DOI QR코드

DOI QR Code

The Importance of Dissolved Organic Nutrients on the Interspecific Competition between the Harmful Dinoflagellate Cochlodinium polykrikoides and the Diatom Skeletonema sp.

유해 와편모조류 Cochlodinium polykrikoides와 규조류 Skeletonema sp.의 종간경쟁에서 용존 유기 영양염의 중요성

  • Kwon, Hyeong Kyu (Korea Inter-University Institute of Ocean Science, Pukyong National University) ;
  • Kim, Hyun Jung (Department of Oceanography, Pukyong National University) ;
  • Yang, Han-Soeb (Department of Oceanography, Pukyong National University) ;
  • Oh, Seok Jin (Department of Oceanography, Pukyong National University)
  • Received : 2014.08.12
  • Accepted : 2014.10.11
  • Published : 2014.11.28

Abstract

We investigated the interspecific competition between the harmful dinoflagellate Cochlodinium polykrikoides and diatom Skeletonema sp. based on the utilization and uptake of dissolved organic nutrients. C. polykrikoides and S. costatum were able to grow using dissolved organic nitrogen (DON) and dissolved organic phosphorus (DOP) as well as dissolved inorganic nitrogen (DIN) and dissolved inorganic phosphorus (DIP). This result indicates that the utilization of dissolved organic nutrients may play a role in surviving strategy in the DIN or DIP-limited environments. The half-saturation constants (Ks) of urea and glycerophosphate (glycero-P) calculated from uptake kinetics experiment of C. polykrikoides was lower than those of Skeletonema sp. This result indicates that Skeletonema sp. have higher affinity for dissolved organic nutrients, such as urea and glycero-P, than C. polykrikoides. Although Skeletonema sp. have higher affinity of dissolved organic nutrients, C. polykrikoides could effectively uptake for urea and glycero-P at sub-saturating nutrient concentrations (${\alpha}$ (${\rho}_{max}/Ks$) of C. polykrikoides was higher than Skeletonema sp.. Therefore, C. polykrikoides by utilization and effectively uptake of dissolved organic nutrients under monoculture may have an advantageous position in the interspecific competition with Skeletonema sp. in the low nutrient environments.

본 연구는 유해 와편모조류 Cochlodinium polykrikoides와 규조류 Skeletonema sp.의 용존 유기 영양염에 대한 이용 및 흡수능력을 통해서 종간 경쟁관계를 파악하였다. C. polykrikoides와 Skeletonema sp.는 용존 무기 질소와 무기인 이외에 다양한 용존 유기 질소와 유기 인을 이용하여 성장하였다. 이는 용존 무기 질소 또는 무기 인이 제한 영양염으로 작용하는 환경에서 중요한 생존전략으로 작용할 것이다. Urea와 glycerophospahte(glycero-P)의 흡수동력학 실험으로부터 도출된 반포화상수(Ks) 값은 C. polykrikoides가 Skeletonema sp.에 비해서 낮은 값을 보였다. 이는 Skeletonema sp.가 C. polykrikoides에 비해서 urea와 glycero-P와 같은 유기 영양염에 대한 친화성이 높음을 의미한다. 하지만 Skeletonema sp.가 유기 영양염에 대한 친화성이 높을지라도 C. polykrikoides가 ${\alpha}$ (${\rho}_{max}/Ks$) 값이 높아, 저농도의 영양염 조건(

Keywords

References

  1. Antia, N.J., P.J. Harrison and L. Oliveira, 1991. Phycological reviews: the role of dissolved organic nitrogen in phytoplankton nutrition, cell biology, and ecology. Phycol., 30: 1-89. https://doi.org/10.2216/i0031-8884-30-1-1.1
  2. Auro, M.E. and W.P. Cochlan, 2012. Nitrogen utilization and toxin production by two diatoms of the Pseudo-nitzschia pseudodelicatissima complex: P. cuspidata and P. fryxelliana. J. Phycol., 49: 156-169.
  3. Baba, T., S. Hiyama and T. Tainaka, 2001. Vertical migration of the toxic dinoflagellate Gymnodinium catenatum and toxicity of cultures oyster in Senzaki Bay, Yamaguchi Prefecture. Bull. Plankton Soc. Jpn., 48: 95-99.
  4. Benitez-Nelson, C.R., 2000. The biogeochemical cycling of phosphorus in marine systems. Earth Sci. Rev., 51: 109-135. https://doi.org/10.1016/S0012-8252(00)00018-0
  5. Berman, T., and D.A. Bronk, 2003. Dissolved organic nitrogen: A dynamic participant in aquatic ecosystems. Aquat. Microbial Ecol., 31: 279-305. https://doi.org/10.3354/ame031279
  6. Brand, L.E., R.R.L. Guillard and L.S. Murphy, 1981. A method for the rapid and precies determination of acclimated phytoplankton reproduction rates. J. Plankton Res., 3: 193-201. https://doi.org/10.1093/plankt/3.2.193
  7. Cermeno, P., J.B. Lee, K. Wyman, O. Schofield and P.G. Falkowski. 2011. Competitive dynamics in two species of marine phytoplankton under non-equilibrium conditions. Mar. Ecol. Prog. Ser., 429: 19-28. https://doi.org/10.3354/meps09088
  8. Coleman, A.W., 1985. Diversity of plastid DNA configuration among classes of eukaryote algae. J. Phycol., 21: 1-16.
  9. 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. Microbiol., 145: 447-459. https://doi.org/10.1099/13500872-145-2-447
  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: Some contemporary studies in marine science, edited by Barnes, H. Allen and Unwin, London, pp. 225-231.
  11. Dugdale, R.C., 1967. Nutrient limitation in the sea: dynamic, identification, and significance. Limnol. Oceanogr., 12: 685-695. https://doi.org/10.4319/lo.1967.12.4.0685
  12. Eppley, R.W., J.N. Rogers and J.J. McCarthy, 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
  13. Fan, C., P.M. Glibert, J. Alexander and M.W. Lomas, 2003. Characterization of urease activity in three marine phytoplankton species, Aureococcus anophagefferens, Prorocentrum minimum, and Thalassiosira weissflogii. Mar. Biol., 142: 949-958. https://doi.org/10.1007/s00227-003-1017-8
  14. Gallagher, J.C., 1982. Physiological variation and electrophoretic banding patterns of genetically different seasonal populations of Skeletonema costatum (Bacillariophyceae). J. phycol., 18: 148-162. https://doi.org/10.1111/j.1529-8817.1982.tb03169.x
  15. Garate-Lizarraga, I., J.J. Bustilos-Guzmain, I. Morquecho and L. Deveze, 2000. First outbreak of Cochlodinium polykrikoides in the Gulf of California. Harmful Algae News, 7 pp.
  16. Gauge, G. E. 1932. Experimental studies on the struggle for existence. 1. Mixed populations of two species of yeast. J. Exp. Biol., 9: 389-402.
  17. Gobler, C.J., A. Burson, F. Koch, Y. Tang and M.R. Mulholland, 2012. The role of nitrogenous nutrients in the occurrence of harmful algal blooms caused by Cochlodinium polykrikoides in New York estuaries (USA). Harmful Algae, 17: 64-74. https://doi.org/10.1016/j.hal.2012.03.001
  18. Guillard, R.R.L. and D. Ryther, 1962. Studies of marine planktonic diatom I: Cyclotella nana Hustedt and Detonula confervacea (Cleve) Gran. Can. J. Microbiol., 8: 229-239. https://doi.org/10.1139/m62-029
  19. Harrison, P.J., J.S. Parslow and H.L. Conway, 1989. Determination of nutrient uptake kinetic parameters: a comparison of methods. Mar. Ecol. Prog. Ser., 52: 301-312. https://doi.org/10.3354/meps052301
  20. Hasle, G.R., 1973. Morphology and taxonomy of Skeletonema costatum (Bacillariophyceae). Nor. J. Bot., 20: 109-137.
  21. Hutchinson, G.E., 1961. The paradox of the plankton. Am. Nat., 95: 137-147. https://doi.org/10.1086/282171
  22. Jauzein, C., S. Loureiro, E. Garces and Y. Collos. 2008. Interactions between ammonium and urea uptake by fice strains of Alexandrium catenella (Dinophyceae) in culture. Aquat. Microb. Ecol., 53: 271-280. https://doi.org/10.3354/ame01249
  23. Jung, S.W, S.M Yun, S.D. Lee, Y.O. Kim and J.H Lee, 2009. Morphological characteristics of four species in the genus Skeletonema in coastal waters of South Korea. Algae, 24: 195-203. https://doi.org/10.4490/ALGAE.2009.24.4.195
  24. Keller, M.D., R.C. Selvin, W. Claus and R.R.L. Guillard, 1987. Media for the culture of oceanic ultraphytoplankton. J. Phycol., 23: 633-638.
  25. Kim, D.I., 2003. Physiological and ecological studies on harmful red tide dinoflagellate Cochlodinium polykrikoides (Margalef). Ph. D. Thesis, Kyushu University, Fukuoka, 154 pp.
  26. Kobori, H. and N. Taga, 1979. Phosphatase activity and its role in the mineralization of organic phosphorus in coastal sea water. J. Exp. Mar. Biol. Ecol., 36: 23-39. https://doi.org/10.1016/0022-0981(79)90098-4
  27. Koizumi, Y., T. Uchida and T. Honjo, 1996. Diurnal vertical migration of Gymnodinium mikimotoi during a red tide in Hoketsu Bay, Japan. J. Plankton Res., 18: 289-294. https://doi.org/10.1093/plankt/18.2.289
  28. Koroleff, F., 1983. Determination of urea. In: Methods of seawater analysis, 2nd. edited by Grasshoff, K., M. Ehrhardt and K. Kremling, Verlag Chemie, Weinheim, pp 158-162.
  29. Kwon, H.K., 2010. Utilization of dissolved organic phosphorus and alkaline phosphatase activity of phytoplankton. M. Sc. Thesis, Pukyung National University, Busan, 86 pp.
  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, 8: 781-791. https://doi.org/10.1016/j.hal.2008.05.006
  31. Lim, W.A, C.S. Jung, C.K. Lee, Y.C. Cho, S.G. Lee, H.G. Kim and I.K. Chung, 2002. The outbreak, maintenance, and decline of the red tide dominated by Cochlodinium polykrikoides in the coastal waters off Southern Korea from August to October, 2000. J. Korean Soc. Oceanogr., 7: 68-77.
  32. Lee, J.H, H.S. Song and E.H. Lee, 1997. Red-tide on phytoplankton diatoms in Incheon Dock of Korea. Kor. J. Environ. Biol., 15: 119-129.
  33. Lomas, M.W. and P.M. Glibert, 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
  34. MacIsaac, J.J, G.S. Grunseich, H.E. Glover, C.M. and Yentsch, 1979. Light and nutrient limitation in Gonyaulax excavata: nitrogen and carbon trace results. In: Toxic Dinoflagellate Blooms, edited by Taylor, D.L. and H.H. Seliger, Elsevier, NewYork, pp. 107-110.
  35. McCarthy, J.J. 1972. The uptake of urea by marine phytoplankton. J. Phycol., 8: 216-222.
  36. McCarthy, J.J., 1980. Nitrogen. In: The Physiological Ecology of Phytoplankton, edited by Morris, I., Blackwell Scientific Publications, Oxford, pp. 191-233.
  37. Milligan, A.S. and P.J. Harrison, 2000. Effects of non-steady state iron limitation on nitrogen assimilatory enzymes in the marine diatom Thalassiosira weissflogii (Bacillariophycea). J. Plankton Res., 36: 78-86.
  38. Mitamura, O. and Y. Saijo, 1980. In situ measurement of the urea decomposition rate and its turnover rate in the Pacific Ocean. Mar. Biol., 58: 147-152. https://doi.org/10.1007/BF00396126
  39. Mobley, H.L.T. and R.P. Hausinger, 1989. Microbial ureases: significance, regulation, and molecular characterization. Microbiol. Rev., 53: 85-108.
  40. Nakamura, Y. and M.M. Watanabe, 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. Narasoe, S., T. Shikata, Y. Yamasaki, T. Matsubara, Y. Shimasaki, Y. Ohima and T. Honjo, 2010. Effects on growth of the red-tide dinoflagellate Gymnodinium instriatum Freudenthal et Lee and a possible link to blooms of this species. Hydorbiol., 56: 225-238.
  42. Nishijima, T., Y. Hata and S. Yamauchi, 1989. Physiological ecology of Prorocentrum triestinum. Bull. Jpn. Soc. Sci. Fish., 55: 2009-2014. https://doi.org/10.2331/suisan.55.2009
  43. Nishikawa, T. and Y. Hori, 2004. Effects of nitrogen, phosphorus and silicon on a growth of a diatom Eucampia zodiacus caused bleaching of seaweed Porphyra isolated from Harima-Nada, Seto Inland Sea, Japan. Nippon Suisan Gakkaishi, 70: 31-38. https://doi.org/10.2331/suisan.70.31
  44. Noh, I.H., 2009. Physiological and ecological studies on the harmful algae Chattonella spp. (Rhaphidophyceae) in the coastal waters of Korea. Ph. D. Thesis, Chonnam National University, Yeosu, 269 pp.
  45. Oh, S.J., T. Yamamoto, Y. Kataoka, O. Matsuda, Y. Matsuyama and Y. Kotani, 2002. Utilization of dissolved organic phosphorus by the two toxic dinoflagellates, Alexandrium tamarense and Gymnodinium catenatum (Dinophyceae). Fish. Sci., 68: 416-424. https://doi.org/10.1046/j.1444-2906.2002.00440.x
  46. 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). Bull. Coast Oceanogr., 43: 85-95.
  47. Oh S.J, H.S. Yang and T. Yamamoto, 2007. Use of a mathematical model to assess the effects of dissolved organic phosphorus on species competition among the dinoflagellates Alexandrium tamarense and Gymnodinium catenatum and the diatom Skeletonema costatum. J. Kor. Fish. Soc., 40: 39-49. https://doi.org/10.5657/kfas.2007.40.1.039
  48. Park, J.A., 2013. DON utilization of toxic dinoflagellate Alexandrium tamarense and Alexandrium catenella isolated form Masan Bay. M. Sc. Thesis, Pukyung National University, Busan, 92 pp.
  49. Park, J.S., Y.H. Yoon and S.J. Oh, 2009. Variational Characteristics of Phytoplankton Community in the Mouth Parts of Gamak Bay, Southern Korea. Kor. J. Environ. Biol., 27: 205-215.
  50. Park, T.G., W.A. Lim, Y.T. Park, C.K. Lee and H.J. Jeong, 2013a. Economic impact, management and mitigation of red tides in Korea. Harmful Algae, 30S: S131-S143.
  51. Park, K.W., J.W. Park, S.H. Yoon and Y.S. Seo, 2013b. Occurrence of Cochlodinium polykrikoides bloom, 2013. 2013 Autumn Meeting on the Korea Society of Oceanography, p. 95.
  52. Porter, K.G. and Y.S. Feig, 1980. The use of DAPI for identifying and counting aquatic microflora. Limnol. Oceanogr., 25: 943-948. https://doi.org/10.4319/lo.1980.25.5.0943
  53. Poulet, S.A. and V. Martin-Jezequel, 1983. Relationships between dissolved free amino acids, chemical composition and growth of the marine diatom Chaetoceros debile. Mar. Biol., 77: 93-100. https://doi.org/10.1007/BF00393214
  54. Provasoil, L., K. Shiraishi and J.R. Lance, 1959. Nutritional idiosyncrasies of Artemia and Tigriopus in monoxenic culture. Ann. N. Y. Sci., 77: 250-261.
  55. Richersons, P, R. Armstrong and C.R. Goldman, 1970. Contemporaneous disequilibrium, a new hypothesis to explain the 'paradox of the plankton'. Pro. Nat. Acad. Sci., 67: 1710-1714. https://doi.org/10.1073/pnas.67.4.1710
  56. Sommer, U., 1989. The role of competition for resources in phytoplankton succession. In: Plankton Ecology: Succession in Plankton Communities, edited by Sommer, U., Springer-Verlag, New York, pp. 57-106.
  57. 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: Physiological Ecology of Harmful Algal Blooms, edited by Anderson, D.M., A.D. Cembella and G.M. Hallegraeff, Springer, NewYork, pp. 135-153.
  58. Strickland, J.D.H. and L. Solorzano, 1966. Determination of monoesterase hydrolysable phosphate and phosphomonoesterase activity in sea water. In: Some contemporary studies in marine science, edited by Barnes, H., Allen and Unwin Ltd, London, pp. 665-674.
  59. Strickland, J.D.H. and T.R. Parson, 1972. A practical handbook of seawater analysis. Fisheries Research Board of Canada, Ottawa, 310 pp.
  60. Tameishi, M., Y. Yamasaki, S. Nagasoe, Y. Shimasaki, Y. Oshima and T. Honjo, 2009. Allelopathic effects of the Dinophyte Prorocentrum minimum on the growth of the Bacillariophyte Skeletonema costatum. Harmful Algae, 8: 421-429. https://doi.org/10.1016/j.hal.2008.09.002
  61. Tang, Y.Z. and C.J. Gobler, 2010. Allelopathic effects of Cochlodinium polykrikoides isolates and blooms from the estuaries of Long Island, New York, on co-occurring phytoplankton, Mar. Ecol. Prog. Ser., 406: 19-13. https://doi.org/10.3354/meps08537
  62. Whyte, J.N.C., N. Haigh, N.G. Ginther and L.J. Keddy, 2001. First record of blooms of Cochlodinium sp.(Gymnodiniales, Dinophyceae) causing mortality to aquacultured salmon on the west coast of Canada. Phycol., 40: 298-304. https://doi.org/10.2216/i0031-8884-40-3-298.1
  63. Wiliams, P.J.B., 1975. Biological and chemical aspects of dissolved organic material in sea water, In: Chemical Oceanography, edited by Riley, J.P. and G. Skirrow, Academic Press Inc., London, pp. 301-363.
  64. Yamamoto, Y., 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. Fish. Sci., 70: 108-115. https://doi.org/10.1111/j.1444-2906.2003.00778.x
  65. Yamaguchi, H., T. Nishijima, H. Nishitani, K. Fukami and M. Adachi., 2004a. Organic phosphorus utilization and alkaline phosphatase production of 3 red tide phytoplankton. Nippon Suisan Gakkaishi, 70: 123-130. https://doi.org/10.2331/suisan.70.123
  66. Yamaguchi, H., T. Nishijima, A. Oda, K. Fukami and M. Adachi, 2004b. Distribution and variation of alkaline phosphatase activity and phosphatase hydrolyzable phosphorus in coastal seawater. Nippon Suisan Gakkaishi, 70: 333-342. https://doi.org/10.2331/suisan.70.333
  67. 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 phytoplankton, Hepterocapsa circularisquama, Fibrocapsa japonica and Chaetoceros ceratosporum. Plankton Biol. Ecol., 52: 65-75.
  68. 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, 7: 26-32. https://doi.org/10.1016/j.hal.2007.05.011
  69. Yuki, K. and S. Yoshimatsu, 1989. Two fish-killing species of Cochlodinium form Harima-Nada, Seto Inland Sea, Japan. In: Red Tides: Biology, Environmental Science, and Toxicology, edited by Okaichi, T., D.M. Anderson and T. Nemoto, Elsevier, NewYork, pp. 451-452.