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 Temperature and Salinity on the Growth and Paralytic Shellfish Toxin (PST) Production by Toxic Dinoflagellate Alexandrium pacificum

유독 와편모조류 Alexandrium pacificum의 생장과 마비성 패독 생산에 미치는 수온과 염분의 영향

  • Li, PeiJin (Major of Oceanography, Division of Earth and Environmental System Sciences, Pukyong National University) ;
  • Oh, Seok Jin (Major of Oceanography, Division of Earth and Environmental System Sciences, Pukyong National University) ;
  • Kim, Seok-Yun (Major of Oceanography, Division of Earth and Environmental System Sciences, Pukyong National University)
  • ;
  • 오석진 (부경대학교 지구환경시스템과학부 해양학전공) ;
  • 김석윤 (부경대학교 지구환경시스템과학부 해양학전공)
  • Received : 2022.08.31
  • Accepted : 2022.10.28
  • Published : 2022.10.31
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Abstract

Growth rate and production of the paralytic shellfish poisoning toxin (PST) of a toxic dinoflagellate Alexandrium pacificum (LIMS-PS-2611) isolated from the southern sea of Korea, were examined under various temperatures and salinity conditions. The maximum growth rate (0.28 day-1) was observed under 25℃ and 30 psu. Optimal growth (≥ 70% of maximum growth rate) was obtained between 20~25℃ and 25~35 psu. Among the PSTs of A. pacificum, the principal toxins were C1+2 and GTX5 in N-sulfocarbamoyl toxin group, and minor components were characterized as neoSTXs in the carbamate toxin group. Maximum toxin content was observed under 20℃ and 30 psu, and the toxin content increased with the increase of salinity. Low toxin contents were measured under the temperature and salinity conditions of the maximum growth rate. Therefore, the PSP of bivalve, which occurs at a temperature range of 20-25℃ in June, might have been derived from A. pacificum.

배양실험을 바탕으로 다양한 수온과 염분 조건에서 유독 와편모조류 Alexandrium pacificum (LIMS-PS-2611)의 생장속도와 마비성 패독(PST)의 변화를 조사하였다. A. pacificum는 수온 25℃, 염분 30 psu 조건에서 최대생장속도를 보였으며, 최대생장속도의 70% 이상은 수온 20~25℃, 염분 25~35 psu 구간에서 나타났다. A. pacificum 체내의 PST 주요성분은 N-sulfocarbamoyl계의 C1+2와 GTX5이었으며, 미량성분은 carbamate계의 neoSTX이었다. 수온과 염분에 따른 독함량의 변화를 보면, A. pacificum는 수온 20℃, 염분 30 psu의 조건에서는 비교적 낮은 독 함량을 보였다. 염분의 증가에 따라 독 함량이 증가하는 경향을 나타냈다. 그러나 최대생장속도를 보였던 수온과 염분 조건에서는 낮은 독 함량을 보였다. 따라서 6월 수온이 20-25℃ 범위일 때 발생하는 이매패류 독화현상은 A. pacificum에 의한 영향일 가능성이 있다.

Keywords

Acknowledgement

이 논문은 부경대학교 자율창의학술연구비(2021년)에 의하여 연구되었다.

References

  1. Anderson, D. M., D. M. Kulis, J. J. Sullivan, S. Hall, and C. Lee(1990), Dynamics and physiology of saxitoxin production by the dinoflagellates Alexandrium spp, Marine Biology, Vol. 104, pp. 511-524. https://doi.org/10.1007/BF01314358
  2. Anderson, D. M.(1990), Toxin variability in Alexandrium species. In: Graneli, E., B. Sundstrom, L. Edler, and D. M. Anderson (Eds.), Toxic Marine Phytoplankton, Elsevier, Amsterdam, pp. 41-51.
  3. Anderson, D. M., T. J. Alpermann, A. D. Cembella, Y. Collos, E. Masseret, and M. Montreson(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
  4. Boczar, B. A., M. K. Beitler, J. Liston, J. Sullivan, and R. A. Cattolico(1988), Paralytic shellfish toxins in Protogonyaulax tamarensis and Protogonyaulax catenella in axenic culture, Plant Physiology, Vol. 88, No. 4, pp. 1285-1290. https://doi.org/10.1104/pp.88.4.1285
  5. Boyer, G. L., J. J. Sullivan, R. J, Andersen, P. J. Harrison, and F. J. R. Taylor(1987), Effects of nutrient limitation on toxin production and composition in the marine dinoflagellate Protogonyaulax tamarensis, Marine Biology, Vol. 96, pp. 123-128. https://doi.org/10.1007/BF00394845
  6. Caruana, A. M. N., M. Le Gac, F. Herve, G.-A. Rovillon, S. Geffroy, F. Malo, E. Abadie, and Z. Amzil(2020), Alexandrium pacificum and Alexandrium minutum: harmful or environmentally friendly?, Marine Environmental Research, Vol. 160, pp. 105014. https://doi.org/10.1016/j.marenvres.2020.105014
  7. Cembella, A. D., J. J. Sullivan, G. L. Boyer, F. J. R. Taylor, and R. J. Anderson(1987), Variation in paralytic shellfish toxin composition within the Protogonyaulax tamarensis/catenella species complex: red tide dinoflagellates, Biochemical Systematics and Ecology, Vol. 15, No. 2, pp. 171-186. https://doi.org/10.1016/0305-1978(87)90018-4
  8. Franks, P. J. S. and D. M. Anderson(1992), Alongshore transport of a toxic phytoplankton bloom in a buoyancy current: Alexandrium tamarense in the Gulf of Maine, Marine Biology, Vol. 112, pp. 153-164. https://doi.org/10.1007/BF00349739
  9. Fulco, V. K. and A. M. Gayoso(2004), Effects of light, temperature and salinity on the growth rate of Alexandrium tamarense from Patagonia (Argentina). In Steidinger, K. A., J. H. Landsberg, C. R. Tomas and G. A. Vargo (Eds), Harmful Algae 2002, Florida Fish and Wildlife Conservation Commission, Florida Institute of Oceanography, and Intergovernmental Oceanographic Commission of UNESCO, Florida, pp. 391-392.
  10. Goldman, J. C. and E. J. Carpenter(1974), A kinetic approach to the effect of temperature on algal growth, Limnology and Oceanography, Vol. 19, No. 5, pp. 756-766. https://doi.org/10.4319/lo.1974.19.5.0756
  11. Guillard, R. R L. and J. H. Ryther(1962), Studies of marine planktonic diatoms. I. Cyclotellanana Hustedt and Detonula confervacea (Cleve) Gran, Canadian Journal of Microbiology, Vol. 8, No. 2, pp. 229-239. https://doi.org/10.1139/m62-029
  12. Hadjadji, I., M. Laabir, H. Frihi, Y. Collos, Z. J. Shao, P. Berrebi, E. Abadie, Z. Amzil, N. Chomerat, J. L. Rolland, F. Rieuvilleneuve, and E. Masseret(2020), Unsuspected intraspecific variability in the toxin production, growth and morphology of the dinoflagellate Alexandrium pacificum R. W. Litaker (Group IV) blooming in a South Western Mediterranean marine ecosystem, Annaba Bay (Algeria), Toxicon, Vol. 180, pp. 79-88. https://doi.org/10.1016/j.toxicon.2020.04.005
  13. Hallegraeff, G. M.(1993), A review of harmful algal blooms and their apparent global increase. Phycologia, Vol. 32(2), pp. 79-99. https://doi.org/10.2216/i0031-8884-32-2-79.1
  14. Hallegraeff, G. M.(2010), Ocean climate change, phytoplankton community responses, and harmful algal blooms: A formidable predictive challenge, Journal of Phcology, Vol. 46, pp. 220-235. https://doi.org/10.1111/j.1529-8817.2010.00815.x
  15. Hamasaki, K., M. Horie, S. Tokimistu, T. Toda, and S. Taguchi(2001), Variability in toxicity of the dinoflagellate Alexandrium tamarense isolated from Hiroshima Bay, western Japan, as a reflection of changing environmental conditions, Journal of Plankton Research, Vol. 23, No. 3, pp. 271-278. https://doi.org/10.1093/plankt/23.3.271
  16. Hwang, D. F. and Y. H. Lu(2000), Influence of environmental and nutritional factors on growth, toxicity, and toxin profile of dinoflagellate Alexandrium minutum, Toxicon, Vol. 38, No. 11, pp. 1491-1503. https://doi.org/10.1016/S0041-0101(00)00080-5
  17. Ishida, Y., C. -H. Kim, Y. Sako, N. Hirooka, and A. Uchida(1993), PSP toxin production is chromosome dependent in Alexandrium spp. In: Smayda, T. J. and Y. Shimizu (Eds.), Toxic Phytoplankton Blooms in the Sea, Elsevier, Netherlands, pp. 881-887.
  18. Kim, K. Y., M. Yoshida, Y. Fukuyo, and C. H. Kim(2002), Morphological Observation of Alexandrium tanarense (Lebour) Balech, A. catenella (Whedon et Kofoid) Balech and one related morphotype (Dinophyceae) in Korea, Algae, Vol. 17, No. 1, pp. 11-19. https://doi.org/10.4490/ALGAE.2002.17.1.011
  19. Kremp, A., A. Godhe, J. Egardt, S. Dupont, S. Suikkanen, S. Casabianca, and A. Penna(2012), Intraspecific variability in the response of bloom-forming marine microalgae to changed climate conditions, Ecology and Evolution, Vol. 2, No. 6, pp. 1195-1207. https://doi.org/10.1002/ece3.245
  20. Laabir, M., Y. Collos, E. Masseret, V. Savart, M. Sibat, and Z. Amzil(2013), Influence of environmental factors on the paralytic shellfish toxin content and profile of Alexandrium catenella (Dinophyceae) isolated from the Mediterranean Sea, Marine Drugs, Vol. 11, No. 5, pp. 1583-1601. https://doi.org/10.3390/md11051583
  21. Larocque, R. and A. D. Cembella(1990), Ecological parameters associated with the seasonal occurrence of Alexandrium spp. and consequent shellfish toxicity in the lower St. Lawrence estuary (Eastern Canada). In Graneli, E., B. Sundstrom, L. Edler, and D. M. Anderson (Eds.), Toxic Marine Phytoplankton, Elsevier, Amsterdam, pp. 368-373.
  22. Lim, P. -T. and T. Ogata(2005), Salinity effect on growth and toxin production of four tropical Alexandrium species (Dinophyceae), Vol. 45, No. 6, pp. 699-710.
  23. Maclntyre, J. G., J. J. Cullen, and A. D. Cembella(1997), Vertical migration, nutrition and toxicity in the dinoflagellate Alexandrium tamarense, Marine Ecology and Progress Series, Vol. 148, pp. 201-216. https://doi.org/10.3354/meps148201
  24. Maranda, L., D. M. Anderson, and Y. Shimizu(1985), Comparison of toxicity between populations of Gonyaulax tamarensis of eastern North American waters, Estuarine, Coastal and Shelf Science, Vol. 21, No. 3, pp. 401-410. https://doi.org/10.1016/0272-7714(85)90020-4
  25. Matsuda, A., T. Nishijima, K. Fukami, and M. Adachi(2006), Growth kinetics and paralytic shellfish poisoning toxin production in phosphorus limited cultures of Alexandrium catenella, Nippon Suisan Gakkaishi, Vol. 72, No. 2, pp. 193-200. https://doi.org/10.2331/suisan.72.193
  26. Mok, J. -S., K. -C. Song, K. -J. Lee, and J. -H. Kim(2013), Variation and profile of paralytic shellfish poisoning toxins in Jinhae Bay, Korea, Fisheries and Aquatic Sciences, Vol. 16, No. 3, pp. 137-142. https://doi.org/10.5657/FAS.2013.0137
  27. NIFS(2022), https://www.nifs.go.kr/bbs?id=shellfish
  28. Ogata, T., T. Ishimaru, and M. Kodama(1987), Effect of water temperature and light intensity on growth rate and toxicity change in Protogonyaulax tamarensis, Marine Biology, Vol. 95, pp. 217-220. https://doi.org/10.1007/BF00409008
  29. Oh S. J., J. -A. Park, H. -K. Kwon, H. S. Yang, and W. -A. Lim(2012), Ecophysiological studies on the population dynamics of two toxic dinoflagellates Alexandrium tamarense and Alexandrium catenella isolated from the southern coast of Korea I. Effects of temperature and salinity on the growth, Journal of the Korean Society for Marine Environmental Engineering, Vol. 15, No. 2, pp. 133-141. https://doi.org/10.7846/JKOSMEE.2012.15.2.133
  30. Oikawa H., T. Fujita, K. Satio, S. Watabe, M. Satomi, and Y. Yano(2004), Comparison of paralytic shellfish poisoning toxin between carnivorous crabs (Telmessus acutidens and Charybdis japonica) and their prey mussel (Mytilus galloprovincialis) in an inshore food chain, Toxicon, Vol. 43, No. 6, pp. 713-719. https://doi.org/10.1016/j.toxicon.2004.03.003
  31. Oshima, Y.(1995), Post-column derivatization HPLC methods of paralytic shellfish poisons, In; Manual on harmful marine microalgae, Hallegraeff, G. M., D. M. Anderson and A. D. Cembella(eds), UNESCO, Paris, pp. 81-94.
  32. Oshima, Y., S. I. Blackburn, and G. M. Hallegraeff(1993), Comparative study on paralytic shellfish toxin profiles of the dinoflagellate Gymnodinium catenatum from three different countries, Marine Biology, Vol. 116, pp. 471-476. https://doi.org/10.1007/BF00350064
  33. Parkhill, J. P. and A. D. Cembella(1999), Effects of salinity, light and inorganic nitrogen on growth and toxigenicity of the marine dinoflagellate Alexandrium tamarense from northeastern Canada, Journal of Plankton Research, Vol. 21 No. 5, pp. 939-955. https://doi.org/10.1093/plankt/21.5.939
  34. Sekiguchi, K., S. Sato, S. Kaga, T. Ogata, and M. Kodama (2001), Accumulation of paralytic shellfish poisoning toxins in bivalves and an ascidian fed on Alexandrium tamarense cells, Fisheries Sciense, Vol. 67, No. 2, pp. 301-305. https://doi.org/10.1046/j.1444-2906.2001.00228.x
  35. Shin, H. H., Z. Li, E. S. Kim, J-W. Park, and W. A. Lim(2017), Which species, Alexandrium catenella (Group I) or A. pacificum (Group IV), is really responsible for past paralytic shellfish poisoning outbreaks in Jinhae-Masan Bay, Korea?, Harmful Algae, Vol. 68, pp. 31-39. https://doi.org/10.1016/j.hal.2017.07.006
  36. Shon, M. B., Y. S. Kim, and C. H. Kim(2009), Paralytic shellfish poisoning of Mediterranean mussels from Jinhae Bay in Korea, Korean Journal Fisheries and Aquatic Sciences, Vol. 42, No. 4, pp. 366-372. https://doi.org/10.5657/kfas.2009.42.4.366
  37. Siu, G. K. Y., M. L. C. Young, and D. K. O. Chan(1997), Environmental and nutritional factors which regulate population dynamics and toxin production in the dinoflagellate Alexandrium catenella, Hydrobiologia, Vol. 352, pp. 117-140. https://doi.org/10.1023/A:1003042431985
  38. Sunda, W. G., E. Graneli, and C. J. Gobler(2006), Positive feedback and the development and persistence of ecosystem disruptive algal blooms, Journal of Phycology, Vol. 42, No. 5, pp. 963-974. https://doi.org/10.1111/j.1529-8817.2006.00261.x
  39. Tanabe, S. H. and Y. Sako(2006), Genetic differentiation in the marine dinoflagellates Alexandrium tamarense and Alexandrium catenella based on DNA-DNA hybridization, Plankton and Benthos Research, Vol. 1 (3), pp. 138-146. https://doi.org/10.3800/pbr.1.138
  40. Taroncher-Oldenburg, G., D. M. Kulis, and D. M. Anderson (1997), Toxin variability during the cell cycle of the dinoflagellate Alexandrium fundyense, Limnology and Oceanography, Vol. 42, No. 5, pp. 1178-1188. https://doi.org/10.4319/lo.1997.42.5_part_2.1178
  41. Taroncher-Oldenburg, G., D. M. Kulis, and D. M. Anderson (1999), Coupling of saxitoxin biosynthesis to the G1 phase of the cell cyclc in the dinoflagellate Alexandrium fundyense: temperature and nutrients effects, Nat Toxins, Vol. 7 (5), pp. 207-219. https://doi.org/10.1002/1522-7189(200009/10)7:5<207::AID-NT61>3.0.CO;2-Q
  42. Taylor, F. J. R., Y. Fukuyo, and J. Larsen(1995), Taxonomy of harmful dinoflagellates. In: Hallegreaff, M., D. M., Anderson, A. D. Cembella and H. O. Enevoldsen (Eds), Manual on Harmful Marine Microalgae, UNESCO, Paris, pp. 283-317.
  43. Wang, D. Z. and D. P. H. Hsieh(2005), Growth and toxin production in batch cultures of a marine dinoflagellate Alexandrium tamarense HK9301 isolated from the South China Sea, Harmful Algae, Vol. 4, No. 2, pp. 401-410. https://doi.org/10.1016/j.hal.2004.07.002
  44. Xu, J., A. Y. T. Ho, L. He, K. Yin, C. Hung, N. Choi, P. K. S. Lam, R. S. S. Wud, 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
  45. Yoshida, T., Y. Sako, and A. Uchida(2001), Geographic differences in paralytic shellfish poisoning toxin profiles among Japanese populations of Alexandrium tamarense and A. catenella (Dinophyceae), Phycological Research, Vol. 49, No. 1, pp. 13-21. https://doi.org/10.1111/j.1440-1835.2001.tb00228.x