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  1. Article ; Online: Corrigendum to "Mixotrophic lifestyle of the ichthyotoxic haptophyte, Prymnesium parvum, offered different sources of phosphorus": HARMFUL ALGAE 127 (2023), Article [HARALG_102483].

    Boucher, Clémence / Lacour, Thomas / André, Julie / Réveillon, Damien / Hansen, Per Juel / Mairet, Francis

    Harmful algae

    2023  Volume 128, Page(s) 102493

    Language English
    Publishing date 2023-08-31
    Publishing country Netherlands
    Document type Published Erratum
    ZDB-ID 2091119-1
    ISSN 1878-1470 ; 1568-9883
    ISSN (online) 1878-1470
    ISSN 1568-9883
    DOI 10.1016/j.hal.2023.102493
    Database MEDical Literature Analysis and Retrieval System OnLINE

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  2. Article ; Online: Toxic responses of metabolites produced by Ostreopsis cf. ovata on a panel of cell types.

    Lanceleur, Rachelle / Gémin, Marin-Pierre / Blier, Anne-Louise / Meslier, Lisa / Réveillon, Damien / Amzil, Zouher / Ternon, Eva / Thomas, Olivier P / Fessard, Valérie

    Toxicon : official journal of the International Society on Toxinology

    2024  Volume 240, Page(s) 107631

    Abstract: Blooms of the dinoflagellate Ostreopsis cf. ovata are regularly associated with human intoxications that are attributed to ovatoxins (OVTXs), the main toxic compounds produced by this organism and close analogs to palytoxin (PlTX). Unlike for PlTX, ... ...

    Abstract Blooms of the dinoflagellate Ostreopsis cf. ovata are regularly associated with human intoxications that are attributed to ovatoxins (OVTXs), the main toxic compounds produced by this organism and close analogs to palytoxin (PlTX). Unlike for PlTX, information on OVTXs'toxicity are scarce due to the absence of commercial standards. Extracts from two cultures of Mediterranean strains of O. cf. ovata (MCCV54 and MCCV55), two fractions containing or not OVTXs (prepared from the MCCV54 extract) and OVTX-a and -d (isolated from the MCCV55 extract) were generated. These chemical samples and PlTX were tested on a panel of cell types from several organs and tissues (skin, intestine, lung, liver and nervous system). The MCCV55 extract, containing a 2-fold higher amount of OVTXs than MCCV54 extract, was shown to be more cytotoxic on all the cell lines and more prone to increase interleukin-8 (IL-8) release in keratinocytes. The fraction containing OVTXs was also cytotoxic on the cell lines tested but induced IL-8 release only in liver cells. Unexpectedly, the cell lines tested showed the same sensitivity to the fraction that does not contain OVTXs. With this fraction, a pro-inflammatory effect was shown both in lung and liver cells. The level of cytotoxicity was similar for OVTX-a and -d, except on intestinal and skin cells where a weak difference of toxicity was observed. Among the 3 toxins, only PlTX induced a pro-inflammatory effect mostly on keratinocytes. These results suggest that the ubiquitous Na
    MeSH term(s) Humans ; Marine Toxins/chemistry ; Interleukin-8 ; Cnidarian Venoms/toxicity ; Dinoflagellida/chemistry ; Polyether Toxins ; Acrylamides
    Chemical Substances Marine Toxins ; Interleukin-8 ; palytoxin (OQ17NC0MOV) ; Cnidarian Venoms ; Polyether Toxins ; Acrylamides
    Language English
    Publishing date 2024-02-06
    Publishing country England
    Document type Journal Article
    ZDB-ID 204479-1
    ISSN 1879-3150 ; 0041-0101
    ISSN (online) 1879-3150
    ISSN 0041-0101
    DOI 10.1016/j.toxicon.2024.107631
    Database MEDical Literature Analysis and Retrieval System OnLINE

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  3. Article ; Online: Extraction and analysis by liquid chromatography - tandem mass spectrometry of intra- and extracellular microcystins and nodularin to study the fate of cyanobacteria and cyanotoxins across the freshwater-marine continuum.

    Réveillon, Damien / Georges des Aulnois, Maxime / Savar, Véronique / Robert, Elise / Caruana, Amandine M N / Briand, Enora / Bormans, Myriam

    Toxicon : official journal of the International Society on Toxinology

    2023  Volume 237, Page(s) 107551

    Abstract: The presence of microcystins (MCs) is increasingly being reported in coastal areas worldwide. To provide reliable data regarding this emerging concern, reproducible and accurate methods are required to quantify MCs in salt-containing samples. Herein, we ... ...

    Abstract The presence of microcystins (MCs) is increasingly being reported in coastal areas worldwide. To provide reliable data regarding this emerging concern, reproducible and accurate methods are required to quantify MCs in salt-containing samples. Herein, we characterized methods of extraction and analysis by liquid chromatography coupled to tandem mass spectrometry (LC-MS/MS) for nine MCs and one nodularin (NOD) variants in both cyanobacteria (intracellular) and dissolved forms (extracellular). Different approaches have been used to cope with salinity for the extraction of dissolved MCs but none assessed solid phase extraction (SPE) so far. It was found that salt had negligible effect on the SPE recovery of dissolved MCs using the C18 cartridge while an overestimation up to 67% was noted for some variants with a polymeric sorbent. The limits of detection (LOD) and quantification (LOQ) were 1.0-22 and 5.5-124 pg on column for the intracellular toxins, while 0.05-0.81 and 0.13-2.4 ng/mL were obtained for dissolved toxins. Extraction recoveries were excellent for intracellular (89-121%) and good to excellent for extracellular cyanotoxins (73-102%) while matrix effects were considered neglectable (<12% for 16/20 toxin-matrix combinations), except for the two MC-RR variants. The strategy based on the application of a corrective factor to compensate for losses proved useful as the accuracy was satisfactory (73-117% for intra- and 81-139% for extracellular cyanotoxins, bias <10% for 46/60 conditions, with a few exceptions), with acceptable precisions (intra- and inter-days variabilities <11%). We then applied this method on natural colonies of Microcystis spp. subjected to a salt shock, mimicking their estuarine transfer, in order to assess their survival and to quantify their toxins. The colonies of Microcystis spp. had both their growth and photosynthetic activity impaired at salinities from 10, while toxins remained mainly intracellular (>76%) even at salinity 20, suggesting a potential health risk and contamination of estuarine organisms.
    MeSH term(s) Microcystins/analysis ; Chromatography, Liquid/methods ; Cyanobacteria Toxins ; Tandem Mass Spectrometry/methods ; Fresh Water/chemistry ; Cyanobacteria ; Microcystis ; Chromatography, High Pressure Liquid ; Solid Phase Extraction
    Chemical Substances Microcystins ; Cyanobacteria Toxins
    Language English
    Publishing date 2023-12-07
    Publishing country England
    Document type Journal Article
    ZDB-ID 204479-1
    ISSN 1879-3150 ; 0041-0101
    ISSN (online) 1879-3150
    ISSN 0041-0101
    DOI 10.1016/j.toxicon.2023.107551
    Database MEDical Literature Analysis and Retrieval System OnLINE

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  4. Article: Deeper insight into Gambierdiscus polynesiensis toxin production relies on specific optimization of high-performance liquid chromatography-high resolution mass spectrometry

    Yon, Thomas / Sibat, Manoella / Réveillon, Damien / Bertrand, Samuel / Chinain, Mireille / Hess, Philipp

    Talanta. 2021 Sept. 01, v. 232

    2021  

    Abstract: Ciguatera food poisoning affects consumer health and fisheries’ economies worldwide in tropical zones, and specifically in the Pacific area. The wide variety of ciguatoxins bio-accumulated in fish or shellfish responsible for this neurological illness ... ...

    Abstract Ciguatera food poisoning affects consumer health and fisheries’ economies worldwide in tropical zones, and specifically in the Pacific area. The wide variety of ciguatoxins bio-accumulated in fish or shellfish responsible for this neurological illness are produced by marine dinoflagellates of the genus Gambierdiscus and bio-transformed through the food web. The evaluation of the contents of ciguatoxins in strains of Gambierdiscus relies on the availability of standards and on the development of sensitive and specific tools to detect them. There is a need for sensitive methods for the analysis of pacific ciguatoxins with high resolution mass spectrometry to ensure unequivocal identification of all congeners. We have applied a fractional factorial design of experiment 2^⁸⁻³ for the screening of the significance of eight parameters potentially influencing ionization and ion transmission and their interactions to evaluate the behavior of sodium adducts, protonated molecules and first water losses of CTX4A/B, CTX3B/C, 2-OH-CTX3C and 44-methylgambierone on a Q-TOF equipment. The four parameters that allowed to significantly increase the peak areas of ciguatoxins and gambierones (up to a factor ten) were the capillary voltage, the sheath gas temperature, the ion funnel low pressure voltage and the ion funnel exit voltage. The optimized method was applied to revisit the toxin profile of G. polynesiensis (strain TB92) with a confirmation of the presence of M-seco-CTX4A only putatively reported so far and the detection of an isomer of CTX4A. The improvement in toxin detection also allowed to obtain informative high resolution targeted MS/MS spectra revealing high similarity in fragmentation patterns between putative isomer (4) of CTX3C, 2-OH-CTX3C and CTX3B on one side and between CTX4A, M-seco-CTX4A and the putative isomer on the other side, suggesting a relation of constitutional isomerism between them for both isomers.
    Keywords Gambierdiscus ; ciguatera ; ciguatoxin ; constitutional isomerization ; electric potential difference ; equipment ; fish ; food webs ; ionization ; isomers ; shellfish ; sodium ; temperature
    Language English
    Dates of publication 2021-0901
    Publishing place Elsevier B.V.
    Document type Article
    Note NAL-AP-2-clean
    ZDB-ID 1500969-5
    ISSN 1873-3573 ; 0039-9140
    ISSN (online) 1873-3573
    ISSN 0039-9140
    DOI 10.1016/j.talanta.2021.122400
    Database NAL-Catalogue (AGRICOLA)

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  5. Article: Combined effects of temperature and light intensity on growth, metabolome and ovatoxin content of a Mediterranean Ostreopsis cf. ovata strain

    Gémin, Marin-Pierre / Bertrand, Samuel / Séchet, Véronique / Amzil, Zouher / Réveillon, Damien

    Harmful algae. 2021 June, v. 106

    2021  

    Abstract: Ostreopsis cf. ovata is a benthic and ovatoxin-producing dinoflagellate proliferating yearly along the Mediterranean coasts where blooms have been related to human illness and unusual mortality of marine organisms. The spreading of O. cf. ovata in this ... ...

    Abstract Ostreopsis cf. ovata is a benthic and ovatoxin-producing dinoflagellate proliferating yearly along the Mediterranean coasts where blooms have been related to human illness and unusual mortality of marine organisms. The spreading of O. cf. ovata in this temperate area has been linked to global changes and its consequences such as the increase of temperature or light intensities. In the present study, an experimental design using batch cultures of pre-acclimated cells of a strain of O. cf. ovata isolated from Villefranche-sur-Mer (NW Mediterranean Sea, France), was implemented to investigate the combined effect of temperature (23, 27 and 30 °C) and light intensity (200, 400 and 600 µmol m⁻²s⁻¹) on the growth, metabolome and OVTX content. Both light intensity and temperature affected the growth as significantly higher growth rates were obtained under 400 and 600 µmol m⁻²s⁻¹ while the maximum values were obtained at 27 °C (0.48 d⁻¹). Metabolomic analyses highlighted a clear effect only for temperature that may correspond to two different strategies of acclimation to suboptimal temperatures. Significant features (such as carotenoid and lipids) modified by the temperature and/or light conditions were annotated. Only temperature induced a significant change of OVTX content with higher values measured at the lowest temperature of 23 °C (29 – 36 pg cell⁻¹). In a context of global changes, these results obtained after acclimation suggest that the increase of temperature might favor the proliferation of less toxic cells. However, in the light of the intraspecific variability of O. cf. ovata, further studies will be necessary to test this hypothesis. This study also highlighted the lack of knowledge about the metabolome composition of such non-model organisms that impairs data interpretation. There is a need to study more deeply the metabolome of toxic dinoflagellates to better understand how they can acclimate to a changing environment.
    Keywords Miozoa ; acclimation ; carotenoids ; experimental design ; human diseases ; intraspecific variation ; light intensity ; metabolome ; metabolomics ; mortality ; temperate zones ; temperature ; toxicity ; France ; Mediterranean Sea
    Language English
    Dates of publication 2021-06
    Publishing place Elsevier B.V.
    Document type Article
    ZDB-ID 2091119-1
    ISSN 1878-1470 ; 1568-9883
    ISSN (online) 1878-1470
    ISSN 1568-9883
    DOI 10.1016/j.hal.2021.102060
    Database NAL-Catalogue (AGRICOLA)

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  6. Article ; Online: Targeted and non-targeted mass spectrometry to explore the chemical diversity of the genus Gambierdiscus in the Atlantic Ocean.

    Yon, Thomas / Réveillon, Damien / Sibat, Manoëlla / Holland, Chris / Litaker, R Wayne / Nascimento, Silvia M / Rossignoli, Araceli E / Riobó, Pilar / Hess, Philipp / Bertrand, Samuel

    Phytochemistry

    2024  Volume 222, Page(s) 114095

    Abstract: Dinoflagellates of the genus Gambierdiscus have been associated with ciguatera, the most common non-bacterial fish-related intoxication in the world. Many studies report the presence of potentially toxic Gambierdiscus species along the Atlantic coasts ... ...

    Abstract Dinoflagellates of the genus Gambierdiscus have been associated with ciguatera, the most common non-bacterial fish-related intoxication in the world. Many studies report the presence of potentially toxic Gambierdiscus species along the Atlantic coasts including G. australes, G. silvae and G. excentricus. Estimates of their toxicity, as determined by bio-assays, vary substantially, both between species and strains of the same species. Therefore, there is a need for additional knowledge on the metabolite production of Gambierdiscus species and their variation to better understand species differences. Using liquid chromatography coupled to mass spectrometry, toxin and metabolomic profiles of five species of Gambierdiscus found in the Atlantic Ocean were reported. In addition, a molecular network was constructed aiming at annotating the metabolomes. Results demonstrated that G. excentricus could be discriminated from the other species based solely on the presence of MTX4 and sulfo-gambierones and that the variation in toxin content for a single strain could be up to a factor of two due to different culture conditions between laboratories. While untargeted analyses highlighted a higher variability at the metabolome level, signal correction was applied and supervised multivariate statistics performed on the untargeted data set permitted the selection of 567 features potentially useful as biomarkers for the distinction of G. excentricus, G. caribaeus, G. carolinianus, G. silvae and G. belizeanus. Further studies will be required to validate the use of these biomarkers in discriminating Gambierdiscus species. The study also provided an overview about 17 compound classes present in Gambierdiscus, however, significant improvements in annotation are still required to reach a more comprehensive knowledge of Gambierdiscus' metabolome.
    MeSH term(s) Atlantic Ocean ; Dinoflagellida/chemistry ; Dinoflagellida/metabolism ; Mass Spectrometry ; Chromatography, Liquid ; Metabolomics
    Language English
    Publishing date 2024-04-16
    Publishing country England
    Document type Journal Article ; Review
    ZDB-ID 208884-8
    ISSN 1873-3700 ; 0031-9422
    ISSN (online) 1873-3700
    ISSN 0031-9422
    DOI 10.1016/j.phytochem.2024.114095
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  7. Article ; Online: Sudden peak in tetrodotoxin in French oysters during the summer of 2021: Source investigation using microscopy, metabarcoding and droplet digital PCR.

    Biessy, Laura / Pearman, John K / Mertens, Kenneth Neil / Réveillon, Damien / Savar, Véronique / Hess, Philipp / Hampton, Hannah / Thompson, Lucy / Lebrun, Luc / Terre-Terrillon, Aouregan / Smith, Kirsty F

    Toxicon : official journal of the International Society on Toxinology

    2024  Volume 243, Page(s) 107721

    Abstract: Tetrodotoxin (TTX) is a potent neurotoxin causing human intoxications from contaminated seafood worldwide and is of emerging concern in Europe. Shellfish have been shown to contain varying TTX concentrations globally, with concentrations typically higher ...

    Abstract Tetrodotoxin (TTX) is a potent neurotoxin causing human intoxications from contaminated seafood worldwide and is of emerging concern in Europe. Shellfish have been shown to contain varying TTX concentrations globally, with concentrations typically higher in Pacific oysters Crassostrea gigas in Europe. Despite many decades of research, the source of TTX remains unknown, with bacterial or algal origins having been suggested. The aim of this study was to identify potential source organisms causing TTX contamination in Pacific oysters in French coastal waters, using three different techniques. Oysters were deployed in cages from April to September 2021 in an estuary where TTX was previously detected. Microscopic analyses of water samples were used to investigate potential microalgal blooms present prior or during the peak in TTX. Differences in the bacterial communities from oyster digestive glands (DG) and remaining flesh were explored using metabarcoding, and lastly, droplet digital PCR assays were developed to investigate the presence of Cephalothrix sp., one European TTX-bearing species in the DG of toxic C. gigas. Oysters analysed by liquid chromatography-tandem mass spectrometry contained quantifiable levels of TTX over a three-week period (24 June-15 July 2021), with concentrations decreasing in the DG from 424 μg/kg for the first detection to 101 μg/kg (equivalent to 74 to 17 μg/kg of total flesh), and trace levels being detected until August 13, 2021. These concentrations are the first report of the European TTX guidance levels being exceeded in French shellfish. Microscopy revealed that some microalgae bloomed during the TTX peak, (e.g., Chaetoceros spp., reaching 40,000 cells/L). Prokaryotic metabarcoding showed increases in abundance of Rubritaleaceae (genus Persicirhabdus) and Neolyngbya, before and during the TTX peak. Both phyla have previously been described as possible TTX-producers and should be investigated further. Droplet digital PCR analyses were negative for the targeted TTX-bearing genus Cephalothrix.
    MeSH term(s) Tetrodotoxin/analysis ; Animals ; Polymerase Chain Reaction ; France ; Microscopy ; Crassostrea ; DNA Barcoding, Taxonomic ; Environmental Monitoring/methods ; Microalgae ; Seasons
    Language English
    Publishing date 2024-04-16
    Publishing country England
    Document type Journal Article
    ZDB-ID 204479-1
    ISSN 1879-3150 ; 0041-0101
    ISSN (online) 1879-3150
    ISSN 0041-0101
    DOI 10.1016/j.toxicon.2024.107721
    Database MEDical Literature Analysis and Retrieval System OnLINE

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  8. Article ; Online: Deeper insight into Gambierdiscus polynesiensis toxin production relies on specific optimization of high-performance liquid chromatography-high resolution mass spectrometry.

    Yon, Thomas / Sibat, Manoella / Réveillon, Damien / Bertrand, Samuel / Chinain, Mireille / Hess, Philipp

    Talanta

    2021  Volume 232, Page(s) 122400

    Abstract: Ciguatera food poisoning affects consumer health and fisheries' economies worldwide in tropical zones, and specifically in the Pacific area. The wide variety of ciguatoxins bio-accumulated in fish or shellfish responsible for this neurological illness ... ...

    Abstract Ciguatera food poisoning affects consumer health and fisheries' economies worldwide in tropical zones, and specifically in the Pacific area. The wide variety of ciguatoxins bio-accumulated in fish or shellfish responsible for this neurological illness are produced by marine dinoflagellates of the genus Gambierdiscus and bio-transformed through the food web. The evaluation of the contents of ciguatoxins in strains of Gambierdiscus relies on the availability of standards and on the development of sensitive and specific tools to detect them. There is a need for sensitive methods for the analysis of pacific ciguatoxins with high resolution mass spectrometry to ensure unequivocal identification of all congeners. We have applied a fractional factorial design of experiment 2^
    MeSH term(s) Animals ; Chromatography, High Pressure Liquid ; Ciguatera Poisoning ; Ciguatoxins/analysis ; Dinoflagellida ; Tandem Mass Spectrometry
    Chemical Substances Ciguatoxins (11050-21-8)
    Language English
    Publishing date 2021-04-15
    Publishing country Netherlands
    Document type Journal Article
    ZDB-ID 1500969-5
    ISSN 1873-3573 ; 0039-9140
    ISSN (online) 1873-3573
    ISSN 0039-9140
    DOI 10.1016/j.talanta.2021.122400
    Database MEDical Literature Analysis and Retrieval System OnLINE

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  9. Article ; Online: Combined effects of temperature and light intensity on growth, metabolome and ovatoxin content of a Mediterranean Ostreopsis cf. ovata strain.

    Gémin, Marin-Pierre / Bertrand, Samuel / Séchet, Véronique / Amzil, Zouher / Réveillon, Damien

    Harmful algae

    2021  Volume 106, Page(s) 102060

    Abstract: Ostreopsis cf. ovata is a benthic and ovatoxin-producing dinoflagellate proliferating yearly along the Mediterranean coasts where blooms have been related to human illness and unusual mortality of marine organisms. The spreading of O. cf. ovata in this ... ...

    Abstract Ostreopsis cf. ovata is a benthic and ovatoxin-producing dinoflagellate proliferating yearly along the Mediterranean coasts where blooms have been related to human illness and unusual mortality of marine organisms. The spreading of O. cf. ovata in this temperate area has been linked to global changes and its consequences such as the increase of temperature or light intensities. In the present study, an experimental design using batch cultures of pre-acclimated cells of a strain of O. cf. ovata isolated from Villefranche-sur-Mer (NW Mediterranean Sea, France), was implemented to investigate the combined effect of temperature (23, 27 and 30 °C) and light intensity (200, 400 and 600 µmol m
    MeSH term(s) Aquatic Organisms ; Dinoflagellida ; Humans ; Marine Toxins ; Metabolome ; Temperature
    Chemical Substances Marine Toxins
    Language English
    Publishing date 2021-06-11
    Publishing country Netherlands
    Document type Journal Article ; Research Support, Non-U.S. Gov't
    ZDB-ID 2091119-1
    ISSN 1878-1470 ; 1568-9883
    ISSN (online) 1878-1470
    ISSN 1568-9883
    DOI 10.1016/j.hal.2021.102060
    Database MEDical Literature Analysis and Retrieval System OnLINE

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  10. Article: Effect of a short-term salinity stress on the growth, biovolume, toxins, osmolytes and metabolite profiles on three strains of the Dinophysis acuminata-complex (Dinophysis cf. sacculus)

    Gaillard, Sylvain / Réveillon, Damien / Danthu, Charline / Hervé, Fabienne / Sibat, Manoella / Carpentier, Liliane / Hégaret, Hélène / Séchet, Véronique / Hess, Philipp

    Harmful algae. 2021 July, v. 107

    2021  

    Abstract: Dinophysis is the main dinoflagellate genus responsible for diarrheic shellfish poisoning (DSP) in human consumers of filter feeding bivalves contaminated with lipophilic diarrheic toxins. Species of this genus have a worldwide distribution driven by ... ...

    Abstract Dinophysis is the main dinoflagellate genus responsible for diarrheic shellfish poisoning (DSP) in human consumers of filter feeding bivalves contaminated with lipophilic diarrheic toxins. Species of this genus have a worldwide distribution driven by environmental conditions (temperature, irradiance, salinity, nutrients etc.), and these factors are sensitive to climate change. The D. acuminata-complex may contain several species, including D. sacculus. The latter has been found in estuaries and semi-enclosed areas, water bodies subjected to quick salinity variations and its natural repartition suggests some tolerance to salinity changes. However, the response of strains of D. acuminata-complex (D. cf. sacculus) subjected to salinity stress and the underlying mechanisms have never been studied in the laboratory. Here, a 24 h hypoosmotic (25) and hyperosmotic (42) stress was performed in vitro in a metabolomic study carried out with three cultivated strains of D. cf. sacculus isolated from the French Atlantic and Mediterranean coasts. Growth rate, biovolume and osmolyte (proline, glycine betaine and dimethylsulfoniopropionate (DMSP)) and toxin contents were measured. Osmolyte contents were higher at the highest salinity, but only a significant increase in glycine betaine was observed between the control (35) and the hyperosmotic treatment. Metabolomics revealed significant and strain-dependent differences in metabolite profiles for different salinities. These results, as well as the absence of effects on growth rate, biovolume, okadaic acid (OA) and pectenotoxin (PTXs) cellular contents, suggest that the D. cf. sacculus strains studied are highly tolerant to salinity variations.
    Keywords Dinophysis ; betaine ; climate change ; dimethylsulfoniopropionate ; humans ; light intensity ; lipophilicity ; metabolites ; metabolomics ; okadaic acid ; proline ; salinity ; salt stress ; salt tolerance ; shellfish ; temperature ; toxins
    Language English
    Dates of publication 2021-07
    Publishing place Elsevier B.V.
    Document type Article
    ZDB-ID 2091119-1
    ISSN 1878-1470 ; 1568-9883
    ISSN (online) 1878-1470
    ISSN 1568-9883
    DOI 10.1016/j.hal.2021.102009
    Database NAL-Catalogue (AGRICOLA)

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