The toxic dinoflagellate Alexandrium minutum impairs the performance of oyster embryos and larvae

Castrec, Justine; Hégaret, Hélène; Huber, Matthias; Grand, Jacqueline Le; Huvet, Arnaud; Tallec, Kévin; Boulais, Myrina; Soudant, Philippe; Fabioux, Caroline

doi:10.1016/j.hal.2020.101744

Cited by 16 publications

(18 citation statements)

References 71 publications

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“…Effects of HABs upon bivalve reproduction and on physiology through parental exposure were reported recently (e.g. Basti et al, 2013;Castrec et al, 2019Castrec et al, , 2020Rolton et al, 2015), and could ultimately alter bivalve population fitness in the case of repeated blooms. Adaptations of bivalve populations to recurrent toxic blooms, reflected by differential physiological responses between populations (Navarro et al, 2014), can lead to the emergence of resistant genotypes (Bricelj et al, 2010(Bricelj et al, , 2005.…”

Section: Discussion and Future Research Recommendationsmentioning

confidence: 87%

“…extracellular compounds toward different cells, such as microalgae, protists, or bivalve gametes (Arzul et al, 1999;Castrec et al, 2019;Flores et al, 2012;Le Goïc et al, 2014Lelong et al, 2011;Long et al, 2018b;Tillmann and John, 2002). Although PST can be released extracellularly (Lefebvre et al, 2008;Persson et al, 2012), many studies reported the bioactivity of extracellular compounds produced by non-PST Alexandrium strains, demonstrating that these effects are independent from PSTs (Bianchi et al, 2019;Borcier et al, 2017;Castrec et al, 2019Castrec et al, , 2020Ford et al, 2008;Long et al, 2018b;Tillmann et al, 2007;Tillmann and John, 2002). Only a few studies focused on the characterization of these compounds, and their precise nature remains unknown (Flores et al, 2012;Ma et al, 2011Ma et al, , 2009).…”

Section: Effects Of Algal Toxins and Extracellular Compounds To Bivalmentioning

confidence: 99%

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Effects of marine harmful algal blooms on bivalve cellular immunity and infectious diseases: A review

Lassudrie

Hégaret

Wikfors

et al. 2020

Developmental & Comparative Immunology

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Bivalves were long thought to be "symptomless carriers" of marine microalgal toxins to human seafood consumers. In the past three decades, science has come to recognize that harmful algae and their toxins can be harmful to grazers, including bivalves. Indeed, studies have shown conclusively that some microalgal toxins function as active grazing deterrents. When responding to marine Harmful Algal Bloom (HAB) events, bivalves can reject toxic cells to minimize toxin and bioactive extracellular compound (BEC) exposure, or ingest and digest cells, incorporating nutritional components and toxins. Several studies have reported modulation of bivalve hemocyte variables in response to HAB exposure. Hemocytes are specialized cells involved in many functions in bivalves, particularly in immunological defense mechanisms. Hemocytes protect tissues by engulfing or encapsulating living pathogens and repair tissue damage caused by injury, poisoning, and infections through inflammatory processes. The effects of HAB exposure observed on bivalve cellular immune variables have raised the question of possible effects on susceptibility to infectious disease. As science has described a previously unrecognized diversity in microalgal bioactive substances, and also found a growing list of infectious diseases in bivalves, episodic reports of interactions between harmful algae and disease in bivalves have been published. Only recently, studies directed to understand the physiological and metabolic bases of these interactions have been undertaken. This review compiles evidence from studies of harmful algal Highlights  Review of the main studies on effects of marine harmful algae on bivalve immune cells (hemocytes) and on infectious disease  Harmful algae can modulate host-pathogen interactions in bivalves on various way (increase or decrease the infection)  Some experimental studies report the involvement of cellular immunity and global physiological weakness in the modulations  Other mechanisms possibly involved: HAB effects on bivalve filtration; direct

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Section: Discussion and Future Research Recommendationsmentioning

confidence: 87%

Section: Effects Of Algal Toxins and Extracellular Compounds To Bivalmentioning

confidence: 99%

Effects of marine harmful algal blooms on bivalve cellular immunity and infectious diseases: A review

Lassudrie

Hégaret

Wikfors

et al. 2020

Developmental & Comparative Immunology

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“…have not been reported yet but could potentially explain the observed effect on gametes and fertilization success. for A. minutum affecting early life stages and adults of C. gigas has also been observed (Castrec et al, 2020(Castrec et al, , 2018. Bioguided-fractionation approaches combining suitable bioassays (Long et al, 2018) as well as chromatography coupled to e.g.…”

Section: Cyclic Ester) Pectenotoxin 2 Biological Activity On Cytoskeletal Dynamics Is Clearly Associatedmentioning

confidence: 99%

“…Some preliminary results also indicate that when gametes were exposed to D. sacculus, abnormal development of D-shaped larvae could be observed (personal communications), leading to the question of the effects on early life stages of C. gigas and ultimately, recruitment. Similarly, when C. gigas larvae were exposed to A. minutum, anomalies in swimming behavior, feeding and growth were observed which led to a decrease in survival and settlement of older larvae stages (Castrec et al, 2020).…”

Section: Cyclic Ester) Pectenotoxin 2 Biological Activity On Cytoskeletal Dynamics Is Clearly Associatedmentioning

confidence: 99%

Cultures of Dinophysis sacculus, D. acuminata and pectenotoxin 2 affect gametes and fertilization success of the Pacific oyster, Crassostrea gigas

Gaillard

Goïc

Malo

et al. 2020

Environmental Pollution

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Dinophysis sacculus and D. acuminata increased mortality of Crassostrea gigas oocytes Exposure of oocytes and spermatozoa to 0.5 cells mL -1 of D. sacculus decreased subsequent fertilization success Oyster gametes were negatively affected by exposure to whole culture or resuspended cells of Dinophysis spp. 5 nM of PTX2 decreased fertilization success of oocytes and 500 nM of PTX2 increased ROS production; OA showed no effect

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“…In particular, contaminants could negatively affect their reproduction as demonstrated in oysters exposed to anthropogenic pollutants (Akcha et al, 2012;Fitzpatrick et al, 2008;Mai et al, 2013;Vignier et al, 2017Vignier et al, , 2015. Experimental studies suggest that harmful algal blooms (HAB), often caused by dinoflagellates, can affect marine bivalve reproduction by altering gamete quality and larval development, growth, and survival (Banno et al, 2018;Basti et al, 2013Basti et al, , 2011Binzer et al, 2018;Bricelj and MacQuarrie, 2007;Castrec et al, 2020Castrec et al, , 2019De Rijcke et al, 2015;Gaillard et al, 2020;Rolton et al, 2018Rolton et al, , 2015Rolton et al, , 2014Tang and Gobler, 2012). In coastal areas, HAB are a recurring phenomenon that can co-occur with the reproduction of free spawning marine organisms (Gaillard et al, 2020).…”

Section: Introductionmentioning

confidence: 99%

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

Castrec

Fabioux

Goïc

et al. 2021

Marine Environmental Research

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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.

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The toxic dinoflagellate Alexandrium minutum impairs the performance of oyster embryos and larvae

Cited by 16 publications

References 71 publications

Effects of marine harmful algal blooms on bivalve cellular immunity and infectious diseases: A review

Effects of marine harmful algal blooms on bivalve cellular immunity and infectious diseases: A review

Cultures of Dinophysis sacculus, D. acuminata and pectenotoxin 2 affect gametes and fertilization success of the Pacific oyster, Crassostrea gigas

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

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