Comparison of short-term toxicity of 14 common phycotoxins (alone and in combination) to the survival of brine shrimp <i>Artemia salina</i>

Comparison of short-term toxicity of 14 common phycotoxins (alone and in combination) to the survival of brine shrimp Artemia salina

PDF

Yuting Zhang¹^,², Shanshan Song³, Bin Zhang³, Yang Zhang³, Miao Tian¹^,², Ziyi Wu¹, Huorong Chen⁴, Guangmao Ding⁴, Renyan Liu³^,^*, Jingli Mu¹^,²^,^*

Acta Oceanologica Sinica | 2023, 42(2) : 134 - 141

Less

Acta Oceanologica Sinica | 2023, 42(2): 134-141

• Marine Biology •

Comparison of short-term toxicity of 14 common phycotoxins (alone and in combination) to the survival of brine shrimp Artemia salina

Full

Yuting Zhang¹^,², Shanshan Song³, Bin Zhang³, Yang Zhang³, Miao Tian¹^,², Ziyi Wu¹, Huorong Chen⁴, Guangmao Ding⁴, Renyan Liu³^,^*, Jingli Mu¹^,²^,^*

Affiliations

¹ Institute of Oceanography, College of Geography and Oceanography, Minjiang University, Fuzhou 350108, China

² Fuzhou Institute of Oceanography, Fuzhou 350108, China

³ Department of Marine Chemistry, National Marine Environmental Monitoring Center, Dalian 116023, China

⁴ Fujian Marine Environment and Fishery Resource Monitoring Center, Fuzhou 350003, China

Published: 2023-02-25 doi: 10.1007/s13131-022-2120-3

Outline

Abstract

Less

Toxic harmful algal blooms (HABs) can cause deleterious effects in marine organisms, threatening the stability of marine ecosystems. It is well known that different strains, natural populations and growth conditions of the same toxic algal species may lead to different amount of phycotoxin production and the ensuing toxicity. To fully assess the ecological risk of toxic HABs, it is of great importance to investigate the toxic effects of phycotoxins in marine organisms. In this study, the short-term toxicity of 14 common phycotoxins (alone and in combination) in the marine zooplankton Artemia salina was investigated. The 48 h LC₅₀ of the 14 phycotoxins varied from 0.019 3 µg/mL to 2.415 µg/mL. The most potent phycotoxin was azaspiracids-3 (AZA3; with a LC₅₀ of 0.019 3 µg/mL), followed by azaspiracids-2 (AZA2; 0.022 6 µg/mL), pectenotoxin-2 (PTX2; 0.046 0 µg/mL) and dinophysistoxin-1 (DTX1; 0.081 8 µg/mL). For the binary exposure, okadaic acid (OA) induced potential additive effects with DTX1, probably due to their similar structure (polyether fatty acid) and mode of action (attacking the serine/threonine phosphoprotein phosphatases). On the other hand, OA showed potential antagonistic effects with PTX2, which might be accounted for by their activation on the detoxification activity of cytochrome P450 activity. In addition, DTX1 induced potential synergetic effects with saxitoxin (STX), yessotoxin (YTX) or PTX2, suggesting the hazard potency of the mixtures of DTX1 and other phycotoxins (like STX, YTX and PTX2) with regard to the ecological risk. These results provide valuable toxicological data for assessing the impact of phycotoxins on marine planktonic species and highlight the potential ecological risk of toxic HABs in marine ecosystems.

Key words

LC₅₀ / harmful algal blooms / binary exposure / ecological risk

Cite this Article

Yuting Zhang, Shanshan Song, Bin Zhang, Yang Zhang, Miao Tian, Ziyi Wu, Huorong Chen, Guangmao Ding, Renyan Liu, Jingli Mu. Comparison of short-term toxicity of 14 common phycotoxins (alone and in combination) to the survival of brine shrimp Artemia salina[J]. Acta Oceanologica Sinica, 2023 , 42 (2) : 134 -141 . DOI: 10.1007/s13131-022-2120-3

Full Text

Less

1 Introduction

Less

The frequency, scale and magnitude of harmful algal blooms (HABs) have increased in the past decades, due to overfishing, coastal eutrophication, global climate change and invasive species dispersal (De Rijcke et al., 2016). For instance, it is reported that the frequency of HABs along Chinese coast has increased at a rate of 40%±4% per decade from 1970 to 2015 (Xiao et al., 2019). HABs can be classified in two categories, according to the mechanisms underlying the negative impacts: (1) non-toxic HABs, which lead to deterioration of water quality by an excessive increase of turbidity and dissolved oxygen consumption; (2) toxic HABs, which synthesize powerful phycotoxins negatively impacting aquaculture, ecological stability and even public health (Simões et al., 2015). Phycotoxins are natural metabolites produced by micro-algae, including dinoflagellates, phytoplankton, cyanobacteria and etc., that inhabit marine, brackish, or freshwater bodies or soils (Quilliam, 1999). It has been well documented that phycotoxins produced by toxic algae species can lead to acute illness in humans (Turki et al., 2014). For example, diarrheic shellfish poisoning (DSP) is mainly due to the phycotoxins (such as okadaic acid and dinophysistoxin) produced by toxic strains of Prorocentrum spp. and Dinophysis spp. (Dickey et al., 1990; Yasumoto, 1990; Bravo et al., 2001), and paralytic shellfish poisoning (PSP) is predominantly linked to the phycotoxins (such as saxitoxin) by toxic strains of Alexandrium spp. (Hallegraeff, 1993; Abdenadher et al., 2012; Anderson et al., 2012).

Besides human-health concerns, phycotoxins produced by toxic HABs can cause deleterious effects in many aquatic organisms, threatening ecological health and stability (Suganuma et al., 1988; Durbin et al., 2002; Zhang et al., 2009; Faassen et al., 2012). Zooplanktons, channeling primary production to higher trophic levels, play a crucial role in marine ecosystems. It is documented that when toxic HABs occur, the produced phycotoxins would induce adverse effects on zooplankton, resulting in a reduction of species diversity (Jonsson et al., 2009; Xu et al., 2017). The responses of zooplankton to toxic HABs vary significantly, mainly depending on the species of toxic algae (Turner , 2014; Xu et al., 2017). However, when exposed to the same species of toxic alga, copepods may give distinct responses (Xu et al., 2017). One possible reason is that different strains, natural populations and growth conditions of the same algal species lead to different amount of phycotoxin production and the ensuing toxicity (Xu et al., 2017). Therefore, to fully conclude the toxicity of HABs and to well compare the potential toxicity of different toxic alga species in zooplankton, it is necessary to include the use of phycotoxins. However, toxicological data for the toxic effects of phycotoxins in aquatic organisms are limited. To date, the median-lethal concentrations (LC₅₀) of okadaic acid (OA); dinophysistoxin-1 (DTX1), saxitoxin (STX), brevetoxin-2 (PbTx2) and brevetoxin-3 (PbTx3) in aquatic organisms have been documented (D’ors et al., 2014; Figueroa et al., 2020; Kirkpatrick et al., 2004; Shaw et al., 1997), but not for other common phycotoxins such as pectenotoxin-2 (PTX2), yessotoxin (YTX), homo-yessotoxin, (hYTX), 13-desmethyl spirolide C (SPX1), gymnodimine (GYM), azaspiracids-1 (AZA1), azaspiracids-2 (AZA2) and azaspiracids-3 (AZA3). In addition, phycotoxins do not only occur singly but also as mixtures in the real-world environment, as subordinate species might also occur during a bloom event (Smayda, 1997; Eckford-Soper and Daugbjerg, 2017), a succession from one dominant specie to another is often observed (Höglander et al., 2004) and some species can produce different analogues of phycotoxins (Alarcan et al., 2018). It is of great importance to study the toxic effects of phycotoxins, alone and in combination, in aquatic organisms, for better understanding the ecological risk of HABs.

In this study, the toxicity of 14 common phycotoxins (including OA, DTX1, PTX2, YTX, hYTX, SPX1, GYM, AZA1, AZA2, AZA3, STX, dcSTX, PbTx2 and PbTx3) on the survival of brine shrimp (Artemia salina) was investigated by assessing the LC₅₀ for 48 h. Furthermore, the combined effect (additive, antagonistic or synergistic) of two different phycotoxins on the survival of A. salina was also investigated. The overall aim of this study was to provide valuable toxicological data for evaluating the toxicity of phycotoxins in zooplankton and to help better understand the ecological risk of toxic HABs.

2 Materials and methods

Less

2.1 Phycotoxins

Certified reference standards for OA, DTX1, PTX2, YTX, hYTX, SPX1, GYM, AZA1, AZA2, AZA3, STX and dcSTX were purchased from the National Research Council Halifax, Canada. PbTx2 and PbTx3 were obtained from Taiwan Renyu Company. The stock solution of STX was dissolved in 3 mmol/L HCl, while others in methanol. The working solutions of phycotoxins were freshly prepared by serial dilution (3 mmol/L HCl for STX; methanol for the other phycotoxins) 30 min prior to each experiment.

2.2 Brine shrimp bioassay

The brine shrimp (Artemia salina) assay was carried out following the previous technique with slight modification (Lincoln et al., 1996; Hisem et al., 2011). One gram of dried A. salina cysts were hatched in filtered artificial seawater (FASW) with gentle aeration for 24 h under a 12 h light: 12 h dark cycle at (25±1)℃. The bacteria-free FASW was prepared by dissolving sea salt in tap water (salinity, 30±1; dissolved oxygen, (6.98±0.17) mg/L), followed by filtering (pore size, 0.22 μm). Newly hatched larvae were collected using a Pasteur pipette after a 24 h incubation and washed with FASW in a petri dish. After washing, A. salina were transferred to a 24-well plate (10 individuals for each well) using a pipette with a 200 μL tip. In general, at each transfer, 2−4 A. salina with approximately 5 μL carrying solution were added to the well. The total volume of carrying solution for each well was less than 20 μL. For the preparation of exposure medium, 20 μL of phycotoxin working solutions or their respective solvent (3 mmol/L HCl for STX; methanol for the other phycotoxins) was transferred into a 24-well microtiter plate with 1.98 mL FASW and 10 A. salina individuals per well. Each group had three replicates. During the exposure experiment, A. salina was not fed. The dissolved oxygen after 48 h exposure was (6.97±0.21) mg/L. The mortality was counted at 48 h using a stereomicroscope (Olympus IX71). The death of an individual was defined as follows: no appendage movements in 10 s.

For the individual exposure experiment, 8 concentrations were tested and the concentration range for most of the tested phycotoxins was from 0 μg/mL to 2 μg/mL. While for those phycotoxins with high cost (such as AZA1, AZA2, AZA3 and etc.), the concentration range was from 0 to ~0.01 μg/mL. One seawater control and two solvent controls (3 mmol/L HCl and methanol, respectively) were included and no dead brine shrimps were observed at the end of exposure. After obtaining the LC₅₀ values, we carried out 9 sets of binary exposure experiment, i.e., OA+DTX1; OA+PTX2; OA+STX; DTX1+PTX2; DTX1+STX; DTX1+YTX; DTX1+hYTX; PTX2+SPX1 and PTX2+hYTX. The phycotoxin concentration was set at 0.068 5 µg/mL (OA); 0.075 5 µg/mL (DTX1); 0.022 5 µg/mL (PTX2); 0.121 µg/mL (STX); 0.027 5 µg/mL (YTX); 0.029 µg/mL (hYTX); 0.035 µg/mL (SPX1), which were less than their respective LC₅₀ values. All the concentrations of phycotoxins mentioned above were nominal, not measured.

2.3 Statistical analysis

Bioassay data for artemia mortality were analyzed using IBM SPSS Statistics 21 software. Phycotoxin concentrations (µg/mL) that resulted in 10% and 50% mortality (i.e., LC₁₀ and LC₅₀ values) were estimated using log-probability curves with 95% confidence intervals. LC₁₀ and LC₅₀ values were determined by probabilistic regression models generated. For the binary exposure, the differences among the treatments were tested using one-way analysis of variance (ANOVA) with specific mean comparisons performed by Fisher’s least significant difference (LSD) post hoc test. Prior to ANOVA analyses, Shapiro-Wilk and Bartlett’s tests were used to test for normality and homogeneity of variances, respectively. All data were presented as means ± standard error of the mean (SEM).

3 Results

Less

3.1 Effect of each phycotoxin

The mortality-concentration curves, LC₅₀ and LC₁₀ values for OA, DTX1, PTX2, PbTx2, PbTx3, YTX, hYTX, STX, dcSTX, GYM, SPX1, AZA1, AZA2 and AZA3 in A. salina were shown in Fig. 1 and Table 1. On the basis of 48 h LC₅₀, the order of toxicity in artemia was AZA3>AZA2>PTX2>DTX1>hYTX>AZA1>SPX1>YTX>GYM>OA>dcSTX>STX>PbTx3>PbTx2. Among the tested 14 phycotoxins, the LC₅₀ value of AZA3 in artemia was the lowest (0.019 3 µg/mL), while PbTx2 showed the least toxic effect with a LC₅₀ value of 2.415 µg/mL.

3.2 Combined effect of two phycotoxins

3.2.1 Combination of OA with DTX1, PTX2 or STX

The artemia from the OA+DTX1 group exhibited higher mortality than those from the OA group (p=0.001 0), but did not show significantly higher mortality than the DTX1 treated artemia (Fig. 2A). No significant difference in the mortality was found among the OA, PTX2 and OA+PTX2 groups (Fig. 2B). Similarly, the mortality of the artemia from the OA+STX group was close to that from the OA alone group and the STX alone group (Fig. 2C).

3.2.2 Combination of DTX1 with PTX2, STX, YTX or hYTX

Relative to the mortality for the DTX1 alone group and the PTX2 alone group, the mortality of the DTX1+PTX2 treated artemia was elevated by 2.6-fold (p<0.000 1) and 10-fold (p<0.000 1), respectively (Fig. 2D). The DTX1+STX treated artemia showed significantly higher mortality than those exposed to individual phycotoxin (DTX1 alone or STX alone) (Fig. 2E). Similarly, significant increases (1.9-fold, p=0.015 and 32-fold, p<0.000 1, respectively) in the mortality were observed in the artemia exposed to DTX1+YTX relative to the artemia from the DTX1 alone group and the YTX alone group (Fig. 2F). In contrast, the artemia from the DTX1+hYTX group did not exhibit higher mortality than those from the DTX1 alone group (Fig. 2G).

3.2.3 Combination of PTX2 with SPX or hYTX

For the binary exposure to PTX2 and SPX1, no significant difference in the mortality was observed among three groups (Fig. 2H). Differently, the mortality for the PTX2+hYTX group was increased by 4.9-fold (p=0.000 2) and 11-fold (p=0.000 3) compared to that for the PTX2 group and the hYTX group, respectively (Fig. 2I).

4 Discussion

Less

The toxicity of phycotoxins has received increasing attention with the increase of frequency, scale and magnitude of toxic harmful algal blooms (HABs) in recent years (De Rijcke et al., 2016). Many studies have been mostly focused on the impacts of phycotoxins on mammals (such as mice, dogs, human cell lines and etc.) to meet the demand of seafood safety control and pollution monitoring (EFSA Panel on Contaminants in the Food Chain, 2010). However, the toxicological data in aquatic organisms is really limited (Table 2), making it difficult to fully evaluate the ecological risk of phycotoxins and toxic HABs. In this study, the short-term toxicity of 14 common phycotoxins (OA, DTX1, PTX2, YTX, hYTX, GYM, SPX1, AZA1, AZA2, AZA3, STX, dcSTX, PbTx2 and PbTx3) in A. salina was investigated. Among the 14 tested phycotoxins, AZA3 (with a LC₅₀ of 0.019 3 µg/mL) was the most toxic phycotoxin in artemia, followed by AZA2 (with a LC₅₀ of 0.022 6 µg/mL). AZAs (including AZA1, AZA2, AZA3, AZA4, AZA5 and etc.) are a group of phycotoxins produced by Azadinium spinosum (Ferreiro et al., 2016). In this study, AZA3 (with a LC₅₀ of 0.019 3 µg/mL) and AZA2 (with a LC₅₀ of 0.022 6 µg/mL) showed higher toxicity than AZA1 (with a LC₅₀ of 0.106 µg/mL). Similarly, a study in mice shows that after intraperitoneal administration, AZA2 (with a minimum lethal dose of 110 µg/kg) and AZA3 (140 µg/kg) are more toxic than AZA1 (150 µg/kg) (Toyofuku, 2006; Twiner et al., 2008). These results reinforce the concept that the toxicity of analogues might vary significantly.

To prevent human intoxications, the European Union (EU) has set regulatory limits of phycotoxins in shellfish mainly based on the toxicity on mice (Alarcan et al., 2018). The limits of OA, AZA, PTX, STX and YTX in 1 kg shellfish meat are 160 µg, 160 µg, 160 µg, 800 µg and 1 mg, respectively. This suggest that YTX might be the least toxic phycotoxin among the five phycotoxins, followed by STX. In the present study, YTX (with a LC₅₀ of 0.171 µg/mL) is found to be more toxic than STX (with a LC₅₀ of 0.899 µg/mL) and OA (with a LC₅₀ of 0.372 µg/mL) in artemia. This suggests that the toxic effects of phycotoxins in mammals (like mice) and in zooplankton (like A. salina) might be distinct. Therefore, besides of the human-health concerns, the investigation of deleterious effects of phycotoxins on marine food webs also requires attention.

The mechanism of action of phycotoxins have been studied for many years. OA and DTX1 belong to the polyether fatty acid toxins (Farabegoli et al., 2018). They share a similar mode of action, that attacking the serine/threonine phosphoprotein phosphatases (PPs), in particular PP2A, and as secondary targets, PP1 and PP2B (Farabegoli et al., 2018). GYM and SPX1, belonging to the cyclic imine group, can block nicotinic and muscarinic acetylcholine receptors in the nervous system and the neuromuscular junction, inducing acute toxicity (Marrouchi et al., 2013). The voltage-gated sodium channel (VGNC) is the recognized receptor of both STX and PbTXs, and the binding to VGNC probably results in disorders of ion homeostasis (Rossini and Hess, 2010). AZA is chemically characterized by a cyclic amine group, a carboxylic acid and a unique tri-spiro ring (Rossini and Hess, 2010). Although the mode of action of the AZAs has not been fully elucidated, AZAs are found to inhibit endocytosis (Sala et al., 2013) and to induce cytoskeleton disorganization (Twiner et al., 2005). Exposure of primary cultured neurons to AZA1 increases nuclear levels of phosphorylated (active) c-Jun-N-terminal kinase (JNK), and an inhibitor of JNK could prevent the cytotoxic effect of AZA1, suggesting that the mechanism of action of AZAs might be associated with JNK production (Vale et al., 2007). YTX is a polycyclic ether compound. Three major responses triggered by YTXs in cultured cells have been reported, i.e., a general alteration, an increase in intracellular Ca²⁺ concentration and a disruption of E-cadherin system (Rossini and Hess, 2010). It is recognized that PTXs can interact with F-actin, leading to alterations in the ultrastructure and functioning of cellular cytoskeleton (Terao et al., 1986; Spector et al., 1999).

As some phycotoxins with a similar mechanism of action might work synergetically and phycotoxins probably occur as mixtures in the real-world environment (Smayda, 1997; Höglander et al., 2004; Ferron et al., 2016a; Eckford-Soper and Daugbjerg, 2017; Alarcan et al., 2018), it is of importance to clarify the combined effects of two phycotoxins. In this study, additive effects were observed in OA+DTX1. As OA and DTX1 share a similar mode of action, the observed potential additive effects of OA and DTX1 in artemia are probably due to the “dose addition”. On the other hand, the combination of OA and PTX2 exhibited potential antagonistic effects. Similarly, a recent study in human intestinal Caco-2 cells shows that the combination of OA with PTX2 results in reduced toxicity (including, the ROS production, IL-8 release and γ-H2AX phosphorylation) at low concentrations (Alarcan et al., 2019). It is reported that OA can interact with regulatory nuclear receptors such as PXR (Fidler et al., 2012; Ferron et al., 2016b), which regulate the expression of some cytochrome P450 enzymes (Wang et al., 2012). PTX2 is believed to interact with the AhR and induce P450 1A protein in hepatic cells (Alarcan et al., 2017, 2019). Therefore, one possible explanation is that the mixture of OA and PTX2 might induce cytochrome P450 activity and efflux transporter expression, resulting in higher detoxification/excretion of toxins and thus decreased toxic effects (Alarcan et al., 2019).

In this study, the binary exposure to DTX1+STX, DTX1+YTX or DTX1+PTX2 dramatically elevated the mortality in artemia, compared to the individual exposure, suggesting that DTX1 can interact with STX, YTX and PTX2, and then induce greater effects than additive. The synergetic effects of two phycotoxins have been documented. For instance, the mixture of AZA1 and YTX shows synergism in human intestinal cell models (Caco-2 cells) and the human intestinal epithelial crypt-like (Ferron et al., 2016b). The combination of YTX and OA with a ratio of 1:26.5 exhibits synergistic effects in the human intestinal epithelial crypt-like cells (Ferron et al., 2016b). Our results further highlight the hazard potency of the mixtures of DTX1 and other phycotoxins (like STX, YTX and PTX2) with regard to the ecological risk. It is worth mentioning that this study was conducted under laboratorial conditions. In the real-world environment, the fluctuated temperature, solar radiation and bacterial communities might influence the degradation of phycotoxins (Alfonso et al., 2008; Donovan et al., 2008; Pan et al., 2020). Although lipophilic phycotoxins (including OA, DTX1, PTX2, YTX, hYTX, SPX1, GYM, AZA1, AZA2, AZA3, PbTx2 and PbTx3) have excellent stability and the half-life of the water soluble phycotoxin STXs is about 9 to 28 days in river water (Jones and Negri, 1997; Chen et al., 2018), the possibility of degradation cannot be excluded. In the future, field studies should be conducted to fully assess the ecological risk of phycotoxins.

In summary, this study demonstrates the individual toxicity of 14 phycotoxins in A. salina. On the basis of 48 h LC₅₀, the order of toxicity in artemia is AZA3 (with a LC₅₀ of 0.019 3 µg/mL)>AZA2 (0.022 6 µg/mL)>PTX2 (0.046 0 µg/mL) >DTX1 (0.081 8 µg/mL)>hYTX (0.085 9 µg/mL)>AZA1 (0.106 µg/mL)>SPX1 (0.118 µg/mL)>YTX (0.171 µg/mL)>GYM (0.191 µg/mL)>OA (0.372 µg/mL)>dcSTX (0.376 µg/mL)>STX (0.899 µg/mL)>PbTx3 (1.279 µg/mL)>PbTx2 (2.415 µg/mL). These data would contribute to a more accurate calculation of predicted no effect concentration (PNEC) in assessing the ecological risk of phycotoxins and HABs using species sensitivity distributions (SSDs). Furthermore, the combination of two phycotoxins exhibits potential additive (OA+DTX1; OA+DTX1), antagonistic (OA+PTX2; OA+STK) or synergetic (DTX1+STX; DTX1+YTX; DTX1+PTX2; PTX2+hYTX) effects with regard to the mortality of A. salina. The findings enrich our understanding on the ecological risk of phycotoxins and HABs in zooplankton and marine ecosystems, especially when two or more phycotoxins occur simultaneously.

Funding

Less

The National Natural Science Foundation of China under contract No. 41576120; the Special Fund Project for Marine and Fishery Protection and Development in Fujian Province, China under contract No. FZJZ-2021-1; the National Key R&D Program of China under contract No. 2017YFC1404803.

References

Less

Abdenadher M, Hamza A, Fekih W, et al. 2012. Factors determining the dynamics of toxic blooms of Alexandrium minutum during a 10-year study along the shallow southwestern Mediterranean coasts. Estuarine, Coastal and Shelf Science, 106: 102–111

Alarcan J, Barbé S, Kopp B, et al. 2019. Combined effects of okadaic acid and pectenotoxin-2, 13-desmethylspirolide C or yessotoxin in human intestinal Caco-2 cells. Chemosphere, 228: 139–148, doi: 10.1016/j.chemosphere.2019.04.018

Alarcan J, Biré R, Le Hégarat L, et al. 2018. Mixtures of lipophilic phycotoxins: exposure data and toxicological assessment. Marine Drugs, 16(2): 46, doi: 10.3390/md16020046

Alarcan J, Dubreil E, Huguet A, et al. 2017. Metabolism of the marine phycotoxin PTX-2 and its effects on hepatic xenobiotic metabolism: activation of nuclear receptors and modulation of the phase I cytochrome P450. Toxins, 9(7): 212, doi: 10.3390/toxins9070212

Alfonso C, Rehmann N, Hess P, et al. 2008. Evaluation of various pH and temperature conditions on the stability of azaspiracids and their importance in preparative isolation and toxicological studies. Analytical Chemistry, 80(24): 9672–9680, doi: 10.1021/ac801506d

Anderson D M, Alpermann T J, Cembella A D, et al. 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

Bravo I, Fernández M L, Ramilo I, et al. 2001. Toxin composition of the toxic dinoflagellate Prorocentrum lima isolated from different locations along the Galician Coast (NW Spain). Toxicon, 39(10): 1537–1545, doi: 10.1016/S0041-0101(01)00126-X

Chen Junhui, Han Tongzhu, Li Xiaotong, 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, doi: 10.1016/j.scitotenv.2017.08.304

De Rijcke M, Van Acker E, Nevejan N, et al. 2016. Toxic dinoflagellates and Vibrio spp. act independently in bivalve larvae. Fish & Shellfish Immunology, 57: 236–242

Dickey R W, Bobzin S C, Faulkner D J, et al. 1990. Identification of okadaic acid from a Caribbean dinoflagellate, Prorocentrum concavum. Toxicon, 28(4): 371–377, doi: 10.1016/0041-0101(90)90074-H

Donovan C J, Ku J C, Quilliam M A, et al. 2008. Bacterial degradation of paralytic shellfish toxins. Toxicon, 52(1): 91–100, doi: 10.1016/j.toxicon.2008.05.005

D’ors A, Bartolomé M C, Sánchez-Fortún S. 2014. Risk associated with toxic blooms of marine phytoplankton functional groups on Artemia franciscana. Journal of Coastal Life Medicine, 2(8): 625–631

Durbin E, Teegarden G, Campbell R, et al. 2002. North Atlantic right whales, Eubalaena glacialis, exposed to paralytic shellfish poisoning (PSP) toxins via a zooplankton vector, Calanus finmarchicus. Harmful Algae, 1(3): 243–251, doi: 10.1016/S1568-9883(02)00046-X

Eckford-Soper L K, Daugbjerg N. 2017. Interspecific competition study between Pseudochattonella farcimen and P. verruculosa (Dictyochophyceae)—Two ichthyotoxic species that co-occur in Scandinavian waters. Microbial Ecology, 73(2): 259–270, doi: 10.1007/s00248-016-0856-z

EFSA Panel on Contaminants in the Food Chain (CONTAM). 2010. Scientific Opinion on marine biotoxins in shellfish–Cyclic imines (spirolides, gymnodimines, pinnatoxins and pteriatoxins). EFSA Journal, 8(6): 1628

Faassen E J, Harkema L, Begeman L, et al. 2012. First report of (homo)anatoxin-a and dog neurotoxicosis after ingestion of benthic cyanobacteria in The Netherlands. Toxicon, 60(3): 378–384, doi: 10.1016/j.toxicon.2012.04.335

Farabegoli F, Blanco L, Rodríguez L P, et al. 2018. Phycotoxins in marine shellfish: origin, occurrence and effects on humans. Marine Drugs, 16(6): 188, doi: 10.3390/md16060188

Ferreiro S F, Vilariño N, Carrera C, et al. 2016. Subacute cardiovascular toxicity of the marine phycotoxin azaspiracid-1 in rats. Toxicological Sciences, 151(1): 104–114, doi: 10.1093/toxsci/kfw025

Ferron P J, Dumazeau K, Beaulieu J F, et al. 2016a. Combined effects of lipophilic phycotoxins (okadaic acid, azapsiracid-1 and yessotoxin) on human intestinal cells models. Toxins, 8(2): 50, doi: 10.3390/toxins8020050

Ferron P J, Hogeveen K, De Sousa G, et al. 2016b. Modulation of CYP3A4 activity alters the cytotoxicity of lipophilic phycotoxins in human hepatic HepaRG cells. Toxicology in Vitro, 33: 136–146, doi: 10.1016/j.tiv.2016.02.021

Fidler A E, Holland P T, Reschly E J, et al. 2012. Activation of a tunicate (Ciona intestinalis) xenobiotic receptor orthologue by both natural toxins and synthetic toxicants. Toxicon, 59(2): 365–372, doi: 10.1016/j.toxicon.2011.12.008

Figueroa D, Signore A, Araneda O, et al. 2020. Toxicity and differential oxidative stress effects on zebrafish larvae following exposure to toxins from the okadaic acid group. Journal of Toxicology and Environmental Health, Part A, 83(15–16): 573–588

Hallegraeff G M. 1993. A review of harmful algal blooms and their apparent global increase. Phycologia, 32(2): 79–99, doi: 10.2216/i0031-8884-32-2-79.1

Hisem D, Hrouzek P, Tomek P, et al. 2011. Cyanobacterial cytotoxicity versus toxicity to brine shrimp Artemia salina. Toxicon, 57(1): 76–83, doi: 10.1016/j.toxicon.2010.10.002

Höglander H, Larsson U, Hajdu S. 2004. Vertical distribution and settling of spring phytoplankton in the offshore NW Baltic Sea proper. Marine Ecology Progress Series, 283: 15–27, doi: 10.3354/meps283015

Jones G J, Negri A P. 1997. Persistence and degradation of cyanobacterial paralytic shellfish poisons (PSPs) in freshwaters. Water Research, 31(3): 525–533, doi: 10.1016/S0043-1354(96)00134-0

Jonsson P R, Pavia H, Toth G. 2009. Formation of harmful algal blooms cannot be explained by allelopathic interactions. Proceedings of the National Academy of Sciences of the United States of America, 106(27): 11177–11182, doi: 10.1073/pnas.0900964106

Kirkpatrick B, Fleming L E, Squicciarini D, et al. 2004. Literature review of Florida red tide: implications for human health effects. Harmful Algae, 3(2): 99–115, doi: 10.1016/j.hal.2003.08.005

Lincoln R A, Strupinski K, Walker J M. 1996. The use of Artemia nauplii (brine shrimp larvae) to detect toxic compounds from microalgal cultures. International Journal of Pharmacognosy, 34(5): 384–389, doi: 10.1076/phbi.34.5.384.13255

Marrouchi R, Rome G, Kharrat R, et al. 2013. Analysis of the action of gymnodimine-A and 13-desmethyl spirolide C on the mouse neuromuscular system in vivo. Toxicon, 75: 27–34, doi: 10.1016/j.toxicon.2013.08.050

Pan Lei, Chen Junhui, He Xiuping, et al. 2020. Aqueous photodegradation of okadaic acid and dinophysistoxin-1: persistence, kinetics, photoproducts, pathways, and toxicity evaluation. Science of the Total Environment, 743: 140593, doi: 10.1016/j.scitotenv.2020.140593

Poli M A. 1988. Laboratory procedures for detoxification of equipment and waste contaminated with brevetoxins PbTx-2 and PbTx-3. Journal of Association of Official Analytical Chemists, 71(5): 1000–1002

Quilliam M A. 1999. Phycotoxins. Journal of AOAC International, 82(2): 495

Rambla-Alegre M, Miles C O, de la Iglesia P, et al. 2018. Occurrence of cyclic imines in European commercial seafood and consumers risk assessment. Environmental Research, 161: 392–398, doi: 10.1016/j.envres.2017.11.028

Rossini G P, Hess P. 2010. Phycotoxins: chemistry, mechanisms of action and shellfish poisoning. In: Luch A, ed. Molecular, Clinical and Environmental Toxicology: Volume 2: Clinical Toxicology. Basel: Birkhä user, 65–122

Sala G L, Bellocci M, Callegari F, et al. 2013. Azaspiracid-1 inhibits the maturation of cathepsin D in mammalian cells. Chemical Research in Toxicology, 26(3): 444–455, doi: 10.1021/tx300511z

Shaw B A, Andersen R J, Harrison P J. 1997. Feeding deterrent and toxicity effects of apo-fucoxanthinoids and phycotoxins on a marine copepod (Tigriopus californicus). Marine Biology, 128(2): 273–280, doi: 10.1007/s002270050092

Simões E, Vieira R C, Schramm M A, et al. 2015. Impact of harmful algal blooms (Dinophysis acuminata) on the immune system of oysters and mussels from Santa Catarina, Brazil. Journal of the Marine Biological Association of the United Kingdom, 95(4): 773–781, doi: 10.1017/S0025315414001702

Smayda T J. 1997. What is a bloom? A commentary. Limnology and Oceanography, 42(5part2): 1132–1136, doi: 10.4319/lo.1997.42.5_part_2.1132

Spector I, Braet F, Shochet N R, et al. 1999. New anti-actin drugs in the study of the organization and function of the actin cytoskeleton. Microscopy Research and Technique, 47(1): 18–37, doi: 10.1002/(SICI)1097-0029(19991001)47:1<18::AID-JEMT3>3.0.CO;2-E

Suganuma M, Fujiki H, Suguri H, et al. 1988. Okadaic acid: an additional non-phorbol-12-tetradecanoate-13-acetate-type tumor promoter. Proceedings of the National Academy of Sciences of the United States of America, 85(6): 1768–1771, doi: 10.1073/pnas.85.6.1768

Terao K, Ito E, Yanagi T, et al. 1986. Histopathological studies on experimental marine toxin poisoning. I. Ultrastructural changes in the small intestine and liver of suckling mice induced by dinophysistoxin-1 and pectenotoxin-1. Toxicon, 24(11–12): 1141–1151

Toyofuku H. 2006. Joint FAO/WHO/IOC activities to provide scientific advice on marine biotoxins (research report). Marine Pollution Bulletin, 52(12): 1735–1745, doi: 10.1016/j.marpolbul.2006.07.007

Turki S, Dhib A, Fertouna-Bellakhal M, et al. 2014. Harmful algal blooms (HABs) associated with phycotoxins in shellfish: what can be learned from five years of monitoring in Bizerte Lagoon (southern Mediterranean Sea)?. Ecological Engineering, 67: 39–47

Turner J T. 2014. Planktonic marine copepods and harmful algae. Harmful Algae, 32: 81–93, doi: 10.1016/j.hal.2013.12.001

Twiner M J, Hess P, Dechraoui M Y B, et al. 2005. Cytotoxic and cytoskeletal effects of azaspiracid-1 on mammalian cell lines. Toxicon, 45(7): 891–900, doi: 10.1016/j.toxicon.2005.02.015

Twiner M J, Rehmann N, Hess P, et al. 2008. Azaspiracid shellfish poisoning: a review on the chemistry, ecology, and toxicology with an emphasis on human health impacts. Marine Drugs, 6(2): 39–72, doi: 10.3390/md6020039

Vale C, Gómez-Limia B, Nicolaou K C, et al. 2007. The c-Jun-N-terminal kinase is involved in the neurotoxic effect of azaspiracid-1. Cellular Physiology and Biochemistry, 20(6): 957–966, doi: 10.1159/000110456

Wang Yueming, Ong S S, Chai S C, et al. 2012. Role of CAR and PXR in xenobiotic sensing and metabolism. Expert Opinion on Drug Metabolism & Toxicology, 8(7): 803–817

Xiao Xi, Agustí S, Pan Yaoru, et al. 2019. Warming amplifies the frequency of harmful algal blooms with eutrophication in Chinese coastal waters. Environmental Science & Technology, 53(22): 13031–13041

Xu Jiayi, Hansen P J, Nielsen L T, et al. 2017. Distinctly different behavioral responses of a copepod, Temora longicornis, to different strains of toxic dinoflagellates, Alexandrium spp. Harmful Algae, 62: 1–9, doi: 10.1016/j.hal.2016.11.020

Yasumoto T. 1990. Marine microorganisms toxins—an overview. In: Granéli E, Sundström B, Edler L, et al., eds. Toxic Marine Phytoplankton. New York: Elsevier, 3–8

Zhang Xue, Hu Hongying, Men Yujie, et al. 2009. Feeding characteristics of a golden alga (Poterioochromonas sp. ) grazing on toxic cyanobacterium Microcystis aeruginosa. Water Research, 43(12): 2953–2960, doi: 10.1016/j.watres.2009.04.003

Appendix

Less

Year 2023 volume 42 Issue 2

PDF

Cite this Article

BibTeX

Article Info

doi: 10.1007/s13131-022-2120-3

Receive Date：2022-01-26
Online Date：2025-11-21
Published：2023-02-25

Article Data

Affiliations

History

Received：2022-01-26
Accepted：2022-09-19

Funding

The National Natural Science Foundation of China under contract No. 41576120; the Special Fund Project for Marine and Fishery Protection and Development in Fujian Province, China under contract No. FZJZ-2021-1; the National Key R&D Program of China under contract No. 2017YFC1404803.

Affiliations

¹ Institute of Oceanography, College of Geography and Oceanography, Minjiang University, Fuzhou 350108, China

² Fuzhou Institute of Oceanography, Fuzhou 350108, China

³ Department of Marine Chemistry, National Marine Environmental Monitoring Center, Dalian 116023, China

⁴ Fujian Marine Environment and Fishery Resource Monitoring Center, Fuzhou 350003, China

Corresponding:

* E-mail: ryliu@nmemc.org.cn; jlmu@mju.edu.cn

jlmu@mju.edu.cn

References

Share

https://castjournals.cast.org.cn/joweb/aos/EN/10.1007/s13131-022-2120-3

Share to

Scan QR to access full text

Cite this article

BibTeX

Citations

表12种不同金属材料的力学参数

科 Family	属数 Number of genus	种数 Number of species	占总种数比例 Percentage of total species (%)	属 Genus	种数 Number of species	占总种数比例 Percentage of total species (%)
鹅膏菌科Amanitaceae	2	11	5.26	鹅膏菌属 Amanita	10	4.78
小菇科 Mycenaceae	2	12	5.74	丝盖伞属 Inocybe	5	2.39
多孔菌科 Polyporaceae	8	14	6.70	蜡蘑属 Laccaria	5	2.39
红菇科 Russulaceae	3	23	11.00	小皮伞属 Marasmius	6	2.87
				小菇属 Mycena	11	5.26
				光柄菇属 Pluteus	5	2.39
				红菇属 Russula	17	8.13
				栓菌属 Trametes	5	2.39

关闭全屏

BibTeX
EndNote
RefWorks
TxT

Table 1. The 48 h LC₅₀ and LC₁₀ values of marine phycotoxins in Artemia salina (n=3)

Phycotoxins	LC₅₀/(µg·mL⁻¹)	LC₁₀/(µg·mL⁻¹)
OA	0.372 [0.287–0.746]	0.124 [0.074 8–0.153]
DTX1	0.081 8 [0.046 0–0.139]	0.029 9 [0.003 27–0.050 7]
PTX2	0.046 0 [0.035 2–0.057 3]	0.021 2 [0.009 57–0.029 4]
YTX	0.171 [0.097 5–0.208]	0.061 2 [0.039 7–0.133]
hYTX	0.085 9 [0.068 9–0.237]	0.048 0 [0.035 9–0.054 8]
GYM	0.191 [0.102–1.667]	0.054 5 [0.042 7–0.102]
SPX1	0.118 [0.091 0–0.345]	0.069 2 [0.061 7–0.087 9]
AZA1	0.106 [0.032 4–10^5.44]	0.021 9 [0.013 2–5.701]
AZA2	0.022 6 [0.017 2–0.038 5]	0.008 89 [0.007 53–0.010 5]
AZA3	0.019 3 [0.014 5–0.036 8]	0.008 55 [0.007 24–0.010 3]
STX	0.899 [0.469–16.520]	0.288 [0.222–0.716]
dcSTX	0.376 [0.281–0.962]	0.194 [0.171–0.242]
PbTx2	2.415 [2.056–3.499]	0.893 [0.423–1.161]
PbTx3	1.279 [1.208–1.355]	0.811 [0.719–0.887]

Note: The 95% confidence interval are given in brackets.

Table 2. List of the recent toxicological data about the toxicity of phycotoxins in aquatic organisms

Phycotoxin	Species	Time	LC₅₀/(µg·mL⁻¹)	Reference
OA	Tigriopus californicus	24 h	41.7	Shaw et al. (1997)
	Artemia franciscana	24 h	6 270*	D’ors et al. (2014)
	Danio rerio larvae	24 h	10	Figueroa et al. (2020)
	Danio rerio larvae	48 h	8.5	Figueroa et al. (2020)
	Danio rerio larvae	72 h	7	Figueroa et al. (2020)
	Daphnia magna	48 h	42.1	Rambla-Alegre et al. (2018)
	Daphnia magna	96 h	0.003	Rambla-Alegre et al. (2018)
	Artemia salina	48 h	0.728	this study
DTX1	Danio rerio larvae	24 h	7	Figueroa et al. (2020)
	Danio rerio larvae	48 h	5.5	Figueroa et al. (2020)
	Danio rerio larvae	72 h	5	Figueroa et al. (2020)
	Daphnia magna	48 h	29	Rambla-Alegre et al. (2018)
	Daphnia magna	96 h	0.008	Rambla-Alegre et al. (2018)
	Artemia salina	48 h	0.081 9	this study
STX	Artemia franciscana	24 h	4 060*	D’ors et al. (2014)
	Artemia salina	48 h	1.042 32	this study
PbTx	Bambusia affinis	24 h	0.000 011	Kirkpatrick et al. (2004)
	Oryzias latipes	24 h	0.015–25	Poli (1988)
PbTx2	Artemia salina	48 h	2.415	this study
PbTx3	Artemia salina	48 h	1.239	this study

Note: * represents the calculated equivalent.

Fig. 1. The 48 h mortality-concentration curves of OA (a), DTX1 (b), PTX2 (c), YTX (d), hYTX (e), SPX1 (f), GYM (g), AZA1 (h), AZA2 (i), AZA3 (j), STX (k), dcSTX (l), PbTx2 (m) and PbTx3 (n) in Artemia salina, where Y−axis is mortality and X−axis is the log₁₀ concentration (unit: ng/mL) of phycotoxins (lg C). The insets are plots of probit transformed responses, where the Y−axis is probit and the X−axis is lg C.

Fig. 2. The individual and combined effects of OA+DTX1 (A), OA+PTX2 (B), OA+STX (C), DTX1+PTX2 (D), DTX1+STX (E), DTX1+YTX (F), DTX1+hYTX (G), PTX2+SPX1 (H) and PTX2+hYTX (I) on the 48 h mortality of Artemia salina. Data were expressed as the mean±SEM (n>3). Bars marked with different letters are significantly different from each other (p<0.05).

Articles: Latest Articles; Most Read; Collections

Updates: Events; News; Multimedia

About: About Us

Contact

No. 86 Xueyuan South Road, Haidian District, Beijing

100081

010-62199257

qkjq@cast.org.cn

Copyright © 2025 China Association for Science and Technology. All rights reserved. For all open access content, the relevant licensing terms apply.
Sponsored by the Office of the Leading Group for Cybersecurity and Informatization of CAST, and supported by Science and Technology Review Publishing House