Bioactive extracellular compounds produced by the dinoflagellate Alexandrium minutum are highly detrimental for oysters

Type Article
Date 2018-06
Language English
Author(s) Castrec Justine1, Soudant P.1, Payton L.2, Tran D.2, Miner Philippe3, Lambert C.1, Le Goic N.1, Huvet ArnaudORCID3, Quillien Virgile3, Boullot F.1, Amzil ZouherORCID4, Hegaret HeleneORCID2, Fabioux C.1
Affiliation(s) 1 : IUEM, LEMAR UMR CNRS UBO IRD Ifremer 6539, Rue Dumont Urville, F-29280 Plouzane, France.
2 : CNRS, EPOC, UMR 5805, F-33120 Arcachon, France.
3 : Ifremer, LEMAR UMR CNRS UBO IRD Ifremer 6539, Ctr Bretagne, CS 10070, F-29280 Plouzane, France.
4 : Ifremer, Lab Phycotoxines, BP 21105, F-44311 Nantes, France.
Source Aquatic Toxicology (0166-445X) (Elsevier Science Bv), 2018-06 , Vol. 199 , P. 188-198
DOI 10.1016/j.aquatox.2018.03.034
WOS© Times Cited 36
Keyword(s) Harmful algal bloom (HAB), Crassostrea gigas, Paralytic shellfish toxins (PST), Bioactive extracellular compounds (BEC), Histology, Behavior
Abstract

Blooms of the dinoflagellate Alexandrium spp., known as producers of paralytic shellfish toxins (PSTs), are regularly detected on the French coastline. PSTs accumulate into harvested shellfish species, such as the Pacific oyster Crassostrea gigas, and can cause strong disorders to consumers at high doses. The impacts of Alexandrium minutum on C. gigas have often been attributed to its production of PSTs without testing separately the effects of the bioactive extracellular compounds (BECs) with allelopathic, hemolytic, cytotoxic or ichthyotoxic properties, which can also be produced by these algae. The BECs, still uncharacterized, are excreted within the environment thereby impacting not only phytoplankton, zooplankton but also marine invertebrates and fishes, without implicating any PST. The aim of this work was to compare the effects of three strains of A. minutum producing either only PSTs, only BECs, or both PSTs and BECs, on the oyster C. gigas. Behavioral and physiological responses of oysters exposed during 4 days were monitored and showed contrasted behavioral and physiological responses in oysters supposedly depending on produced bioactive substances. The non-PST extracellular-compound-producing strain primarily strongly modified valve-activity behavior of C. gigas and induced hemocyte mobilization within the gills, whereas the PST-producing strain caused inflammatory responses within the digestive gland and disrupted the daily biological rhythm of valve activity behavior. BECs may therefore have a significant harmful effect on the gills, which is one of the first organ in contact with the extracellular substances released in the water by A. minutum. Conversely, the PSTs impact the digestive gland, where they are released and mainly accumulated, after degradation of algal cells during digestion process of bivalves. This study provides a better understanding of the toxicity of A. minutum on oyster and highlights the significant role of BECs in this toxicity calling for further chemical characterization of these substances.

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Castrec Justine, Soudant P., Payton L., Tran D., Miner Philippe, Lambert C., Le Goic N., Huvet Arnaud, Quillien Virgile, Boullot F., Amzil Zouher, Hegaret Helene, Fabioux C. (2018). Bioactive extracellular compounds produced by the dinoflagellate Alexandrium minutum are highly detrimental for oysters. Aquatic Toxicology, 199, 188-198. Publisher's official version : https://doi.org/10.1016/j.aquatox.2018.03.034 , Open Access version : https://archimer.ifremer.fr/doc/00435/54637/