The toxic dinoflagellate Alexandrium minutum affects oyster gamete health and fertilization potential

Abstract

Dinoflagellates from the globally distributed genus Alexandrium are known to produce both paralytic shellfish toxins (PST) and uncharacterized bioactive extracellular compounds (BEC) with allelopathic, ichthyotoxic, hemolytic and cytotoxic activities. In France, blooms of Alexandrium minutum appear generally during the spawning period of most bivalves. These blooms could therefore alter gametes and/or larval development of bivalves, causing severe issues for ecologically and economically important species, such as the Pacific oyster Crassostrea (=Magallana) gigas. The aim of this work was to test the effects of three strains of A. minutum producing either only PST, only BEC, or both PST and BEC upon oyster gametes, and potential consequences on fertilization success. Oocytes and spermatozoa were exposed in vitro for 2 hours to a range of environmentally realistic A. minutum concentrations (10 to 2.5 × 104 cells mL-1). Following exposure, gamete viability and reactive oxygen species (ROS) production were assessed by flow cytometry, spermatozoa motility and fertilization capacities of both spermatozoa and oocytes were analysed by microscopy. Viability and fertilization capacity of spermatozoa and oocytes were drastically reduced following exposure to 2.5 × 104 cells mL-1 of A. minutum. The BEC-producing strain was the most potent strain decreasing spermatozoa motility, increasing ROS production of oocytes, and decreasing fertilization, from the concentration of 2.5 × 103 cells mL-1. This study highlights the significant cellular toxicity of the BEC produced by A. minutum on oyster gametes. Physical contact between gametes and motile thecate A. minutum cells may also contribute to alter oyster gamete integrity. These results suggest that oyster gametes exposure to A. minutum blooms could affect oyster fertility and reproduction success. Highlights► Oyster spermatozoa and oocytes were exposed in vitro to Alexandrium minutum strains. ► Viability and fertilization capacity of gametes were drastically reduced. ► The toxicity of Alexandrium minutum upon oyster gametes is strain-specific. ► A non-PST-producing strain increased reactive oxygen species production in oocytes. ► This strain also decreased spermatozoa motility and gamete fertilization.Please note that this is an author-produced PDF of an article accepted for publication following peer review. The definitive publisher-authenticated version is available on the publisher Web site.

Effects of Harmful Algal Blooms on Fish and Shellfish Species: A Case Study of New Zealand in a Changing Environment

“…Recent studies have provided a better understanding of the toxicity of A. minutum to bivalves [ 66 , 75 ], with BECs found to be responsible for the negative effects on the gills of adult C. gigas , whereas PSTs impact the digestive gland [ 66 ]. Direct exposure of the early life stages of C. gigas also negatively affected gamete quality, fertilization success, and subsequent larval development [ 16 , 17 , 67 , 74 ], with negative effects attributed primarily to BECs rather than PSTs.…”

“…The direct effects of HABs on cultured fish and shellfish species can be substantial and are likely to become more significant considering increasing climate anomalies and as the farmed supply of seafood grows [ 15 ]. The early life stages of cultured species are particularly susceptible to harmful algae and their associated toxic compounds [ 12 , 16 , 17 , 18 , 19 , 20 , 21 , 22 , 23 ]. Most farmed species are confined and cannot escape blooms.…”

Unknown Extracellular and Bioactive Metabolites of the Genus Alexandrium: A Review of Overlooked Toxins

“…In the plankton realm, BECs may negatively affect competing protists [58][59][60], immobilise prey [61,62] and predators [4,63], inhibit putative parasites [64], or affect grazing of copepods [65]. Moreover, there is growing evidence that BECs might also be responsible for physiological incapacitation of shellfish [66][67][68][69][70][71][72] or fish [73]. Nevertheless, detailed knowledge on chemical details of the metabolites mediating these interactions is largely lacking.…”

“…A number of recent studies used a comparative approach with strains that were thoroughly characterised with respect to different bioactive compounds, enabling the distinction between effects from PSTs or BECs (Figure 2). In particular, some of these new studies [66][67][68][70][71][72] exposed bivalve species (M. gigas, Mytilus edulis, Pecten maximus) to different strains of Alexandrium spp., for which PST production and BECs potency (measured as allelochemical or hemolytic potencies) were characterised. These studies clearly highlight that a majority of the deleterious effects observed on bivalves might indeed be due to BECs produced by Alexandrium spp.…”