Accumulation and Self-Cleaning of PSP Toxins in Green Mussel, Perna viridis, Fed on Various Cell Density of Alexandrium minutum
Article Sidebar
Main Article Content
Abstract
Paralytic shellfish poisoning (PSP) is a serious threat to marine ecosystems and human health, caused by toxins from harmful algal blooms. This study investigates the accumulation and self-cleaning processes of PSP toxins in the green mussel, Perna viridis, fed various cell densities of Alexandrium minutum, a major PSP toxin producer. The first part assessed the clearance rate of the green mussels over 24 h, feeding them A. minutum at concentrations of 100, 500, 1,000, and 3,000 cells·mL-1. Results showed that clearance rates increased with higher cell density. The total PSP toxins accumulated in the mussels were proportional to the total toxin found in A. minutum. The second part of the study examined the accumulation of PSP in mussels fed A. minutum for two consecutive weeks at a cell density of 500 cells·mL-1, followed by two weeks of self-cleaning while being fed the non-toxic alga Isochrysis sp. The results showed that the PSP toxin content increased during feeding on A. minutum, surpassing the regulatory limit (0.8 µgSTXeq·g-1) after 10 days. PSP toxin levels peaked at 2.16±0.21 µgSTXeq·g-1 after 14 days, approximately 2.7 times the regulatory limit. During the self-cleaning period, toxin levels gradually declined to safe concentrations within one day, with no detectable toxins at the end of the experiment. The elimination of GTX1,4 toxin (highly toxic derivatives) was particularly rapid during the self-cleaning phase. These findings suggest that mussels could serve as an effective indicator species for early warning of PSP outbreaks.
Article Details
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
References
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 14: 10–35. DOI: 10.1016/j.hal.2011.10.012.
Asakawa, M., R. Beppu, K. Ito, M. Tsubota, H. Takayama and K. Miyazawa. 2006. Accumulation of paralytic shellfish poison (PSP) and biotransformation of its components in oysters Crassostrea gigas fed with the toxic dinoflagellate Alexandrium tamarense. Journal of the Food Hygienic Society of Japan 47(1): 28–32. DOI: 10.3358/shokueishi.47.28.
Bajarias, F.F., J. Relox and Y. Fukuyo. 2006. PSP in the Philippines: three decades of monitoring a disaster. Coastal Marine Science 30(1): 104–106.
Bricelj, V., J. Lee, A. Cembella and D. Anderson. 1990. Uptake kinetics of paralytic shellfish toxins from the dinoflagellate Alexandrium fundyense in the mussel Mytilus edulis. Marine Ecology 63: 177–188.
Bricelj, V. and S. Shumway. 1998. Paralytic shellfish toxins in bivalve molluscs: Occurrence, transfer kinetics, and biotransformation. Reviews in Fisheries Science 6(4): 315–383.
Burrell, S., T. Gunnarsson, K. Gunnarsson, D. Clarke and A.D. Turner. 2012. First detection of paralytic shellfish poisoning (PSP) toxins in Icelandic mussels (Mytilus edulis): Links to causative phytoplankton species. Food Control 31(2): 295–301.
Carreto, J.I. and H.R. Benavide. 1993. World record of PSP in Southern Argentina. Harmful Algal News, IOC/UNESCO 5(2). https://unesdoc.unesco.org/ark:/48223/pf0000178854. Cited 24 Dec 2024.
Chen, C.Y. and H.N. Chou. 2001. Accumulation and depuration of paralytic shellfish poisoning toxins by purple clam Hiatula rostrata Lighttoot. Toxicon 39(7): 1029–1034. DOI: 10.1016/s0041-0101(00)00242-7.
Choi, N., D. Hsieh, P. Lam and W.X. Wang. 2003. Field depuration and biotransformation of paralytic shellfish toxins in scallop Chlamys nobilis and green-lipped mussel Perna viridis. Marine Biology 143: 927–934. DOI: 10.1007/s00227-003-1148-y.
Coughlan, J. 1969. The estimation of filtering rate from the clearance of suspensions. Marine Biology 2(4): 356–358.
Department of Fisheries. 2022. Statistics of Marine Shellfish Culture Survey 2021 No. 5/2022. Fishery Statistics Group, Fisheries Development Policy and Planning Division, Department of Fisheries, Ministry of Agriculture and Cooperatives, Bangkok, Thailand. 29 pp.
Fish Inspection and Quality Control Division, Department of Fisheries. 2016. Quantitative Determination of Paralytic Shellfish Poisoning Toxins Using HPLC No.TC-15. Department of Fisheries, Ministry of Agriculture and Cooperatives, Bangkok, Thailand. 25 pp.
Fu, Z., A. Piumsomboon, P. Punnarak, P. Uttayarnmanee, C. P. Leaw, P.T. Lim, A. Wang and H. Gu. 2021. Diversity and distribution of harmful microalgae in the Gulf of Thailand assessed by DNA metabarcoding. Harmful algae 106: 102063. DOI: 10.1016/j.hal.2021.102063.
Guéguen, M., B. Michele, R. Baron, L. Patrick, T. Philippe, M. Julie and Z. Amzil. 2008. Detoxification of Pacific oyster Crassostrea gigas fed on diets of Skeletonema costatum with and without silt, following PSP contamination by Alexandrium minutum. Aquatic Living Resources 21(1): 13–20. DOI: 10.1051/alr:2008010.
Haberkorn, H., D. Tran, J.C. Massabuau, P. Ciret, V. Savar and P. Soudant. 2011. Relationship between valve activity, microalgae concentration in the water and toxin accumulation in the digestive gland of the Pacific oyster Crassostrea gigas exposed to Alexandrium minutum. Marine Pollution Bulletin 62(6): 1191–1197. DOI: 10.1016/j.marpolbul.2011.03.034.
Hégaret, H., S. Shumway, G. Wikfors, S. Pate and J. Burkholder. 2008. Potential transport of harmful algae via relocation of bivalve molluscs. Marine Ecology 361: 169–179. DOI: 10.3354/meps07375.
IBM Corp. 2017. IBM SPSS Statistics for Windows, Version 25.0. Armonk, New York, USA.
Ichimi, K., T. Suzuki and M. Yamasaki. 2001. Non-selective retention of PSP toxins by the mussel Mytilus galloprovincialis fed with the toxic dinoflagellate Alexandrium tamarense. Toxicon 39: 1917–1921. DOI: 10.1016/s0041-0101(01)00177-5.
Jørgensen, B.C. 1996. Bivalve filter feeding revisited. Marine Ecology Progress Series 142: 287–302.
Kao, C.Y. 1996. Tetrodotoxin, saxitoxin and their significance in the study of excitation phenomena. Pharmacological Reviews 18: 997–1049.
Kodama, M. and S. Sato. 2008. Metabolism of paralytic shellfish toxins incorporated into bivalves. In: Seafood and Freshwater Toxins: Pharmacology, Physiology and Detection, 2nd ed. (ed. L.M. Botana), pp. 165–175. CRC Press, Florida, USA.
Kodama, M. 2010. Paralytic shellfish poisoning toxins: Biochemistry and origin. Aqua-BioScience Monographs 3(1): 1–38. DOI: 10.3390/toxins12050344.
Kusnoputranto, H., S. Moersidik, D. Wisnubroto and M. Makmur. 2014. Accumulation and depuration of PSP toxin (paralytic shellfish poisoning) by green mussels. Indonesian Journal of Marine Sciences 19(1): 27–34.
Kwong, R.W.M., W.X. Wang, P.K.S. Lam and P.K.N. Yu. 2006. The uptake, distribution and elimination of paralytic shellfish toxins in mussels and fish exposed to toxic dinoflagellates. Aquatic Toxicology 80(1): 82–91.
Lau, W.L.S., I.K. Law, G.R. Liow, K.S. Hii, G. Usup, P.T. Lim and C.P. Leaw. 2017. Life-history stages of natural bloom populations and the bloom dynamics of a tropical Asian ribotype of Alexandrium minutum. Harmful Algae 70: 52–63. DOI: 10.1016/j.hal.2017.10.006.
Li, S.C., W.X. Wang and D.P. Hsieh. 2001. Feeding and absorption of the toxic dinoflagellate Alexandrium tamarense by two marine bivalves from the South China Sea. Marine Biology 139(4): 617–624. DOI: 10.1007/s002270100613.
Lim, P.T., C.P. Leaw and G. Usup. 2004. First incidence of paralytic shellfish poisoning on the east coast of Peninsular Malaysia. In: Marine Science into the New Millennium: New Perspectives and Challenges (eds. S.M. Phang, V.C. Chong, S.S. Ho, N. Mokhtar and J.L.S. Ooi), pp. 661–667. University of Malaya, Maritime Research Centre, Kuala Lumpur, Malaysia.
Lim, P.T., G. Usup and C.P. Leaw. 2012. Harmful algal blooms in Malaysian waters. Sains Malaysiana 41(12): 1509–1515.
Liu, Y., F.Z. Kong, X.G. Xun, L. Dai, H.X. Geng, X.L. Hu, R.C. Yu, Z.M. Bao and M.J. Zhou. 2020. Biokinetics and biotransformation of paralytic shellfish toxins in different tissues of Yesso scallops, Patinopecten yessoensis. Chemosphere 261: 128063. DOI: 10.1016/j.chemosphere.2020.128063.
McFarren, E.F., M.L. Schafer, J.E. Campbell, K.H. Lewis, E.T. Jensen and E.J. Schantz. 1961. Public health significance of paralytic shellfish poison. Advances in Food Research 10: 135–179.
Mok, J.S., E.G. Oh, K.T. Son, T.S. Lee, K.J. Lee, K.C. Song and J.H. Kim. 2012. Accumulation and depuration of paralytic shellfish poison in marine organisms. Korean Journal of Fisheries and Aquatic Sciences 45: 465–471.
Montojo, U., M.I. Romero, V.M. Borja, M.F. Cayme, S. Sato, M. Kodama and Y. Fukuyo. 2012. Vulnerability of tropical shellfishes against PSP contamination during bloom of Pyrodinium bahamense var. compressum. Coastal Marine Science 35(1): 64–66.
Phumphoung, P., T. Lirdwitayaprasit and S. Subsinserm. 2019. Growth and toxin in Alexandrium minutum isolated from Chao Phraya River mouth. Proceedings of 9th National Conference on Algae and Plankton 2019: 53–58.
Piumsomboon, A., C. Songroop, A. Kungsuwan and P. Pholpunthin. 2001. Species of the dinoflagellate genus Alexandrium (Gonyaulacales) in the Gulf of Thailand. In: Harmful Algal Bloom 2000 (eds. G.M. Hallegraeff, S.I. Blackburn, C.J. Bolch and R.J. Lewis), pp. 12–15. IOC/UNESCO, Paris, France.
Prakoon, W., S. Tunkijjanukij, T.T. Nguyen and U. Na-Nakorn. 2010. Spatial and temporal genetic variation of green mussel, Perna viridis in the Gulf of Thailand and implication for aquaculture. Marine Biotechnology 12(5): 506–515. DOI: 10.1007/s10126-009-9234-x.
Qiu, J., H. Fan, T. Liu, X. Liang, F. Meng, M.A. Quilliam and A. Li. 2018. Application of activated carbon to accelerate detoxification of paralytic shellfish toxins from mussels Mytilus galloprovincialis and scallops Chlamys farreri. Ecotoxicology and Environmental Safety 148: 402–409.
Samsur, M., Y. Yamaguchi, T. Sagara, T. Takatani, O. Arakawa and T. Noguchi. 2006. Accumulation and depuration profiles of PSP toxins in the short-necked clam Tapes japonica fed with the toxic dinoflagellate Alexandrium catenella. Toxicon 48: 323–330. DOI: 10.1016/j.toxicon.2006.06.002.
Sekiguchi, K., O. Takehiko, S. Kaga, Y. Makoto, Y. Fukuyo and M. Kodama. 2001. Accumulation of paralytic shellfish toxins in the scallop Patinopecten yessoensis caused by the dinoflagellate Alexandrium catenella in Otsuchi Bay, Iwate Prefecture, Northern Pacific Coast of Japan. Fisheries Science 67(6): 1157–1162.
Shimizu, Y. 1978. Dinoflagellate toxins. In: Marine Natural Products (ed. P.J. Scheuer), pp. 1–42. Academic Press, New York, USA.
Shimizu, Y. and M. Yoshioka. 1981. Transformation of paralytic shellfish toxins as demonstrated in scallop homogenates. Science 212(4494): 547–549.
Songroop, C. 1998. Morphology and toxin production of dinoflagellate genus Alexandrium in the upper gulf of Thailand. Master thesis in Marine Science, Graduate School, Chulalongkorn University, Bangkok, Thailand. 118 pp.
Suvapepun, S. 1984. Shellfish poisoning in association with the occurrence of potentially toxic dinoflagellates in the Gulf of Thailand. Toxic red tides and shellfish toxicity in Southeast Asia: Proceedings of a consultative meeting held in Singapore, 11–14 Sep 1984: 87–89.
Suzuki, T., K. Ichimi, Y. Oshima and T. Kamiyama. 2003. Paralytic shellfish poisoning (PSP) toxin profiles and short-term detoxification kinetics in mussels Mytilus galloprovincialis fed with the toxic dinoflagellate Alexandrium tamarense. Harmful Algae 2: 201–206. DOI: 10.1016/S1568-9883(03)00042-8.
Velásquez, C. and J.M. Navarro. 2014. Feeding and intoxication–detoxification dynamics in two populations of the mussel Mytilus chilensis (Hupé, 1854) with different histories of exposure to paralytic shellfish poisoning (PSP). Marine and Freshwater Behaviour and Physiology 47(3): 185–195.
Wang, Z.H., X.P. Nie, S.J. Jiang, J.G. Zhao, Y. Cao, Y.J. Zhang and D.Z. Wang. 2011. Source and profile of paralytic shellfish poisoning toxins in shellfish in Daya Bay, South China Sea. Marine Environmental Research 72(1): 53–59. DOI: 10.1016/j.marenvres.2011.04.007.