Sublethal exposure of eastern oyster Crassostrea virginicato the goniodomin‐producing dinoflagellate Alexandrium monilatum: Fate of toxins, histopathology, and gene expression

The dinoflagellate Alexandrium monilatumforms blooms during summer in tributaries of the lower Chesapeake Bay. Questions persist about the potential for A. monilatumto negatively affect aquatic organisms. Its main toxin, goniodomin A (GDA), a polyketide macrolide, has been shown to have adverse effects on animals, for example through cytotoxicity and interaction with actin. Eastern oysters Crassostrea virginicawere exposed for 96 h to sublethal concentrations of A. monilatum(615 ± 47 cells/mL [average ± SD]; containing mainly intracellular GDA [215 ± 7.15 pg/cell] and to a lesser extent goniodomin B, goniodomin C, and GDA seco‐acid as quantified by liquid chromatography coupled to tandem mass spectrometry) or to nontoxic phytoplankton or were unexposed. They were subsequently depurated for 96 h by exposure to nontoxic phytoplankton. Clearance rates were estimated, and oysters were sampled daily and tissue (gill, digestive gland, and remaining tissues) excised for analyses by histopathology, gene expression quantified by quantitative PCR, and goniodomin quantification. A positive clearance rate, no mortality, and no tissue pathologies were observed in oysters exposed to A. monilatum. Goniodomin A was detected in gill 6 h after exposure (504 ± 329 μg/kg [average ± SE]) and to a lesser extent in the digestive gland and remaining soft tissues. In the digestive gland, a trend of transformation of GDA to GDA seco‐acid was observed. The majority of toxins (≥83%) were depurated after 96 h. Expression of genes involved in oxidative response increased 14‐fold after 6 h, and those involved in actin synthesis showed a 27‐fold change after 24 h, while expression of apoptosis genes increased 6.9‐fold after 96 h compared with the control (eastern oysters exposed to nontoxic phytoplankton). Exposure experiments (nonsublethal or chronic) should be carried out to better assess the threat of this species and toxins for eastern oysters and other marine organisms. Impact statementThis study highlighted accumulation and depuration of goniodomins (polyketide macrolides) in tissues of eastern oysters exposed to the dinoflagellate Alexandrium monilatumwithout mortality or pathological changes. This sublethal exposure increased the expression of genes involved in apoptosis, oxidative stress responses, and cellular structure. This work revealed that A. monilatumand its toxins could be a potential emerging threat for eastern oyster, especially as the number of goniodomin‐producing species is increasing worldwide. This study highlighted accumulation and depuration of goniodomins (polyketide macrolides) in tissues of eastern oysters exposed to the dinoflagellate Alexandrium monilatumwithout mortality or pathological changes. This sublethal exposure increased the expression of genes involved in apoptosis, oxidative stress responses, and cellular structure. This work revealed that A. monilatumand its toxins could be a potential emerging threat for eastern oyster, especially as the number of goniodomin‐producing species is increasing worldwide.