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Home / Regular Issue / JTAS Vol. 46 (1) Feb. 2023 / JTAS-2538-2022


Paralytic Shellfish Profiles Produced by the Toxic Dinoflagellate Pyrodinium bahamense from Sepanggar Bay, Malaysia

Asilah Al-Has, Normawaty Mohammad-Noor, Sitti Raehanah M. Shaleh, Mohd Nor Azman Ayub, Deny Susanti and Ghaffur Rahim Mustakim

Pertanika Journal of Tropical Agricultural Science, Volume 46, Issue 1, February 2023


Keywords: Gonyautoxin, HPLC, PSP, Pyrodinium bahamense, saxitoxin

Published on: 22 Febuary 2023

Pyrodinium bahamense var compressum is a harmful dinoflagellate that produces saxitoxin, which causes paralytic shellfish poisoning (PSP) that is deadly to humans. A non-axenic culture of P. bahamense was established using f/2 media from samples collected from Sepanggar Bay, Kota Kinabalu, Sabah. Toxin analyses of cultures harvested on days 60, 120, 180, and 360 were performed using high-performance liquid chromatography with a fluorescence detector and compared with samples collected at the same location during the bloom in 2021. The highest cell toxin content was found in the bloom sample (86.2 fmole/cell), and no toxin was detected in the culture 60 days old. In addition, cell toxin content for the P. bahamense culture was low (9.4-16.5 fmole/cell). Based on the toxin profile, P. bahamense comprises 84- 98% of gonyautoxin 4. In summary, the current findings add to the existing knowledge of the toxin profiling of P. bahamense, a toxic, harmful algal bloom species, thus, leading to better toxin management.

  • Adam, A., Mohammad-Noor, N., Anton, A., Saleh, E., Saad, S., & Shaleh, S. R. M. (2011). Temporal and spatial distribution of harmful algal bloom (HAB) species in coastal waters of Kota Kinabalu, Sabah, Malaysia. Harmful Algae, 10(5), 495–502.

  • Anderson, D. M., Kulis, D. M., Sullivan, J. J., Hall, S., & Lee, C. (1990). Dynamics and physiology of saxitoxin production by the dinoflagellates Alexandrium spp. Marine Biology, 104, 511-524.

  • AOAC International. (2011). Paralytic shellfish toxins in mussels, clams, scallops and oysters by liquid chromatography post-column oxidation. AOAC International.

  • Band-schmidt, C. J., Bustillos-Guzman, J., Morquecho, L., Grate-Lizarraga, I., Alonso-Rodríguez, R., Reyes-Salinas, A., Erler, K., & Luckas, B. (2006). Variations of PSP toxin profiles during different growth phases in Gymnodinium catenatum (Dinophyceae) strains isolated from three location in the Gulf of California, Mexico. Journal of Phycology, 42(4), 757–768.

  • Banguera-Hinestroza, E., Eikrem, W., Mansour, H., Solberg, I., Cúrdia, J., Holtermann, K., Edvardsen, B., & Kaartvedt, S. (2016). Seasonality and toxin production of Pyrodinium bahamense in a Red Sea lagoon. Harmful Algae, 55, 163–171.

  • Farabegoli, F., Blanco, L., Rodríguez, L. P., Juan, M. V., & Ana, G. C. (2018). Phycotoxins in marine shellfish: Origin, occurrence and effects on humans. Marine Drugs, 16(6), 188.

  • Gedaria, A. I., Luckas, B., Reinhardt, K., & Azanza, R. V. (2007). Growth response and toxin concentration of cultured Pyrodinium bahamense var. compressum to varying salinity and temperature conditions. Toxicon, 50(4), 518–529.

  • Guillard, R. R., & Ryther, J. H. (1962). Studies of marine planktonic diatoms: I. Cyclotella nana Hustedt, and Detonula confervacea (cleve) Gran. Canadian Journal of Microbiology, 8(2), 229-239.

  • Hayashi, R., Saito, H., Okumura, M., & Kondo, F. (2006). Cell bioassay for paralytic shellfish poisoning (PSP): Comparison with postcolumn derivatization liquid chromatographic analysis and application to the monitoring of PSP in shellfish. Journal of Agricultural and Food Chemistry, 54(2), 269–273.

  • Hummert, C., Ritscher, M., Reinharde, K., & Luckas, B. (1997). Analysis of the characteristic PSP profiles of Pyrodinium bahamense and several strains of Alexandrium by HPLC based on ion-pair chromatographic separation, post-column oxidation, and fluorescence detection. Chromatographia, 45, 312–316.

  • Jipanin, S. J., Shaleh, S. M., Lim, P. T., Leaw, C. P., & Mustapha, S. (2019). The monitoring of harmful algae blooms in Sabah, Malaysia. In IOP conference series: Journal of Physics (Vol. 1358, No. 1, p. 012014). IOP Publishing.

  • Landsberg, J. H., Hall, S., Johannessen, J. N., White, K. D., Conrad, S. M., Abbott, J. P., Flewelling, L. J., Richardson, R. W., Dickey, R. W., Jester, E. L. E., Etheridge, S. M., Deeds, J. R., Dolah, F. M. V., Leighfield, T. A., Zou, Y., Beaudry, C. G., Benner, R. A., Rogers, P. L., Scott, P. S., … Steidinger, K. A. (2006). Saxitoxin puffer fish poisoning in the United States, with the first report of Pyrodinium bahamense as the putative toxin source. Environmental Health Perspectives, 114(10), 1502–1507.

  • Lopez, C. B., Tilney, C. L., Muhlbach, E., Bouchard, J. N., Villac, M. C., Henschen, K. L., Markley, L. R., Abbe, S. K., Shankar, S., Shea, C. P., Flewelling, L., Garrett, M., Badylak, S., Phlips, E. J., Hall, L. M., Lasi, M. A., Parks, A. A., Paperno, R., Adams, D. H., … Hubbard, K. A. (2021). High-resolution spatiotemporal dynamics of harmful algae in the Indian River Lagoon (Florida) — A case study of Aureoumbra lagunensis, Pyrodinium bahamense, and Pseudo-nitzschia. Frontiers in Marine Science, 8, 769877.

  • Lorons, D., Jafar-Sidik, M., Ali, N., Mohamad-Azaini, F., Rodrigues, K. F., & Chin, G. J. W. L. (2022). The variation of environmental profiles during harmful algal bloom in Sepanggar Bay, Sabah, Malaysia. Journal of Oceanography, 78(2), 121–132.

  • Mohammad-Noor, N., Weliyadi, E., Aung, T., Adam, A., & Hanan, D. S. M. (2014). Effects of meteorological conditions on the occurrence of Cochlodinium polykrikoides and Pyrodinium bahamense var. compressum in coastal waters of Kota Kinabalu, Sabah, Malaysia. Sains Malaysiana, 43(1), 21–29.

  • Mohammad-Noor, N., Adam, A., Lim, P. T., Leaw, C. P., Lau, W. L., Liow, G. R., Muhamad-Bunnori, N., Hamdan, N. A., Md-Nor, A., Kemat, N., & Muniandi, D. (2018). First report of paralytic shellfish poisoning (PSP) caused by Alexandrium tamiyavanichii in Kuantan Port, Pahang, East Coast of Malaysia. Phycological Research, 66(1), 37-44.

  • Montojo, U. M., Sakamoto, S., Cayme, M. F., Gatdula, N. C., Furio, E. F., Relox, J. R., Sato, S., Fukuyo, Y., & Kodama, M. (2006). Remarkable difference in accumulation of paralytic shellfish poisoning toxins among bivalve species exposed to Pyrodinium bahamense var. compressum bloom in Masinloc Bay, Philippines. Toxicon, 48(1), 85–92.

  • Morquecho, L. (2019). Pyrodinium bahamense one the most significant harmful dinoflagellate in Mexico. Frontiers in Marine Science, 6, 1.

  • Muhammad Shaleh, S. R., Doinsing, J., Peter, C. Anton, A., & Saleh, E. (2010). Effects on salinity on interspecific growth interactions between 2 harmful algal species Pyrodinium var. compressum and Cochlodinium polykrikoides in laboratory cultures. In Proceedings of the 13th International Conference on Harmful Algae (95-97). Environmental Publication Department.

  • Mustakim, G. R., Anton, A., Samsur, M., & Ayub, M. N. A. (2016). Determination of PSP concentration in shellfish from Kuala Penyu, Sabah using HPLC method. Transactions on Science and Technology, 3(2–2), 433–438.

  • Mustakim, G. R., Muhammad Shaleh, S. R., & Ayub, M. N. A. (2019). Effect of different concentration of soil extracts on the growth of Pyrodinium bahamense var. compressum. International Journal of Fisheries and Aquatic Studies, 7(5), 353–355.

  • Nishitani, L., & Chew, K. K. (1984). Recent developments in paralytic shellfish poisoning research. Aquaculture, 39(1-4), 317–329.

  • Oshima, Y. (1995). Postcolumn derivation liquid chromatographic method for paralytic shellfish toxins. Journal of AOAC International, 78(2), 528-532.

  • Oyaneder-Terrazas, J., Contreras, H. R., & García, C. (2017). Prevalence, variability and bioconcentration of saxitoxin-group in different marine species present in the food chain. Toxins, 9(6), 190.

  • Oyaneder-Terrazas, J., Figueroa, D., Araneda, O. F., & García, C. (2022). Saxitoxin group toxins accumulation induces antioxidant responses in tissues of Mytilus chilensis, Ameghinomya antiqua, and Concholepas concholepas during a bloom of Alexandrium pacificum. Antioxidants, 11(2), 392.

  • Phlips, E. J., Badylak, S., Bledsoe, E., & Cichra, M. (2006). Factors affecting the distribution of Pyrodinium bahamense var. bahamense in coastal waters of Florida. Marine Ecology Progress Series, 322, 99–115.

  • Rodrigues, E. T., Nascimento, S. F., Pires, C. L., Godinho, L. P., Churro, C., Moreno, M. J., & Pardal, M. A. (2021). Determination of intestinal absorption of the paralytic shellfish toxin GTX-5 using the Caco-2 human cell model. Environmental Science Pollution Research, 28, 67256-67266.

  • Schantz, E. J., Mold, J. D., Warren Stanger, D., John, S., Riel, F. J., Bowden, J. P., Lynch, J. M., Wayler, R. S., Riegel, B., & Sommer, H. (1957). Paralytic shellfish poison. VI. A procedure for the isolation and purification of the poison from toxic clam and mussel tissues. Journal of the American Chemical Society, 79(19), 5230–5235.

  • Suleiman, M., Jelip, J., Rundi, C., & Chua, T. H. (2017). Case report: Paralytic shellfish poisoning in Sabah, Malaysia. The American Journal of Tropical Medicine and Hygiene, 97(6), 1731–1736.

  • Tang, Y., Zhang, H., Wang, Y., Fan, C., & Shen, X. (2021). Combined effects of temperature and toxic algal abundance on paralytic shellfish toxic accumulation, tissue distribution and elimination dynamics in mussels Mytilus coruscus. Toxins, 13(6), 425.

  • Usup, G., Ahmad, A., Matsuoka, K., Teen, P., & Pin, C. (2012). Biology, ecology and bloom dynamics of the toxic marine dinoflagellate Pyrodinium bahamense. Harmful Algae, 14, 301–312.

  • Usup, G., Cheah, M. Y., Ng, B. K., Leaw, C. P., & Ahmad, A. (2006). Toxin profile and relative toxicity of three paralytic shellfish poisoning toxin-producing dinoflagellates from Malaysia. Malaysian Applied Biology, 35, 41–45.

  • Usup, G., Kulis, D. M., & Anderson, D. M. (1994). Growth and toxin production of the toxic dinoflagellate Pyrodinium bahamense var. compressum in laboratory cultures. Natural Toxins, 2(5), 254–262.

  • Vilariño, N., Louzao, M. C., Abal, P., Cagide, E., Carrera, C., Vieytes, M. R., & Botana, L. M. (2018). Human poisoning from marine toxins: Unknowns for optimal consumer protection. Toxins, 10(8), 324.

  • Wiese, M., D’Agostino, P. M., Mihali, T. K., Moffitt, M. C., & Neilan, B. A. (2010). Neurotoxic alkaloids: Saxitoxin and its analogs. Marine Drugs, 8(7), 2185–2211.

  • Yahumin, S., Rodrigues, K. F., & Chin, G. J. W. L. (2022). Characterization of the saxitoxin biosynthetic starting gene, sxt4, in the toxic dinoflagellate, Pyrodinium bahamense var. compressum. Journal of Sustainability Science and Management, 7(7), 152-165.

  • Yñiguez, A. T., Lim, P. T., Leaw, C. P., Jipanin, S. J., Iwataki, M., Benico, G., & Azanza, R. V. (2021). Over 30 years of HABs in the Philippines and Malaysia: What have we learned?. Harmful Algae, 102, 101776.

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