Cite this paper:
Xiuping HE, Junhui CHEN, Jiuming WANG, Xia SUN, Ming XIN, Baodong WANG, Shengkang LIANG. Spatial variation of lipophilic marine algal toxins and its relationship with physicochemical parameters in spring in Laizhou Bay, China[J]. Journal of Oceanology and Limnology, 2022, 40(6): 2242-2255

Spatial variation of lipophilic marine algal toxins and its relationship with physicochemical parameters in spring in Laizhou Bay, China

Xiuping HE1,2,3,4, Junhui CHEN1,2,3,4, Jiuming WANG1, Xia SUN1,2,3, Ming XIN1,2,3, Baodong WANG1,2,3, Shengkang LIANG5
1 Marine Bioresource and Environment Research Center, Key Laboratory of Marine Eco-Environmental Science and Technology, First Institute of Oceanography, Ministry of Natural Resources, Qingdao 266061, China;
2 Laboratory for Marine Ecology and Environmental Science, Pilot National Laboratory for Marine Science and Technology(Qingdao), Qingdao 266237, China;
3 Qingdao Key Laboratory of Analytical Technology Development and Standardization of Chinese Medicines, Qingdao 266590, China;
4 Shandong University of Science and Technology, Qingdao 266590, China;
5 Key Laboratory of Marine Chemistry Theory and Technology, Ministry of Education, Ocean University of China, Qingdao 266100, China
Lipophilic marine algal toxins (LMATs) are produced by some toxigenic microalgae, which pose a serious threat to marine ecosystem and even human health. The occurrence and environmental control factors of LMATs in the surface seawater and phytoplankton in spring in Laizhou Bay in which Huanghe (Yellow) River estuary is included, in Shandong, East China were investigated. Okadaic acid (OA), pectenotoxin-2 (PTX2), dinophysistoxin-1 (DTX1), pectenotoxin-2 seco acid (PTX2 SA), DTX2, 7-epi-PTX2 SA, PTX11, and 13-desmethyl spirolide C (SPX1) were detected from the surface seawater samples, and PTX2, 7-epi-PTX2 SA, OA, DTX2, DTX1, PTX2 SA, and PTX11 were discovered in the phytoplankton samples showed a decreasing trend. The concentrations of ∑LMATs in the seawater and phytoplankton ranged 2.03–74.38 ng/L on average of 13.72 ng/L and 0.98–479.27 pg/L on average of 50.20 pg/L, respectively. The joint influence of terrigenous input and internal circulation could promote the growth, toxin production, and toxin release of toxin-producing algae, leading to a higher content of LMATs in the bay nearby the Huanghe River estuary in both seawater and phytoplankton. The concentration of LMATs in spring was higher than that in summer, showing obvious seasonal variation. In addition, no significant correlation between most of the physiochemical parameters and LMAT contents in seawater was revealed by correlation analysis except for the positive correlation between DTX2 and chlorophyll a, OA and NH4-N. However, the increase of dissolved inorganic nitrogen content in seawater could enhance the production of OA, DTX1, and DTX2 in phytoplankton due probably to that the inorganic N input could benefit the growth and stimulate toxin production of toxin-producing algae. The result also proved that some PTX2 may be originated from Procentrum spp. and OA, DTXs and part of PTX2 may be originated from Dinophysis spp.
Key words:    lipophilic marine algal toxin|Laizhou Bay|seawater|phytoplankton|environmental factor   
Received: 2022-02-21   Revised:
PDF (939 KB) Free
Print this page
Add to favorites
Email this article to others
Articles by Xiuping HE
Articles by Junhui CHEN
Articles by Jiuming WANG
Articles by Xia SUN
Articles by Ming XIN
Articles by Baodong WANG
Articles by Shengkang LIANG
Ajani P A, Larsson M E, Rubio A et al. 2016. Modelling bloom formation of the toxic dinoflagellates Dinophysis acuminata and Dinophysis caudata in a highly modified estuary, south eastern Australia. Estuarine, Coastal and Shelf Science, 183: 95-106.
Armi Z, Turki S, Trabelsi E et al. 2012. Occurrence of diarrhetic shellfish poisoning (DSP) toxins in clams (Ruditapes decussatus) from Tunis north lagoon. Environmental Monitoring and Assessment, 184(8): 5085-5095.
Basti L, Suzuki T, Uchida H et al. 2018. Thermal acclimation affects growth and lipophilic toxin production in a strain of cosmopolitan harmful alga Dinophysis acuminata.Harmful Algae, 73: 119-128.
Basti L, Uchida H, Matsushima R et al. 2015. Influence of Temperature on growth and production of pectenotoxin-2 by a monoclonal culture of Dinophysis caudata. Marine Drugs, 13(12): 7124-7137.
Bosch-Orea C, Sanchís J, Farré M et al. 2017. Analysis of lipophilic marine biotoxins by liquid chromatography coupled with high-resolution mass spectrometry in seawater from the Catalan Coast. Analytical and Bioanalytical Chemistry, 409(23): 5451-5462.
Chen J H, Han T Z, Li X T et al. 2018. Occurrence and distribution of marine natural organic pollutants: lipophilic marine algal toxins in the Yellow Sea and the Bohai Sea, China. Science of the Total Environment, 612: 931-939.
Chen J H, Li X, Wang S et al. 2017. Screening of lipophilic marine toxins in marine aquaculture environment using liquid chromatography-mass spectrometry. Chemosphere, 168: 32-40.
De Schrijver K, Maes I, De Man L et al. 2002. An outbreak of diarrhoeic shellfish poisoning in Antwerp, Belgium.Eurosurveillance, 7(10): 138-141.
Elgarch A, Vale P, Rifai S et al. 2008. Detection of diarrheic shellfish poisoning and azaspiracids toxins in Moroccan mussels: comparison of LC-MS method with the commercial immunoassay kit. Marine Drugs, 6(4): 587-594.
Farabegoli F, Blanco L, Rodríguez L et al. 2018. Phycotoxins in marine shellfish: origin, occurrence and effects on humans. Marine Drugs, 16(6): 188.
Gerssen A, Mulder P P J, De Boer J. 2011. Screening of lipophilic marine toxins in shellfish and algae:Development of a library using liquid chromatography coupled to orbitrap mass spectrometry. Analytica Chimica Acta, 685(2): 176-185.
Grattan L M, Holobaugh S, Morris J G. 2016. Harmful algal blooms and public health. Harmful Algae, 57: 2-8.
Guo F, Wang B D, Xin M et al. 2017. Nutrient distributions in the Laizhou Bay in spring and summer of 2015. Advances in Marine Science, 35(2): 258-266. (in Chinese with English abstract)
Hackett J D, Tong M M, Kulis D M et al. 2009. DSP toxin production de novo in cultures of Dinophysis acuminata(Dinophyceae) from North America. Harmful Algae, 8(6):873-879.
Hallegraeff G M. 2010. Ocean climate change, phytoplankton community responses, and harmful algal blooms:a formidable predictive challenge. Limnology and Oceanography, 46(2): 220-235.
Hattenrath-Lehmann T, Gobler C J. 2015. The contribution of inorganic and organic nutrients to the growth of a North American isolate of the mixotrophic dinoflagellate, Dinophysis acuminata. Limnology and Oceanography, 60(5): 1588-1603.
Hattenrath-Lehmann T K, Marcoval M A, Mittlesdorf H et al. 2015. Nitrogenous nutrients promote the growth and toxicity of Dinophysis acuminata during estuarine bloom events. PLoS One, 10(4): e0124148.
He X P, Chen J H, Wu D N et al. 2019. Distribution characteristics and environmental control factors of lipophilic marine algal toxins in Changjiang estuary and the adjacent East China Sea. Toxins, 11(10): 596.
He X P, Chen J H, Wu D N et al. 2020. Occurrence, distribution, source, and influencing factors of lipophilic marine algal toxins in Laizhou Bay, Bohai Sea, China. Marine Pollution Bulletin, 150: 110789.
Holmes M J, Teo S L M. 2002. Toxic marine dinoflagellates in Singapore waters that cause seafood poisonings. Clinical and Experimental Pharmacology and Physiology, 29(9):829-836.
Hossen V, Jourdan-da Silva N, Guillois-Bécel Y et al. 2011.Food poisoning outbreaks linked to mussels contaminated with okadaic acid and ester dinophysistoxin-3 in France, June 2009. Eurosurveillance, 16(3): 1-7.
Huang D J, Su J L, Zhang L R. 1998. Numerical study of the winter and summer circulation in the Bohai Sea. Acta Aerodynamica Sinica, 16(1): 115-121. (in Chinese with English abstract)
Huang L, Zou Y, Weng H W et al. 2015. Proteomic profile in Perna viridis after exposed to Prorocentrum lima, a dinoflagellate producing DSP toxins. Environmental Pollution, 196: 350-357.
Jiang T, Liu L, Li Y et al. 2017. Occurrence of marine algal toxins in oyster and phytoplankton samples in Daya Bay, South China Sea. Chemosphere, 183: 80-88.
Jørgensen K, Andersen P. 2007. Relation between the concentration of Dinophysis acuminata and diarrheic shellfish poisoning toxins in blue mussels (Mytilus edulis)during a toxic episode in the Limfjord (Denmark), 2006.Journal of Shellfish Research, 26(4): 1081-1087.
Kamiyama T, Nagai S, Suzuki T et al. 2010. Effect of temperature on production of okadaic acid, dinophysistoxin-1, and pectenotoxin-2 by Dinophysis acuminata in culture experiments. Aquatic Microbial Ecology, 60(2): 193-202.
Kim J H, Lee K J, Suzuki T et al. 2010. Seasonal variability of lipophilic shellfish toxins in bivalves and waters, and abundance of Dinophysis spp. in Jinhae Bay, Korea.Journal of Shellfish Research, 29(4): 1061-1067.
Koukaras K, Nikolaidis G. 2004. Dinophysis blooms in Greek coastal waters (Thermaikos Gulf, NW Aegean Sea).Journal of Plankton Research, 26(4): 445-457.
Lefebvre K A, Bill B D, Erickson A et al. 2008. Characterization of intracellular and extracellular saxitoxin levels in both field and cultured Alexandrium spp. samples from Sequim Bay, Washington. Marine Drugs, 6(2): 103-116.
Li A F, Sun G, Qiu J B et al. 2015. Lipophilic shellfish toxins in Dinophysis caudata picked cells and in shellfish from the East China Sea. Environmental Science and Pollution Research, 22(4): 3116-3126.
Li A F, Li M H, Qiu J B et al. 2018. Effect of suspended particulate matter on the accumulation of dissolved diarrhetic shellfish toxins by mussels (Mytilus galloprovincialis) under laboratory conditions. Toxins, 10(7): 273.
Li F L, Li Z X, Guo M M et al. 2016. Investigation of diarrhetic shellfish toxins in Lingshan Bay, Yellow Sea, China, using solid-phase adsorption toxin tracking (SPATT). Food Additives & Contaminants: Part A, 33(8): 1367-1373.
Li M H, Sun G, Qiu J B et al. 2017. Occurrence and variation of lipophilic shellfish toxins in phytoplankton, shellfish and seawater samples from the aquaculture zone in the Yellow Sea, China. Toxicon, 127: 1-10.
Li X, Li Z Y, Chen J H et al. 2014. Detection, occurrence and monthly variations of typical lipophilic marine toxins associated with diarrhetic shellfish poisoning in the coastal seawater of Qingdao City, China. Chemosphere, 111: 560-567.
Likumahua S, De Boer M K, Krock B et al. 2020. Variability of dinoflagellates and their associated toxins in relation with environmental drivers in Ambon Bay, eastern Indonesia.Marine Pollution Bulletin, 150: 110778.
Liu Y, Yu R C, Kong F Z et al. 2017. Lipophilic marine toxins discovered in the Bohai Sea using high performance liquid chromatography coupled with tandem mass spectrometry.Chemosphere, 183: 380-388.
MacKenzie L, Holland P, McNabb P et al. 2002. Complex toxin profiles in phytoplankton and Greenshell mussels(Perna canaliculus), revealed by LC-MS/MS analysis.Toxicon, 40(9): 1321-1330.
Mackenzie L A. 2019. A long-term time series of Dinophysis acuminata blooms and associated shellfish toxin contamination in Port Underwood, Marlborough Sounds, New Zealand. Toxins, 11(2): 74.
Madigan T L, Lee K G, Padula D J et al. 2006. Diarrhetic shellfish poisoning (DSP) toxins in South Australian shellfish. Harmful Algae, 5(2): 119-123.
Mafra L L, Nolli P K W, Mota L E et al. 2019. Multi-species okadaic acid contamination and human poisoning during a massive bloom of Dinophysis acuminata complex in southern Brazil. Harmful Algae, 89: 101662.
Miles C O, Wilkins A L, Munday R et al. 2004. Isolation of pectenotoxin-2 from Dinophysis acuta and its conversion to pectenotoxin-2 seco acid, and preliminary assessment of their acute toxicities. Toxicon, 43(1): 1-9.
Nicolas J, Hoogenboom R L A P, Hendriksen P J M et al. 2017.Marine biotoxins and associated outbreaks following seafood consumption: prevention and surveillance in the 21st century. Global Food Security, 15: 11-21.
Nielsen L T, Krock B, Hansen P J. 2012. Effects of light and food availability on toxin production, growth and photosynthesis in Dinophysis acuminata. Marine Ecology-Progress Series, 471: 37-50.
Pan L, Chen J H, Shen H H et al. 2017. Profiling of extracellular toxins associated with diarrhetic shellfish poison in Prorocentrum lima culture medium by high-performance liquid chromatography coupled with mass spectrometry.Toxins, 9(10): 308.
Parsons T R, Maita Y, Lalli C M, 1984. A Manual of Chemical and Biological Methods for Seawater Analysis. Pergamon Press, New York, NY, USA.
Reguera B, Pizarro G. 2008. Planktonic dinoflagellates which produce polyether toxins of the Old DSP complex.In: Botana L M ed. Seafood and Freshwater Toxins:Pharmacology, Physiology and Detection. 2nd edn. Taylor& Francis, London, UK, p.257-284.
Reguera B, Riobó P, Rodríguez F et al. 2014. Dinophysis toxins: Causative organisms, distribution and fate in shellfish. Marine Drugs, 12(1): 394-461.
Sahraoui I, Bouchouicha D, Mabrouk H H et al. 2013.Driving factors of the potentially toxic and harmful species of Prorocentrum Ehrenbergin a semi-enclosed Mediterranean lagoon (Tunisia, SW Mediterranean).Mediterranean Marine Science, 14(2): 353-362.
Sun X P. 2006. Regional Oceanography in China Seas. China Ocean Press, China, Beijing, 376p.
Suzuki T, Miyazono A, Baba K et al. 2009. LC-MS/MS analysis of okadaic acid analogues and other lipophilic toxins in single-cell isolates of several Dinophysis species collected in Hokkaido, Japan. Harmful Algae, 8(2): 233-238.
Suzuki T, Igarashi T, Ichimi K et al. 2005. Kinetics of diarrhetic shellfish poisoning toxins, okadaic acid, dinophysistoxin-1, pectenotoxin-6 and yessotoxin in scallops Patinopecten yessoensis. Fisheries Science, 71(4): 948.
Takahashi E, Yu Q M, Eaglesham G et al. 2007. Occurrence and seasonal variations of algal toxins in water, phytoplankton and shellfish from North Stradbroke Island, Queensland, Australia. Marine Environmental Research, 64(4): 429-442.
Taylor M, McIntyre L, Ritson M et al. 2013. Outbreak of diarrhetic shellfish poisoning associated with mussels, British Columbia, Canada. Marine Drugs, 11(5): 1669-1676.
Trainer V L, Moore L, Bill B D et al. 2013. Diarrhetic shellfish toxins and other lipophilic toxins of human health concern in Washington State. Marine Drugs, 11(6): 1815-1835.
Villalobos L G, Santinelli N, Sastre V et al. 2015. Dinophysis Species Associated with Diarrhetic Shellfish Poisoning Episodes in North Patagonian Gulfs (Chubut Argentina).Journal of Shellfish Research, 34(3): 1141-1149.
Visciano P, Schirone M, Berti M et al. 2016. Marine biotoxins:occurrence, toxicity, regulatory limits and reference methods. Frontiers in Microbiology, 7: 1051.
Wang J M, Chen J H, He X P et al. 2021. Simple determination of six groups of lipophilic marine algal toxins in seawater by automated on-line solid phase extraction coupled to liquid chromatography-tandem mass spectrometry.Chemosphere, 262: 128374.
Wang Y L, Chen J H, Li Z Y et al. 2015. Determination of typical lipophilic marine toxins in marine sediments from three coastal bays of China using liquid chromatographytandem mass spectrometry after accelerated solvent extraction. Marine Pollution Bulletin, 101(2): 954-960.
Wu D N, Chen J H, He X P et al. 2019. Distribution, partitioning, and seasonal variation of lipophilic marine algal toxins in aquatic environments of a typical semi-closed mariculture bay. Environmental Pollution, 255: 113299.
Yu R C, Liu D Y. 2016. Harmful algal blooms in the coastal waters of China: current situation, long-term changes and prevention strategies. Bulletin of the Chinese Academy of Sciences, 31(10): 1167-1174. (in Chinese with English abstract)
Zhang J F, Gao X L. 2015. Heavy metals in surface sediments of the intertidal Laizhou Bay, Bohai Sea, China:distributions, sources and contamination assessment.Marine Pollution Bulletin, 98(1-2): 320-327.
Zhao B R, Zhuang G W, Cao D M. 1995. Circulation, tidal residual currents and their effects on the sedimentations in the Bohai Sea. Oceanologia et Limnologia Sinica, 26(5):466-473. (in Chinese with English abstract)
Copyright © Haiyang Xuebao