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

•Paralytic shellfish toxins (PSTs) and bioactive extracellular compounds (BECs) of Alexandrium minutum have contrasted effects upon Crassostrea gigas oysters.•BECs affect nutrition and valve-activity behavior.•BECs induce hemocyte mobilization in gills.•PSTs disrupt biological rhythm.•PSTs provoke i...

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Published inAquatic toxicology Vol. 199; pp. 188 - 198
Main Authors Castrec, J., Soudant, P., Payton, L., Tran, D., Miner, P., Lambert, C., Le Goïc, N., Huvet, A., Quillien, V., Boullot, F., Amzil, Z., Hégaret, H., Fabioux, C.
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LanguageEnglish
Published Netherlands Elsevier B.V 01.06.2018
Elsevier
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Abstract •Paralytic shellfish toxins (PSTs) and bioactive extracellular compounds (BECs) of Alexandrium minutum have contrasted effects upon Crassostrea gigas oysters.•BECs affect nutrition and valve-activity behavior.•BECs induce hemocyte mobilization in gills.•PSTs disrupt biological rhythm.•PSTs provoke inflammation in the digestive gland. 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.
AbstractList •Paralytic shellfish toxins (PSTs) and bioactive extracellular compounds (BECs) of Alexandrium minutum have contrasted effects upon Crassostrea gigas oysters.•BECs affect nutrition and valve-activity behavior.•BECs induce hemocyte mobilization in gills.•PSTs disrupt biological rhythm.•PSTs provoke inflammation in the digestive gland. 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.
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.
Author Huvet, A.
Miner, P.
Le Goïc, N.
Soudant, P.
Payton, L.
Amzil, Z.
Castrec, J.
Tran, D.
Lambert, C.
Quillien, V.
Hégaret, H.
Fabioux, C.
Boullot, F.
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Keywords Harmful algal bloom (HAB)
Histology
Behavior
Paralytic shellfish toxins (PST)
Crassostrea gigas
Bioactive extracellular compounds (BEC)
ACL
Language English
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Snippet •Paralytic shellfish toxins (PSTs) and bioactive extracellular compounds (BECs) of Alexandrium minutum have contrasted effects upon Crassostrea gigas...
Blooms of the dinoflagellate Alexandrium spp., known as producers of paralytic shellfish toxins (PSTs), are regularly detected on the French coastline. PSTs...
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StartPage 188
SubjectTerms Behavior
Bioactive extracellular compounds (BEC)
Crassostrea gigas
Earth Sciences
Harmful algal bloom (HAB)
Histology
Life Sciences
Oceanography
Paralytic shellfish toxins (PST)
Sciences of the Universe
Toxicology
Title Bioactive extracellular compounds produced by the dinoflagellate Alexandrium minutum are highly detrimental for oysters
URI https://dx.doi.org/10.1016/j.aquatox.2018.03.034
https://www.ncbi.nlm.nih.gov/pubmed/29653309
https://hal.science/hal-02324608
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