Journal of the Korean Society of Marine Environment & Safety (해양환경안전학회지)

The Korean Society of Marine Environment and safety (해양환경안전학회)
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Effects of Dissolved Inorganic and Organic Nutrient (Nitrogen and Phosphorus) on the Growth of Dinoflagellate Alexandrium affine

와편모조류 Alexandrium affine의 생장에 미치는 용존태 무기 및 유기 영양염(질소와 인)의 영향

  • Oh, Seok Jin (Department of Oceanography, Pukyong National University) ;
  • Kim, Ji Hye (Department of Oceanography, Pukyong National University) ;
  • Park, Kyung Woo (Oceanic Climate and Ecology Research Division, National Institute of Fisheries Science) ;
  • Kim, Seok-Yun (Department of Oceanography, Pukyong National University)
  • 오석진 (부경대학교 해양학과) ;
  • 김지혜 (부경대학교 해양학과) ;
  • 박경우 (국립수산과학원 기후변화연구과) ;
  • 김석윤 (부경대학교 해양학과)
  • Received : 2021.07.12
  • Accepted : 2021.08.27
  • Published : 2021.08.31
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Abstract

In this study, we investigated the effects of dissolved inorganic and organic nutrient on the growth of dinoflagellate Alexandrium affine (LIMS-PS-2345). The maximum uptake rates (ρmax) and half saturation constants (Ks) calculated from the uptake kinetics experiment were 77.0 pmol/cell/hr, 17.6 μM for nitrate and 15.5 pmol/cell/hr, 3.88 μM for phosphate, respectively. These results suggested that this species has high inorganic nutrient demand and a low affinity for inorganic nutrients. During the utilization of organic nutrients for A. affine, growth rates of experimental groups added by organic nitrogen (urea and glycine) and phosphorus (adenosine triphosphate and glycerol phosphate) were above 70 %, compared to the experimental groups added by inorganic nutrients. Thus, A. affine may need to utilize organic nutrients to understand the dominant strategy and advantageous position in the interspecific competition within low inorganic nutrient environments.

본 연구에서는 와편모조류 Alexandrium affine(LIMS-PS-2345)의 생장에 미치는 용존태 무기 및 유기 영양염의 영향을 조사하였다. 영양염 흡수 동력학 실험에서 A. affine의 최대흡수속도(ρmax)와 반포화상수(Ks)는 질산염에서 77.0 pmol/cell/hr과 17.6 μM, 인산염에서 15.5 pmol/cell/hr과 3.88 μM로 산출되어, 무기영양염에 대하여 높은 요구량 및 낮은 친화성을 가지고 있는 것으로 나타났다. 유기 영양염에 따른 A. affine의 생장속도를 확인한 결과, 유기 질소 urea, glycine와 유기 인 adenosine triphosphate(ATP), glycerol phosphate(Glycerol-P) 첨가구에서 무기 영양염 첨가구의 70 % 이상 생장속도를 보였다. 따라서 낮은 무기 영양염 환경에서 A. affine의 우점화와 종간경쟁에서 우위를 위해서는 용존태 유기 영양염의 이용이 필요할 것으로 생각된다.

Keywords

Acknowledgement

이 논문은 부경대학교 자율창의학술연구비(2019년)에 의하여 연구되었습니다.

References

  1. Anderson, D. M., S Chisholm, and C. Watras(1983), Importance of life cycle events in the population dynamics of Gonyaulax tamarensis, Marine Biology, Vol. 76, No. 2, pp. 179-189. https://doi.org/10.1007/BF00392734
  2. Anderson, D. M., T. J. Alpermann, A. D. Cembella, Y. Collos, E. Masseret, and M. Montresor(2012), The globally distributed genus Alexandrium: Multifaceted roles in marine ecosystems and impacts on human health, Harmful Algae, Vol. 14, pp. 10-35. https://doi.org/10.1016/j.hal.2011.10.012
  3. Auro, M. E. and W. P. Cochlan(2013), Nitrogen utilization and toxin production by two diatoms of the Pseudo-nitzschia pseudodelicatissima complex: P. cuspidata and P. fryxelliana, Journal of Phycology, Vol. 49, No. 1, pp. 156-169. https://doi.org/10.1111/jpy.12033
  4. Baek, S. H., S. Shimode, M. S. Han, and T. Kikuchi(2008), Growth of dinoflagellates, Ceratium furca and Ceratium fusus in Sagami Bay, Japan: The role of nutrients, Harmful Algae, Vol. 7, pp. 729-739. https://doi.org/10.1016/j.hal.2008.02.007
  5. Balech, E.(1995) The Genus Alexandrium (Halim) (Dinoflagellata), Sherkin Island Marine Station, p. 151.
  6. Bronk, D. A.(2002) Dynamics of DON, In: Hansell D. A. and A. C. Craig (eds), Biogeochemistry of marine dissolved organic matter, Academic Press, MA, pp. 153-247.
  7. Cho, C. H.(1978), On the Gonyaulax red tide in Jinhae bay, Bulletin of the Korean Fisheries Society, Vol. 11, No. 2, pp. 111-114.
  8. Collier, J. L., B. Brahamsha, and B. Palenik(1999), The marine cyanobacterium Synechococcus sp. WH7805 requires urease (urea amidohydrolase, EC 3.5.1.5) to utilize urea as a nitrogen source: molecular-genetic and biochemical analysis of the enzyme, Microbiology, Vol. 145, Vol. 2, pp. 447-459. https://doi.org/10.1099/13500872-145-2-447
  9. Collos, Y., C. Gagne, M. Laabi, A. Vaquer, P. Cecchi, and P. Souchu(2004), Nitrogenous nutrition of Alexandrium catenella (Dinophyceae) in cultures and in Thau lagoon, Southern France, Journal of Phycology, Vol. 40, pp. 96-103. https://doi.org/10.1046/j.1529-8817.2004.03034.x
  10. Cowey, C. B. and E. D. S. Corner(1966), The amino acid composition of certain unicellular algae, and of the faecal pellets produced by Calanus finmarchicus when feeding on them, In: Barnes, H. (ed), Some contemporary studies in marine science, George Allen & Unwin Ltd., London, pp. 225-231.
  11. Dugdale, R. C.(1967), Nutrient limitation in the sea: dynamics, identification and significance, Limnology and Oceanography, Vol. 12, No. 4, pp. 685-695. https://doi.org/10.4319/lo.1967.12.4.0685
  12. Dyhrman, S. T. and D. M. Anderson(2003), Urease activity in cultures and field populations of the toxic dinoflagellate Alexandrium, Limnology and Oceanography, Vol. 48, No. 2, pp. 647-655. https://doi.org/10.4319/lo.2003.48.2.0647
  13. Egge, J. K.(1998), Are diatoms poor competitors at low phosphate concentrations? Journal of Marine Systems, Vol. 16, No. 3, pp. 191-198. https://doi.org/10.1016/S0924-7963(97)00113-9
  14. Eppley, R. W., J. N. Rogers, and J. J. McCarthy(1969), Half-saturation constant for uptake of nitrate and ammonium by marine phytoplankton, Limnology and Oceanography, Vol. 14, No. 6, pp. 912-920. https://doi.org/10.4319/lo.1969.14.6.0912
  15. Fukuyo, Y.(1985), Morphology of Protogonyaulax tamarensis (Lebour) Taylor and Protogonyaulax catenella (Whedon and Kofoid) Taylor from Japanese coastal waters, Bulletin of Marine Science-Miami, Vol. 37, No. 2, pp. 529-537.
  16. Garate-Lizarraga, I., D. Lopez-Cortes, J. Bustillos-Guzman, F. Hernandez-Sandoval, and I. Murillo-Murillo(2002), Physicochemical characteristics and phytoplankton biomass during El Nino 1997-1998 in Bahia Concepcion, Gulf of California, American Society of Limnology and Oceanography, Albuquerque, p. 56.
  17. Gentien, P., P. Donaghay, H. Yamazaki, R. Raine, B. Reguera, and T. Osborn(2005), Harmful algal blooms in stratified environments, Oceanography, Vol. 18, No. 2, pp. 172-183. https://doi.org/10.5670/oceanog.2005.52
  18. Guillard, R. R. L. and J. H. Ryther(1962), Studies of marine planktonic diatoms: I. Cyclotella nana Hustedt and Detonula conjervaces (Cleve) Gran, Canadian Journal of Microbiology, Vol. 8, No. 2, pp. 229-239. https://doi.org/10.1139/m62-029
  19. Hallegraeff, G. M.(2010), Ocean climate change, phytoplankton community responses, and harmful algal blooms: a formidable predictive challenge, Journal of Phycology, Vol. 46, pp. 220-235. https://doi.org/10.1111/j.1529-8817.2010.00815.x
  20. Hallegraeff, G. M., C. J. Bolch, S. I. Blackburn, and Y. Oshima(1991), Species of the toxigenic dinoflagellate genus Alexandrium in southeastern Australian waters, Botanica Marina, Vol. 34, pp. 575-587.
  21. Harrison, P. J., J. S. Parslow, and H. L. Conway(1989), Determination of nutrient uptake kinetic parameters: a comparison of methods, Marine Ecology Progress Series, Vol. 52, pp. 301-312. https://doi.org/10.3354/meps052301
  22. Kim, D. I.(2003), Physiological and ecological studies on harmful red tide dinoflagellate Cochlodinium polykrikoides (Margalef). Ph. D. Thesis, Kyushu University, Fukuoka, pp. 154.
  23. Kim, D. I., T. Matsubara, S. J. Oh, Y. Shimasaki, Y. Oshima and T. Honjo(2007), Effects of nitrogen and phosphate sources on the utilization and growth kinetics of the harmful dinoflagellate Cochlodinium polykrikoides isolated from Yatsushiro Sea, Japan, Nippon Suisan Gakkaishi, Vol. 73, No. 4, pp. 711-717. https://doi.org/10.2331/suisan.73.711
  24. Kim, H. G., J. S. Park, and S. G. Lee(1990), Coastal algal blooms caused by the cyst-forming dinoflagellates, Bulletin of the Korean Fisheries Society, Vol. 23, No. 6, pp. 468-474.
  25. Kim, J. H., S. J. Oh, and S. -Y. Kim(2019), The effect of temperature, salinity and irradiance on the growth of Alexandrium affine (Dinophyceae) isolated from Southern Sea of Korea, Journal of the Korean Society of Marine Environment & Safety, Vol. 25, No. 2, pp. 229-236. https://doi.org/10.7837/kosomes.2019.25.2.229
  26. Kim, S.(2006), Patterns in host range for two strains fo Amoebophrya (Dinophyta) inffecting thecate dinoflagellates: Amoebophyra spp. ex Alexandrium affine ex Gonyaulax polygramma, Journal of Phycology, Vol. 42, pp. 1170-1173. https://doi.org/10.1111/j.1529-8817.2006.00277.x
  27. Kwon, H. G., H. J. Kim, H. -S. Yang, and S. J. Oh(2014), The importance of dissolved organic nutrients on the interspecific competition between the harmful dinoflagellate Cochlodinium polykrikoides and the diatom Skeletonema sp., The Sea, Vol. 19, No. 4, pp. 232-242. https://doi.org/10.7850/jkso.2014.19.4.232
  28. Kwon, H. G., J. A. Park, H. -S. Yang, and S. J. Oh(2013), Dominance and survival strategy of toxic dinoflagellate Alexandrium tamarense and Alexandium catenella under dissolved inorganic nitrogen-limited conditions, Journal of the Korean Society for Marine Environment and Energy, Vol. 16, No. 1, pp. 25-35. https://doi.org/10.7846/JKOSMEE.2013.16.1.25
  29. Kwon, H. K., S. J. Oh, and H. -S. Yang(2011), Ecological significance of alkaline phosphatase activity and phosphatasehydrolyzed phosphorus in the northern part of Gamak Bay, Korea, Marine Pollution Bulletin, Vol. 62, No. 11, pp. 2476-2482. https://doi.org/10.1016/j.marpolbul.2011.07.027
  30. Lartigue, J., E. L. E. Jester, R. W. Dickey, and T. A. Villareal(2009), Nitrogen source effects on the growth and toxicity of two strains of the ciguatera-causing dinoflagellate Gambierdiscus toxicus, Harmful Algae, Vol. 8, No. 5, pp. 781-791. https://doi.org/10.1016/j.hal.2008.05.006
  31. Leong, S. C. Y. and S. Taguchi(2004), Response of the dinoflagellate Alexandrium tamarense to a range of nitrogen sources and concentrations: growth rate, chemical carbon and nitrogen, and pigments, Hydrobiologia, Vol. 515, pp. 215-224. https://doi.org/10.1023/B:HYDR.0000027331.49819.a4
  32. Li, T., R. Yu, and M. Zhou(2011), Short-term effects of different nitrogen substrates on growth and toxin production of dinoflagellate Alexandrium catenella Balech (strain ACDH), Harmful Algae, Vol. 12, pp. 46-54. https://doi.org/10.1016/j.hal.2011.08.011
  33. Lieberman, O. S., M. Shilo, and J. van Rijn(1994), The physiological ecology of a freshwater dinoflagellate bloom population: vertical migration, nitrogen limitation and nutrient uptake kinetics, Journal of Phycology, Vol. 30, pp. 964-971. https://doi.org/10.1111/j.0022-3646.1994.00964.x
  34. Lim, W. A., W. J. Go, K. Y. Kim, and J. W. Park(2020), Variation in harmful algal blooms in Korean coastal water since 1970, Journal of the Korean Society of Marine Environment & Safety, Vol. 26, No. 5, pp. 523-530. https://doi.org/10.7837/kosomes.2020.26.5.523
  35. Lomas, M. W. and P. M. Gilbert(2000), Comparison of nitrate uptake, storage, and reduction in marine diatoms and flagellates, Journal of Phycology, Vol. 36, pp. 903-913. https://doi.org/10.1046/j.1529-8817.2000.99029.x
  36. MacIsaac, J. J., G. S. Grunseich, H. E. Glover, and C. M. Yentsch(1979), Light and nutrient limiting in Gonyaulax excavata: Nitrogen and carbon trace results, In: Taylor, D. L. and H. H. Selige (eds.), Toxic Dinoflagellate Blooms, Elsevier, New York, pp. 107-110.
  37. Nagasoe, S., T. Shikata, Y. Yamasaki, T. Matsubara, Y. Shimasaki, Y. Ohima, and T. Honjo(2010), Effects of nutrients on growth of the red-tide dinoflagellate Gyrodinium instriatum Freudenthal et Lee and a possible link to blooms of this species, Hydorbiologia, Vol. 651, pp. 225-238. https://doi.org/10.1007/s10750-010-0301-0
  38. Nakamura, Y.(1985), Ammonium uptake kinetics and interaction between nitrate and ammonium uptake in Chatonella antique, Journal of the Oceanographical Society of Japan, Vol. 41, pp. 33-38. https://doi.org/10.1007/BF02109929
  39. Ngoc, N. L.(2004), An autecological study of the potentially toxic dinoflagellate Alexandrium affine isolated from Vietnamese water, Harmful algae, Vol. 3, No. 2, pp. 117-129. https://doi.org/10.1016/S1568-9883(03)00062-3
  40. Nishijima, T., Y. Hata, and S. Yamauchi(1990), Physiological ecology of Prorocentrum triestinum, Bulletin of the Japanese Society of Scientific Fisheries, Vol. 55, No. 11, pp. 2009-2014. https://doi.org/10.2331/suisan.55.2009
  41. Oh, S. J., H. G. Kwon, and H. -S. Yang(2010), Alkaline phosphatase activity and utilization of dissolved organic phosphorus by phytoplankton isolated from Korean coastal waters, The Sea, Vol. 15, No. 1, pp 16-24.
  42. Oh, S. J., Y. Matsuyama, T. Yamamoto, M. Nakajima, H. Takatsuzi, and K. Hujisawa(2005), Recent developments and causes of harmful dinoflagellates blooms in the Seto lnland Sea - Ecological importance of dissolved organic phosphorus (DOP). Bulletin on Coastal Oceanography, Vol. 43, pp. 85-95.
  43. Park, J., H. J. Jeong, Y. D. Yoo, and E. Y. Yoon(2013), Mixotrophic dinoflagellate red tides in Korean waters: distribution and ecophysiology, Harmful Algae, Vol. 30S, pp. S28-S40. https://doi.org/10.1016/j.hal.2013.10.004
  44. Park, T. G. and Y. S. Kong(2009), Temporal changes in abundances of the toxic dinoflagellate Alexandrium minutum (Dinophyceae) in Chinhae Bay, Korea, Journal of the Environmental Sciences, Vol. 18, No. 12, pp. 1331-1338. https://doi.org/10.5322/JES.2009.18.12.1331
  45. Porter, K. G. and Y. S. Feig(1980), The use of DAPI for identifying and counting aquatic microflora, Limnology and Oceanography, Vol. 25, No. 5, pp. 943-948. https://doi.org/10.4319/lo.1980.25.5.0943
  46. Provasoil, L., K. Shiraishi, and J. R. Lance(1959), Nutritional idiosyncrasies of Artemia and Tigriopus in monoxenic culture, Annals of the New York Academy of Sciences, Vol. 77, pp. 250-261. https://doi.org/10.1111/j.1749-6632.1959.tb36905.x
  47. Sherr, E. B., B. F. Sherr, T. Berman, and J. M. McCarthy (1982), Differences in nitrate and ammonia uptake among components of a phytoplankton population, Journal of Plankton Research, Vol. 4, No. 4, pp. 961-965. https://doi.org/10.1093/plankt/4.4.961
  48. Shin, H. H., S. H. Baek, L. Zhun, M. S. Han, S. J. Oh, S. H. Youn, Y. S. Kim, D. K. Kim, and W. A. Lim(2014), Resting cysts, and effects of temperature and salinity on the growth of vegetative cells of the potentially harmful species Alexandrium insuetum Balech (Dinophyceae), Harmful Algae, Vol. 39, pp. 175-184. https://doi.org/10.1016/j.hal.2014.07.012
  49. Shin, H. H., Y. H. Yoon, and K. Matsuoka(2007), Modern dinoflagellate cycsts distribution off the eastern part of Geoje Island, Korea, Ocean Science Journal, Vol. 42, No. 1, pp. 31-39. https://doi.org/10.1007/BF03020908
  50. Shin, H. H., Y. H. Yoon, Y. O. Kim, and K. Matsuoka(2011), Dinoflagellate cysts in surface sediments from southern coast of Korea, Estuaries and Coasts, Vol. 34, No. 4, pp. 712-725. https://doi.org/10.1007/s12237-011-9373-y
  51. Sidabutar, T., D. P. Praseno, and Y. Fukuyo(2000), Status of harmful algal blooms in Indonesian waters, 9th International Conference on Harmful Algal Blooms, Conference Abstracts, Tasmania, p. 220.
  52. Steidinger, K. A., G. A. Vargo, P. A. Tester, and C. R Tomas(1998), Bloom dynamics and physiology of Gymnodinium breve with emphasis on Gulf of Mexico, In: Anderson, D. M., A. D. Cembella and G. M. Hallegraeff (eds.), Physiological Ecology of Harmful Algal Blooms, Springer, New York, pp. 135-153.
  53. Subong, B. J. J., G. A. Benico, A. K. L. Sulit, C. O. Mendoza, L. J. Cruz, R. V. Azanza, and E. C. Jimenez(2017), Toxicity and protein expression of Alexandrium species collected in the Philippine Water, Philippine Journal of Science, Vol. 146, No. 40, pp. 425-436.
  54. Tomas, C. R.(1979), Olisthodiscus luteus (Chrysophyceae). III. Uptake and utilization of nitrogen and phosphorus, Journal of Phycology, Vol. 15, No. 1, pp. 5-12. https://doi.org/10.1111/j.0022-3646.1979.00005.x
  55. Vera, G., S. Fraga, J. M. Franco, and G. Sanchez Rivas(1999) Primer registro en el Peru del dinoflagelado Alexandrium af ine Inoue y Fukuyo, Informe Progresivo, Instituto del, No. 105, pp 3-12.
  56. White, A. and S. Dyhrman(2013), The marine phosphorus cycle, Frontiers in Microbiology, Vol. 4, pp. 1-2. https://doi.org/10.3389/fmicb.2013.00001
  57. Xu, J., A. Y. T. Ho, L. He, K. Yin, C. Hung, N. Choi, P. K. S. Lam, R. S. S. Wu, D. M. Anderson, and P. J. Harrison(2012), Effects of inorganic and organic nitrogen and phosphorus on the growth and toxicity of two Alexandrium species from Hong Kong, Harmful Algae, Vol. 16, pp. 89-97. https://doi.org/10.1016/j.hal.2012.02.006
  58. Yamaguchi, H., H. Sakou, K. Fukami, M. Adachi, M. Yamaguchi, and N. Nishijima(2005), Utilization of organic phosphorus and production of alkaline phosphatase by the marine phytoplankton, Heterocapsa circularisquama, Fibrocapsa japonica and Chaetoceros ceratosporum. Plankton Biology & Ecology, Vol. 52, No. 2, pp. 65-75.
  59. Yamaguchi, H., S. Sakamoto, and M. Yamaguchi(2008), Nutrition and growth kinetics in nitrogen- and phosphorus-limited cultures of the novel red tide flagellate Chattonella ovata (Raphidophyceae), Harmful Algae, Vol. 7, pp. 26-32. https://doi.org/10.1016/j.hal.2007.05.011
  60. Yamamoto, T., S. J. Oh, and Y. Kataoka(2004), Growth and uptake kinetics for nitrate, ammonium and phosphate by the toxic dinoflagellate Gymnodinium catenatum isolated from Hiroshima Bay, Japan, Fisheries Science, Vol. 70, No. 1, pp. 108-115. https://doi.org/10.1111/j.1444-2906.2003.00778.x
  61. Yoshida, M., C. V. Thuoc, K. Matsuoka, T. Ogata, Y. Fukuyo, and N. Chu(2000), The occurrence of PSP and DSP causative dinoflagellates in northern Vietnamese coastal waters, 9th International Conference on Harmful Algal Blooms, Conference Abstracts, Tasmania, p. 248.