Uptake kinetics and biotransformation of paralytic shellfish poisoning toxins in perna viridis

Abstract

Increasing reports of algal blooms or “red tides” around the world in the past decades have raised public concern towards this issue, particularly in regard to harmful algal blooms (HABs). HABs are usually caused by a small group of marine dinoflagellates that produce non-protein potent neurotoxins. These HABs appear to be increasing worldwide both in frequency and in geographic area and have caused major adverse impacts to mariculture industries. Although Hong Kong has frequently been affected by HABs, there is no detailed information on the toxin accumulation in local mussels. The consumption of toxin-laden mussels can pose a significant risk to public health. Since most bivalves can accumulate algal toxins in their tissues with no apparent effect on their feeding activity, Perna viridis (green-lipped mussel) was used to study the uptake kinetics and biotransformation of paralytic shellfish poisoning (PSP) toxins by feeding the mussels with a PSP-producing dinoflagellate, Alexandrium tamarense (ATCI01), at a density of 104 cells/ml to mimic bloom conditions. Temporal changes in the toxin contents and the toxin profiles of five tissue compartments (hepatopancreas, gills, foot, adductor muscle and viscera) were monitored during the dosing and depuration phases by high-performance liquid chromatography (HPLC). The toxin profiles of the tissue compartments were compared with those of A. tamarense to understand the mechanism of toxin uptake in the mussels. The dominant toxin in A. tamarense was N-sulfocarbamoyl toxin (C2), which comprised 99% of total toxins with only a trace amount of carbamate toxin (GTX3). C2 toxin was the dominant toxin found in all analyzed tissue compartments in the mussel. The highest toxicity was observed in the hepatopancreas, which was consistent with similar studies reported in the literature. This study also attempts to model the transfer kinetics of C2 toxin between different compartments during detoxification. The uptake rate constant was highest for the viscera, and was slightly lower for the hepatopancreas. The percentage distribution of various toxins in individual tissues varied with detoxification duration. The probable mechanism of removal of toxins in mussels is by transferring toxins accumulated in viscera to hepatopancreas for toxin elimination. During the toxification experiment, apart from C2 toxin, low levels of other PSP toxins, which were not produced by A. tamarense, were also detected in the mussel. Specifically, P. viridis was able to transform C2 into carbamate toxins (GTX1/4, GTX2, NEO, STX) and decarbamoyl toxins (dcGTX2/3). In addition to the ability to accumulate toxins, P. viridis is capable of converting C2 toxin into other PSP toxins, although it was generally assumed by most scientists that mussels do not have such abilities. In conclusion, P. viridis is not only able to accumulate high levels of C2 toxin in various tissues, but is also capable of transforming C2 toxins to more potent carbamate and decarbamate toxins, which may greatly increase the toxicity of the mussels.