Progress in Fishery Sciences (Feb 2023)
Accumulation and Transformation of Paralytic Shellfish Toxin in Mussel Mytilus galloprovincialis Exposed to Alexandrium catenella
Abstract
Paralytic shellfish toxins (PSTs) are phycotoxins widely distributed worldwide and pose serious marine ecosystems and human health threats. In China's Yellow Sea and the Bohai Sea, Alexandrium spp. has been certified as the major causative dinoflagellate of PSTs, especially in Qinhuangdao, Hebei Province where several poisoning events have been reported, with tens of consumers suffering and some even dying. In terms of these events, mussels contaminated with PSTs were the major cause of consumer poisoning. Therefore, it is vital to reveal the risk of PSTs in these shellfish, which requires scientific opinions on the formation of terminal components of PSTs in mussels. Generally, mussels are not sensitive to PSTs, resulting in the high accumulation of PSTs in their tissues. The PSTs distribute, bio-transfer, and metabolism, and the terminal metabolites pose a risk to consumers. From 2016 to the present, several serious events have occurred in Qinhuangdao caused by PSTs contamination in mussels, which resulted in poisoning by tens of consumers and a huge loss of regional economy. This study exposed purple mussel Mytilus galloprovincialis, the key cultured species of bivalves in Qinhuangdao, to Alexandrium catenella (GY-H25), the predominant producer of PSTs in this area. The accumulation and biotransformation process of PSTs in visceral mass and edible tissue and the accumulation metabolism kinetics were analyzed under exposure to different cell densities by liquid chromatography-tandem mass spectrometry. Our results showed that the growth and toxin production of GY-H25 was stable. The main components of PSTs were N-sulfocarbamoylgonyautoxin (C1 and C2), with the highest algal cell density of 3.5×107 cells/L and the highest production capacity of 2.96 pg STXeq/cell. Toxin-producing algae with the highest production of PSTs per unit volume and algal cell density (22 days) were selected for the exposure experiment. After exposure, the mussel accumulated a high content of PSTs in both visceral mass and edible tissue, with a similar trend in both exposure densities. The whole exposure experiment could be divided into four periods: 0~2 days as the initial exposure period (period Ⅰ); 2~7 days as the period of rapid accumulation (period Ⅱ); 7~12 days as the period of rapid metabolism (period Ⅲ); 12~30 days as the stable period (period Ⅳ). However, the level of PSTs in the visceral mass of mussels in both exposure groups exceeded the maximum residue limit (MRL) of EU (800 μg STX EQ/kg) at the end of the experiment, while that of PSTs in edible flesh was below the MRL. Comparatively, the highest concentration of PSTs in the visceral mass reached 6815.36 μg/kg in the high exposure group, which was 2.61 times that of the low exposure group, with an average accumulation rate of 17.89%, which was significantly higher than that of the low exposure group (13.06%). The results showed that the accumulation of PSTs in the visceral mass and edible tissue of Mytilus galloprovincialis was harmful to its tissues and organs. The toxin excretion rates of the high-and low-concentration groups of PSTs were 74.39 % and 59.15 %, respectively, after 23 days. The average daily elimination rate was 14.4 %, the metabolism rate of Mytilus edulis slowed down in the stable period (period Ⅳ), and some toxins remained in the visceral mass after 23 days of metabolism, which easily formed long-term toxin retention and threatened human life safety. In addition, PSTs in Mytilus galloprovincialis showed a strong biotransformation ability, mainly occurring among C1, C2, and GTX5. According to this research, the transformation pathway from C2 to GTX5 was the main pathway for GTX5 formation during rapid metabolism and stable periods. At the same time, the transformation of C1 to GTX5 was higher than that of C2 to C1, leading to a reduction in the overall proportion of C1. According to the comprehensive evaluation of the metabolic products and toxic equivalence factor (TEF) of GST components in mussels, the metabolic transformation of PSTs in mussels will further promote the formation and proportion of highly toxic GTX5, which will increase the terminal toxicity of PSTs in mussels and may also pose a higher risk to consumers. In this study, compared with the natural conditions, the concentration of toxic algae was far below the harmful algal bloom exposure. The total accumulation of toxins was far lower than the total accumulation of toxins in mussels exposed to harmful algal blooms. Even so, the total amount of residual toxins in the mussel viscera of the high concentration group was still enough to threaten human life safety at the end of the experiment. It was found that the toxin content in the visceral tissue tended to be stable over 12 to 30 days without an obvious downward trend. Even the toxin content increases due to the toxin transformation phenomenon, which means the difficulty in predicting the time required for PSTs in the visceral mass reduced to below the MRLs. Therefore, this study contributes to the scientific assessment of PSTs risk in mussels and provides a basis for establishing regional PSTs monitoring programs.
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