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Nitrate uptake of the red tide dinoflagellate Prorocentrum micans measured using a nutrient repletion method: effect of light intensity

  • Lee, Kyung Ha (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) ;
  • Kim, Hye Jeong (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University) ;
  • Lim, An Suk (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University)
  • Received : 2017.03.05
  • Accepted : 2017.05.20
  • Published : 2017.06.15

Abstract

The ability of a red tide species to take up nutrients is a critical factor affecting its red tide dynamics and species competition. Nutrient uptake by red tide species has been conventionally measured by incubating nutrient-depleted cells for a short period at 1 or 2 light intensities. This method may be applicable to certain conditions under which cells remain in oligotrophic water for a long time and high nutrients are suddenly introduced. Thus, a new method should be developed that can be applicable to the conditions under which cells are maintained in eutrophicated waters in healthy conditions and experience light and dark cycles and different light intensities during vertical migration. In this study, a new repletion method reflecting these conditions was developed. The nitrate uptake rates of the red tide dinoflagellate Prorocentrum micans originally maintained in nitrate repletion and depletion conditions as a function of nitrate concentration were measured. With increasing light intensity from 10 to $100{\mu}E\;m^{-2}s^{-1}$, the maximum nitrate uptake rate ($V_{max}$) of P. micans increased from 3.6 to $10.8 pM\;cell^{-1}d^{-1}$ and the half saturation constant ($K_{s-NO3}$) increased from 4.1 to $6.9{\mu}M$. At $20{\mu}E\;m^{-2}s^{-1}$, the $V_{max}$ and $K_{s-NO3}$ of P. micans originally maintained in a nitrate repletion condition were similar to those maintained in a nitrate depletion condition. Thus, differences in cells under nutrient repletion and depletion conditions may not affect $K_{s-NO3}$ and $V_{max}$. Moreover, different light intensities may cause differences in the nitrate uptake of migratory phototrophic dinoflagellates.

Keywords

References

  1. Allen, W. E. 1941. Twenty years' statistical studies of marine plankton dinoflagellates of southern California. Am. Midl. Nat. 26:603-635. https://doi.org/10.2307/2420738
  2. 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
  3. Anderson, D. M., Glibert, P. M. & Burkholder, J. M. 2002. Harmful algal blooms and eutrophication: nutrient sources, composition, and consequences. Estuaries 25:704-726. https://doi.org/10.1007/BF02804901
  4. Carpenter, E. J. & Guillard, R. R. L. 1971. Intraspecific differences in nitrate half-saturation constants for three species of marine phytoplankton. Ecology 52:183-185. https://doi.org/10.2307/1934753
  5. Cochlan, W. P. & Harrison, P. J. 1991. Kinetics of nitrogen (nitrate, ammonium and urea) uptake by the picoflagellate Micromonas pusilla (Prasinophyceae). J. Exp. Mar. Biol. Ecol. 153:129-141. https://doi.org/10.1016/0022-0981(91)90220-Q
  6. Collos, Y., Gagne, C., Laabir, M., Vaquer, A., Cecchi, P. & Souchu, P. 2004. Nitrogenous nutrition of Alexandrium catenella (Dinophyceae) in cultures and in Thau laggon, Southern France. J. Phycol. 40:96-103. https://doi.org/10.1046/j.1529-8817.2004.03034.x
  7. Cullen, J. J. & Horrigan, S. G. 1981. Effects of nitrate on the diurnal vertical migration, carbon to nitrogen ratio, and the photosynthetic capacity of the dinoflagellate Gymnodinium splendens. Mar. Biol. 62:81-89. https://doi.org/10.1007/BF00388169
  8. Dortch, Q., Thompson, P. A. & Harrison, P. J. 1991. Variability in nitrate uptake kinetics in Thalassiosira pseudonana (Bacillariophyceae). J. Phycol. 27:35-39. https://doi.org/10.1111/j.0022-3646.1991.00035.x
  9. Eppley, R. W. 1973. Nitrate uptake. In Stein, J. R., Hellebust, J. A. & Craigie, J. S. (Eds.) Handbook of Phycological Methods: Physiological and Biochemical Methods. Vol. 2. Cambridge University Press, Cambridge, pp. 401-409.
  10. Eppley, R. W. & Coatsworth, J. L. 1968. Uptake of nitrate and nitrite by Ditylum brightwellii-kinetics and mechanisms. J. Phycol. 4:151-156. https://doi.org/10.1111/j.1529-8817.1968.tb04689.x
  11. 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. https://doi.org/10.4319/lo.1969.14.6.0912
  12. Eppley, R. W. & Thomas, W. H. 1969. Comparison of half-saturation constants for growth and nitrate uptake of marine phytoplankton. J. Phycol. 5:375-379. https://doi.org/10.1111/j.1529-8817.1969.tb02628.x
  13. Fan, C., Glibert, P. M. & Burkholder, J. M. 2003. Characterization of the affinity for nitrogen, uptake kinetics, and environmental relationships for Prorocentrum minimum in natural blooms and laboratory cultures. Harmful Algae 2:283-299. https://doi.org/10.1016/S1568-9883(03)00047-7
  14. Fu, F. X., Tatters, A. O. & Hutchins, D. A. 2012. Global change and the future of harmful algal blooms in the ocean. Mar. Ecol. Prog. Ser. 470:207-233. https://doi.org/10.3354/meps10047
  15. 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. https://doi.org/10.1016/j.hal.2011.10.023
  16. Glibert, P. M., Icarus Allen, J., Artioli, Y., Beusen, A., Bouwman, L., Harle, J., Holmes, R. & Holt, J. 2014. Vulnerability of coastal ecosystems to changes in harmful algal bloom distribution in response to climate change: projections based on model analysis. Glob. Chang. Biol. 20:3845-3858. https://doi.org/10.1111/gcb.12662
  17. Guillard, R. R. 1975. Culture of phytoplankton for feeding marine invertebrates. In Smith, W. L. & Chanley, M. H. (Eds.) Culture of Marine Invertebrate Animals. Springer, New York, pp. 29-60.
  18. 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
  19. Hasle, G. R. 1950. Phototactic vertical migration in marine dinoflagellates. Oikos 2:162-175. https://doi.org/10.2307/3564790
  20. Herndon, J. & Cochlan, W. P. 2007. Nitrogen utilization by the raphidophyte Heterosigma akashiwo: growth and uptake kinetics in laboratory cultures. Harmful Algae 6:260-270. https://doi.org/10.1016/j.hal.2006.08.006
  21. Hu, H., Zhang, J. & Chen, W. 2011. Competition of bloom-forming marine phytoplankton at low nutrient concentrations. J. Environ. Sci. 23:656-663. https://doi.org/10.1016/S1001-0742(10)60459-7
  22. Hu, Z., Duan, S., Xu, N. & Mulholland, M. R. 2014. Growth and nitrogen uptake kinetics in cultured Prorocentrum donghaiense. PLoS ONE 9:e94030. https://doi.org/10.1371/journal.pone.0094030
  23. 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
  24. 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
  25. Jeong, H. J., Yoo, Y. D., Park, J. Y., Song, J. Y., Kim, S. T., Lee, S. H., Kim, K. Y. & Yih, W. H. 2005. Feeding by the phototrophic red-tide dinoflagellates: five species newly revealed and six species previously known to be mixotrophic. Aquat. Microb. Ecol. 40:133-155. https://doi.org/10.3354/ame040133
  26. Ji, R. & Franks, P. J. 2007. Vertical migration of dinoflagellates: model analysis of strategies, growth, and vertical distribution patterns. Mar. Ecol. Prog. Ser. 344:49-61. https://doi.org/10.3354/meps06952
  27. Ji, X., Han, X., Zheng, L., Yang, B., Yu, Z. & Zou, J. 2011. Allelopathic interactions between Prorocentrum micans and Skeletonema costatum or Karenia mikimotoi in laboratory cultures. Chin. J. Oceanol. Limnol. 29:840-848. https://doi.org/10.1007/s00343-011-0512-x
  28. Kang, N. S., Lee, K. H., Jeong, H. J., Yoo, Y. D., Seong, K. A., Potvin, E., 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
  29. Killberg-Thoreson, L., Mulholland, M. R., Heil, C. A., Sanderson, M. P., O'Neil, J. M. & Bronk, D. A. 2014. Nitrogen uptake kinetics in field populations and cultured strains of Karenia brevis. Harmful Algae 38:73-85. https://doi.org/10.1016/j.hal.2014.04.008
  30. Kudela, R. M. & Cochlan, W. P. 2000. Nitrogen and carbon uptake kinetics and the influence of irradiance for a red tide bloom off southern California. Aquat. Microb. Ecol. 21:31-47. https://doi.org/10.3354/ame021031
  31. Kudela, R. M., Lane, J. Q. & Cochlan, W. P. 2008a. The potential role of anthropogenically derived nitrogen in the growth of harmful algae in California, USA. Harmful Algae 8:103-110. https://doi.org/10.1016/j.hal.2008.08.019
  32. Kudela, R. M., Ryan, J. P., Blakely, M. D., Lane, J. Q. & Peterson, T. D. 2008b. Linking the physiology and ecology of Cochlodinium to better understand harmful algal bloom events: a comparative approach. Harmful Algae 7:278-292. https://doi.org/10.1016/j.hal.2007.12.016
  33. Kudela, R. M., Seeyave, S. & Cochlan, W. P. 2010. The role of nutrients in regulation and promotion of harmful algal blooms in upwelling systems. Prog. Oceanogr. 85:122-135. https://doi.org/10.1016/j.pocean.2010.02.008
  34. 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
  35. Li, J., Glibert, P. M. & Zhou, M. 2010. Temporal and spatial variability in nitrogen uptake kinetics during harmful dinoflagellate blooms in the East China Sea. Harmful Algae 9:531-539. https://doi.org/10.1016/j.hal.2010.03.007
  36. Lim, A. S., Jeong, H. J., Jang, T. Y., Jang, S. H. & Franks, P. J. S. 2014. Inhibition of growth rate and swimming speed of the harmful dinoflagellate Cochlodinium polykrikoides by diatoms: implications for red tide formation. Harmful Algae 37:53-61. https://doi.org/10.1016/j.hal.2014.05.003
  37. Lomas, M. W. & Glibert, P. M. 2000. Comparisons of nitrate uptake, storage, and reduction in marine diatoms and flagellates. J. Phycol. 36:903-913. https://doi.org/10.1046/j.1529-8817.2000.99029.x
  38. MacIsaac, J. J., Grunseich, G. S., Glober, H. E. & Yentsch, C. M. 1979. Light and nutrient limitation in Gonyaulax excavata: nitrogen and carbon trace results. In Taylor, D. L. & Selige, H. H. (Eds.) Toxic Dinoflagellate Blooms. Elsevier, New York, pp. 107-110.
  39. Maguer, J. -F., L'Helguen, S., Madec, C., Labry, C. & Le Corre, P. 2007. Nitrogen uptake and assimilation kinetics in Alexandrium minutum (Dynophyceae): effect of N-limited growth rate on nitrate and ammonium interactions. J. Phycol. 43:295-303. https://doi.org/10.1111/j.1529-8817.2007.00334.x
  40. Nakamura, Y. & Watanabe, M. M. 1983. Nitrate and phosphate uptake kinetics of Chattonella antiqua grown in light/dark cycles. J. Oceanogr. Soc. Jpn. 39:167-170. https://doi.org/10.1007/BF02070260
  41. 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
  42. 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
  43. Pena-Manjarrez, J. L., Helenes, J., Gaxiola-Castro, G. & Orellana-Cepeda, E. 2005. Dinoflagellate cysts and bloom events at Todos Santos Bay, Baja California, Mexico, 1999-2000. Cont. Shelf Res. 25:1375-1393. https://doi.org/10.1016/j.csr.2005.02.002
  44. Pybus, C. 1990. Blooms of Prorocentrum micans (Dinophyta) in the Galway Bay area. J. Mar. Biol. Assoc. U. K. 70:697-705. https://doi.org/10.1017/S0025315400058987
  45. Qi, Y. Z. & Zhu, C. J. 1994. A comparative study of nitrate uptake kinetics by two red tide causative algae. Asian Mar. Biol. 11:103-106.
  46. Seeyave, S., Probyn, T. A., Pitcher, G. C., Lucas, M. I. & Purdie, D. A. 2009. Nitrogen nutrition in assemblages dominated by Pseudo-nitzschia spp., Alexandrium catenella and Dinophysis acuminata off the west coast of South Africa. Mar. Ecol. Prog. Ser. 379:91-107. https://doi.org/10.3354/meps07898
  47. Sinclair, G., Kamykowski, D. & Glibert, P. M. 2009. Growth, uptake, and assimilation of ammonium, nitrate, and urea, by three strains of Karenia brevis grown under low light. Harmful Algae 8:770-780. https://doi.org/10.1016/j.hal.2009.02.006
  48. Sinclair, G. A., Kamykowski, D., Milligan, E. & Schaeffer, B. 2006. Nitrate uptake by Karenia brevis. I. Influences of prior environmental exposure and biochemical state on diel uptake of nitrate. Mar. Ecol. Prog. Ser. 328:117-124. https://doi.org/10.3354/meps328117
  49. Shankle, A. M., Mayali, X. & Franks, P. J. S. 2004. Temporal patterns in population genetic diversity of Prorocentrum micans (Dinophyceae). J. Phycol. 40:239-247. https://doi.org/10.1111/j.1529-8817.2004.03021.x
  50. Shumway, S. E. 1990. A review of the effects of algal blooms on shellfish and aquaculture. J. World Aquac. Soc. 21:65-104. https://doi.org/10.1111/j.1749-7345.1990.tb00529.x
  51. 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
  52. Suzuki, L. & Johnson, C. H. 2001. Algae know the time of day: circadian and photoperiodic programs. J. Phycol. 37:933-942. https://doi.org/10.1046/j.1529-8817.2001.01094.x
  53. Uchida, T. 1981. The relationships between Prorocentrum micans-growth and its ecological environment. Sci. Pap. Inst. Algol. Res. Fac. Sci. Hokkaido Univ. 7:17-76.
  54. Van Dolah, F. M., Lidie, K. B., Morey, J. S., Brunelle, S. A., Ryan, J. C., Monroe, E. A. & Haynes, B. L. 2007. Microarray analysis of diurnal- and circadian-regulated genes in the Florida red-tide dinoflagellate Karenia brevis (Dinophyceae). J. Phycol. 43:741-752. https://doi.org/10.1111/j.1529-8817.2007.00354.x
  55. Yamamoto, T., Oh, S. J. & Kataoka, Y. 2004. Growth and uptake kinetics for nitrate, ammonium and phosphate by the toxic dinoflagellate Gymnodinium catenatum isolated from Hiroshima Bay, Japan. Fish. Sci. 70:108-115. https://doi.org/10.1111/j.1444-2906.2003.00778.x
  56. Zheng-fang, W., Qing, Z. & Min, G. 1995. The effects of nitrogen, phosphorus, vitamins and trace metals on the growth of the red tide organism Prorocentrum micans. Chin. J. Oceanol. Limnol. 13:338-342. https://doi.org/10.1007/BF02889468

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