. 2009. Spatial and temporal variations in nutrient and chlorophyll-a concentrations in the northern East China Sea surrounding Cheju Island. Cont. Shelf Res. 29:1426–1436. doi.org/10.1016/j.csr.2009.03.012
  25. Kim, H.-C., Yoo, S. & Oh, I. S. 2007. Relationship between phytoplankton bloom and wind stress in the sub-polar frontal area of the Japan/East Sea. J. Mar. Syst. 67:205–216. doi.org/10.1016/j.jmarsys.2006.05.016
  26. 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. doi.org/10.3354/meps280085
  27. Kim, T.-W., Lee, K., Najjar, R. G., Jeong, H.-D. & Jeong, H. J. 2011. Increasing N abundance in the northwestern Pacific Ocean due to atmospheric nitrogen deposition. Science 334:505–509. doi.org/10.1126/science.1206583
  28. Kim, Y., Youn, S.-H., Oh, H. J., et al. 2020. Spatiotemporal variation in phytoplankton community driven by environmental factors in the northern East China Sea. Water 12:2695. doi.org/10.3390/w12102695
  29. Kim, Y. H., Seo, H. J., Yang, H. J., et al. 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. doi.org/10.3389/fmars.2023.1192529
  30. Kremp, A., Rengefors, K. & Montresor, M. 2009. Species specific encystment patterns in three Baltic cold-water dinoflagellates: the role of multiple cues in resting cyst formation. Limnol. Oceanogr. 54:1125–1138. doi.org/10.4319/lo.2009.54.4.1125
  31. Kwon, J. E., Jeong, H. J., Kim, S. J., Jang, S. H., Lee, K. H. & Seong, K. A. 2017. Newly discovered role of the heterotrophic nanoflagellate Katablepharis japonica, a predator of toxic or harmful dinoflagellates and raphidophytes. Harmful Algae 68:224–239. doi.org/10.1016/j.hal.2017.08.009
  32. Lee, K. H., Jeong, H. J., Jang, T. Y., et al. 2014a. 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. doi.org/10.1016/j.jembe.2014.05.011
  33. Lee, M. J., Jeong, H. J., Jang, S. H., et al. 2016. Most low-abundance "background" Symbiodinium spp. are transitory and have minimal functional significance for symbiotic corals. Microb. Ecol. 71:771–783. doi.org/10.1007/s00248-015-0724-2
  34. Lee, Y., Choi, J. K., Youn, S. & Roh, S. 2014b. Influence of the physical forcing of different water masses on the spatial and temporal distributions of picophytoplankton in the northern East China Sea. Cont. Shelf Res. 88:216–227. doi.org/10.1016/j.csr.2014.08.001
  35. Li, A., Stoecker, D. K. & Coats, D. W. 2000. Spatial and temporal aspects of Gyrodinium galatheanum in Chesapeake Bay: distribution and mixotrophy. J. Plankton Res. 22:2105–2124. doi.org/10.1093/plankt/22.11.2105
  36. Li, G., Han, X., Yue, S., Wen, G., Rongmin, Y. & Kusky, T. M. 2006. Monthly variations of water masses in the East China Seas. Cont. Shelf Res. 26:1954–1970. doi.org/10.1016/j.csr.2006.06.008
  37. Lie, H.-J. & Cho, C.-H. 2016. Seasonal circulation patterns of the Yellow and East China Seas derived from satellite-tracked drifter trajectories and hydrographic observations. Prog. Oceanogr. 146:121–141. doi.org/10.1016/j.pocean.2016.06.004
  38. Lie, H.-J., Cho, C.-H., Lee, J.-H., Lee, S. & Tang, Y. 2000. Seasonal variation of the Cheju warm current in the northern East China Sea. J. Oceanogr. 56:197–211. doi.org/10.1023/A:1011139313988
  39. Liu, S. M., Qi, X. H., Li, X., et al. 2016. Nutrient dynamics from the Changjiang (Yangtze river) estuary to the East China Sea. J. Mar. Syst. 154:15–27. doi.org/10.1016/j.jmarsys.2015.05.010
  40. Liu, Z., Gan, J., Hu, J., Wu, H., Cai, Z. & Deng, Y. 2021. Progress on circulation dynamics in the East China Sea and southern Yellow Sea: origination, pathways, and destinations of shelf currents. Prog. Oceanogr. 193:102553. doi.org/10.1016/j.pocean.2021.102553
  41. Lovejoy, C., Legendre, L., Martineau, M.-J., Bâcle, J. & von Quillfeldt, C. H. 2002. Distribution of phytoplankton and other protists in the North Water. Deep Sea Res. Part II Top. Stud. Oceanogr. 49:5027–5047. doi.org/10.1016/S0967-0645(02)00176-5
  42. Martin, M. 2011. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J. 17:10–12. doi.org/10.14806/ej.17.1.200
  43. Moon, J.-Y., Lee, K., Lim, W.-A., et al. 2021. Anthropogenic nitrogen is changing the East China and Yellow seas from being N deficient to being P deficient. Limnol. Oceanogr. 66:914–924. doi.org/10.1002/lno.11651
  44. Ou, L., Wang, D., Huang, B., Hong, H., Qi, Y. & Lu, S. 2008. Comparative study of phosphorus strategies of three typical harmful algae in Chinese coastal waters. J. Plankton Res. 30:1007–1017. doi.org/10.1093/plankt/fbn058
  45. Paasche, E. 1973. Silicon and the ecology of marine plankton diatoms. II. Silicate-uptake kinetics in five diatom species. Mar. Biol. 19:262–269. doi.org/10.1007/BF02097147
  46. Pang, I.-C., Rho, H.-K. & Kim, T.-H. 1992. Seasonal variations of water mass distributions and their causes in the Yellow Sea, the East China Sea and the adjacent seas of Cheju Island. Korean J. Fish. Aquat. Sci. 25:151–163.
  47. Pawlowski, J., Kelly-Quinn, M., Altermatt, F., et al. 2018. The future of biotic indices in the ecogenomic era: integrating (e)DNA metabarcoding in biological assessment of aquatic ecosystems. Sci. Total Environ. 637–638:1295–1310. doi.org/10.1016/j.scitotenv.2018.05.002
  48. Pawlowski, J., Lejzerowicz, F., Apotheloz-Perret-Gentil, L., Visco, J. & Esling, P. 2016. Protist metabarcoding and environmental biomonitoring: time for change. Eur. J. Protistol. 55:12–25. doi.org/10.1016/j.ejop.2016.02.003
  49. Piwosz, K., Shabarova, T., Pernthaler, J., et al. 2020. Bacterial and eukaryotic small-subunit amplicon data do not provide a quantitative picture of microbial communities, but they are reliable in the context of ecological interpretations. mSphere 5:e00052-20. doi.org/10.1128/mSphere.00052-20
  50. Qi, J., Yin, B., Zhang, Q., Yang, D. & Xu, Z. 2014. Analysis of seasonal variation of water masses in East China Sea. Chin. J. Oceanol. Limnol. 32:958–971. doi.org/10.1007/s00343-014-3269-1
  51. Raven, J. A. 1998. The twelfth Tansley Lecture. Small is beautiful: the picophytoplankton. Funct. Ecol. 12:503–513. doi.org/10.1046/j.1365-2435.1998.00233.x
  52. Seo, H. J., Kim, Y. H., Yang, H. J., et al. 2024. Spring protistan communities in response to warming in the northeastern East China Sea. Mar. Environ. Res. 196:106376. doi.org/10.1016/j.marenvres.2024.106376
  53. Son, Y. B. & Choi, J.-K. 2022. Mapping the Changjiang diluted water in the East China Sea during summer over a 10-year period using GOCI satellite sensor data. Front. Mar. Sci. 9:1024306. doi.org/10.3389/fmars.2022.1024306
  54. Stoeck, T., Bass, D., Nebel, M., et al. 2010. Multiple marker parallel tag environmental DNA sequencing reveals a highly complex eukaryotic community in marine anoxic water. Mol. Ecol. 19:21–31. doi.org/10.1111/j.1365-294X.2009.04480.x
  55. Suzuki, Y. & Takahashi, M. 1995. Growth responses of several diatom species isolated from various environments to temperature. J. Phycol. 31:880–888. doi.org/10.1111/j.0022-3646.1995.00880.x
  56. Wang, B.-D., Wang, X.-L. & Zhan, R. 2003. Nutrient conditions in the Yellow Sea and the East China Sea. Estuar. Coast. Shelf Sci. 58:127–136. doi.org/10.1016/S0272-7714(03)00067-2
  57. Wang, Y., Guo, X., Zhao, L. & Zhang, J. 2019. Seasonal variations in nutrients and biogenic particles in the upper and lower layers of East China Sea Shelf and their export to adjacent seas. Prog. Oceanogr. 176:102138. doi.org/10.1016/j.pocean.2019.102138
  58. Worden, A. Z., Follows, M. J., Giovannoni, S. J., Wilken, S., Zimmerman, A. E. & Keeling, P. J. 2015. Rethinking the marine carbon cycle: factoring in the multifarious lifestyles of microbes. Science 347:1257594. doi.org/10.1126/science.1257594
  59. Yanao, S. & Matsuno, T. 2013. Characteristics of outer shelf water in the East China Sea. J. Oceanogr. 69:245–258. doi.org/10.1007/s10872-012-0169-x
  60. Yang, H. J., Kim, Y. H., Seo, H. J., Lee, M. J. & Jang, S. H. 2024. Insights into plankton communities in a Margalefidinium polykrikoides (Gymnodiniales, Dinophyceae) bloom and adjacent non-bloom waters. Algae 39:277–291. doi.org/10.4490/algae.2024.39.12.10
  61. Yarimizu, K., Sildever, S., Hamamoto, Y., et al. 2021. Development of an absolute quantification method for ribosomal RNA gene copy numbers per eukaryotic single cell by digital PCR. Harmful Algae 103:102008. doi.org/10.1016/j.hal.2021.102008
  62. Yoo, D., Kim, J.-K. & Choi, B.-J. 2023. Distribution and origin of the mid-depth cold water pools observed in the Jeju Strait in the summer of 2019. J. Korean Soc. Oceanogr. 28:19–40 (in Korean with English summary). doi.org/10.7850/jkso.2023.28.1.019
  63. Yoo, Y. D., Jeong, H. J., Kim, M. S., et al. 2009. Feeding by phototrophic red-tide dinoflagellates on the ubiquitous marine diatom Skeletonema costatum. J. Eukaryot. Microbiol. 56:413–420. doi.org/10.1111/j.1550-7408.2009.00421.x
  64. Zhang, J., Guo, X. & Zhao, L. 2019. Tracing external sources of nutrients in the East China Sea and evaluating their contributions to primary production. Prog. Oceanogr. 176:102122. doi.org/10.1016/j.pocean.2019.102122
  65. Zhang, R., Chen, M., Cao, J., Ma, Q., Yang, J. & Qiu, Y. 2012. Nitrogen fixation in the East China Sea and southern Yellow Sea during summer 2006. Mar. Ecol. Prog. Ser. 447:77–86. doi.org/10.3354/meps09509
  66. Zhou, Z.-X., Yu, R.-C., Sun, C., Feng, M. & Zhou, M.-J. 2019. Impacts of Changjiang River discharge and Kuroshio intrusion on the diatom and dinoflagellate blooms in the East China Sea. J. Geophys. Res. Oceans 124:5244–5257. doi.org/10.1029/2019JC015158