Cyanotoxins in the Food Chain

A special issue of Toxins (ISSN 2072-6651). This special issue belongs to the section "Marine and Freshwater Toxins".

Deadline for manuscript submissions: closed (20 April 2023) | Viewed by 11248

Special Issue Editors


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Guest Editor
Robert Gordon University, Garthdee House, Garthdee Road, Aberdeen AB10 7QB, Scotland, UK
Interests: cyanotoxins; bioremediation; nature-based water treatment; advanced oxidation processes; bioactive peptides; purification and analysis
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Guest Editor
CyanoSol Research Group, School of Pharmacy and Life Sciences, Robert Gordon University, Aberdeen, UK
Interests: cyanotoxins; bioremediation; nature-based water treatment; advanced oxidation processes; bioactive peptides; purification and analysis

Special Issue Information

Dear Colleagues,

Exposure to toxins produced by cyanobacteria is typical via ingestion of contaminated drinking or recreational water, and public health in many countries has been protected by the application of WHO guidelines in monitoring programs. In contrast, our understanding of the occurrence of cyanotoxins in the food chain is still in its infancy, so we are keen to hear reports of cyanotoxin (microcystins, nodularins, saxitoxins, cylindrospermopsins, and anatoxins)-associated metabolites along with other bioactive peptides such as cyanopeptolins in the food web. There is a need to understand spatial and temporal toxin occurrence in whole ecosystems, especially those where water supply is frequently contaminated but used for irrigation and as a source of fish/shellfish. With increasing climate events and freshwater to the marine transfer of blooms and phytoplankton, we must also consider exploring potential exposure following the ingestion of marine organisms.

As toxins progress through the food chain, they may bind to proteins or be modified/detoxified; robust methods to unravel these interactions are still needed, along with mass balance through the trophic levels.

Prof. Dr. Christine Edwards
Prof. Dr. Linda Ann Lawton
Guest Editors

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Keywords

  • cyanotoxins
  • microcystin
  • cylindrospermopsin
  • anatoxin-a
  • saxitoxins
  • nodularin
  • novel methods
  • toxin conjugates
  • crops
  • vegetables

Published Papers (5 papers)

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Research

16 pages, 4159 KiB  
Article
Microcystins and Cyanobacterial Contaminants in the French Small-Scale Productions of Spirulina (Limnospira sp.)
by Pierre-Etienne Pinchart, Amandine Leruste, Vanina Pasqualini and Felice Mastroleo
Toxins 2023, 15(6), 354; https://doi.org/10.3390/toxins15060354 - 24 May 2023
Cited by 2 | Viewed by 2188
Abstract
Spirulina is consumed worldwide, in the form of food or dietary supplements, for its nutritional value and health potential. However, these products may contain cyanotoxins, including hepatotoxic microcystins (MCs), produced by cyanobacterial contaminants. The French spirulina market has the particularity of being supplied [...] Read more.
Spirulina is consumed worldwide, in the form of food or dietary supplements, for its nutritional value and health potential. However, these products may contain cyanotoxins, including hepatotoxic microcystins (MCs), produced by cyanobacterial contaminants. The French spirulina market has the particularity of being supplied half-locally by approximately 180 small-scale spirulina production farms. Data about this particular production and possible contaminations with other cyanobacteria and MCs are scarce. Thus, we collected the results of MC analyses and total cyanobacteria counts, carried out between 2013 and 2021, from 95 French spirulina producers who agreed to share their data. These data consisted of MC concentrations determined with an enzyme-linked immunosorbent assay (ELISA) using 623 dry spirulina samples and 105 samples of spirulina cultures. In addition, potentially unsafe samples of dry spirulina were further investigated through mass spectrometry, as duplicate analysis. We confirmed that the situation of the French spirulina production stayed within the safe regulatory level in terms of MC levels. On the other hand, the inventory of cyanobacterial contaminants, based on 539 count results, included 14 taxa. We present their prevalence, interannual evolution and geographical distribution. We also suggested improvements in cultivation practices to limit their propagation. Full article
(This article belongs to the Special Issue Cyanotoxins in the Food Chain)
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18 pages, 1801 KiB  
Article
Determination of Microcystins in Fish Tissue by ELISA and MALDI-TOF MS Using a Highly Specific Single Domain Antibody
by Natalia Badagian, Macarena Pírez Schirmer, Andrés Pérez Parada, Gualberto Gonzalez-Sapienza and Beatriz M. Brena
Toxins 2023, 15(2), 84; https://doi.org/10.3390/toxins15020084 - 17 Jan 2023
Cited by 1 | Viewed by 1640
Abstract
The development of simple, reliable, and cost-effective methods is critically important to study the spatial and temporal variation of microcystins (MCs) in the food chain. Nanobodies (Nbs), antigen binding fragments from camelid antibodies, present valuable features for analytical applications. Their small antigen binding [...] Read more.
The development of simple, reliable, and cost-effective methods is critically important to study the spatial and temporal variation of microcystins (MCs) in the food chain. Nanobodies (Nbs), antigen binding fragments from camelid antibodies, present valuable features for analytical applications. Their small antigen binding site offers a focused recognition of small analytes, reducing spurious cross-reactivity and matrix effects. A high affinity and broad cross-reactivity anti-MCs-Nb, from a llama antibody library, was validated in enzyme linked immunosorbent assay (ELISA), and bound to magnetic particles with an internal standard for pre-concentration in quantitative-matrix-assisted laser desorption ionization-time of flight mass spectrometry (Nb-QMALDI MS). Both methods are easy and fast; ELISA provides a global result, while Nb-QMALDI MS allows for the quantification of individual congeners and showed excellent performance in the fish muscle extracts. The ELISA assay range was 1.8–29 ng/g and for Nb-QMALDI, it was 0.29–29 ng/g fish ww. Fifty-five fish from a MC-containing dam were analyzed by both methods. The correlation ELISA/sum of the MC congeners by Nb-QMALDI-MS was very high (r Spearman = 0.9645, p < 0.0001). Using ROC curves, ELISA cut-off limits were defined to accurately predict the sum of MCs by Nb-QMALDI-MS (100% sensitivity; ≥89% specificity). Both methods were shown to be simple and efficient for screening MCs in fish muscle to prioritize samples for confirmatory methods. Full article
(This article belongs to the Special Issue Cyanotoxins in the Food Chain)
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34 pages, 4265 KiB  
Article
A Feasibility Study into the Production of a Mussel Matrix Reference Material for the Cyanobacterial Toxins Microcystins and Nodularins
by Andrew D. Turner, Daniel G. Beach, Amanda Foss, Ingunn A. Samdal, Kjersti L. E. Løvberg, Julia Waack, Christine Edwards, Linda A. Lawton, Karl J. Dean, Benjamin H. Maskrey and Adam M. Lewis
Toxins 2023, 15(1), 27; https://doi.org/10.3390/toxins15010027 - 30 Dec 2022
Cited by 3 | Viewed by 1990
Abstract
Microcystins and nodularins, produced naturally by certain species of cyanobacteria, have been found to accumulate in aquatic foodstuffs such as fish and shellfish, resulting in a risk to the health of the seafood consumer. Monitoring of toxins in such organisms for risk management [...] Read more.
Microcystins and nodularins, produced naturally by certain species of cyanobacteria, have been found to accumulate in aquatic foodstuffs such as fish and shellfish, resulting in a risk to the health of the seafood consumer. Monitoring of toxins in such organisms for risk management purposes requires the availability of certified matrix reference materials to aid method development, validation and routine quality assurance. This study consequently targeted the preparation of a mussel tissue reference material incurred with a range of microcystin analogues and nodularins. Nine targeted analogues were incorporated into the material as confirmed through liquid chromatography with tandem mass spectrometry (LC-MS/MS), with an additional 15 analogues detected using LC coupled to non-targeted high resolution mass spectrometry (LC-HRMS). Toxins in the reference material and additional source tissues were quantified using LC-MS/MS, two different enzyme-linked immunosorbent assay (ELISA) methods and with an oxidative-cleavage method quantifying 3-methoxy-2-methyl-4-phenylbutyric acid (MMPB). Correlations between the concentrations quantified using the different methods were variable, likely relating to differences in assay cross-reactivities and differences in the abilities of each method to detect bound toxins. A consensus concentration of total soluble toxins determined from the four independent test methods was 2425 ± 575 µg/kg wet weight. A mean 43 ± 9% of bound toxins were present in addition to the freely extractable soluble form (57 ± 9%). The reference material produced was homogenous and stable when stored in the freezer for six months without any post-production stabilization applied. Consequently, a cyanotoxin shellfish reference material has been produced which demonstrates the feasibility of developing certified seafood matrix reference materials for a large range of cyanotoxins and could provide a valuable future resource for cyanotoxin risk monitoring, management and mitigation. Full article
(This article belongs to the Special Issue Cyanotoxins in the Food Chain)
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18 pages, 1695 KiB  
Article
LC-MS/MS Validation and Quantification of Cyanotoxins in Algal Food Supplements from the Belgium Market and Their Molecular Origins
by Wannes Hugo R. Van Hassel, Anne-Catherine Ahn, Bart Huybrechts, Julien Masquelier, Annick Wilmotte and Mirjana Andjelkovic
Toxins 2022, 14(8), 513; https://doi.org/10.3390/toxins14080513 - 27 Jul 2022
Cited by 10 | Viewed by 1939
Abstract
Food supplements are gaining popularity worldwide. However, harmful natural compounds can contaminate these products. In the case of algae-based products, the presence of toxin-producing cyanobacteria may cause health risks. However, data about the prevalence of algal food supplements on the Belgian market and [...] Read more.
Food supplements are gaining popularity worldwide. However, harmful natural compounds can contaminate these products. In the case of algae-based products, the presence of toxin-producing cyanobacteria may cause health risks. However, data about the prevalence of algal food supplements on the Belgian market and possible contaminations with cyanotoxins are scarce. Therefore, we optimized and validated a method based on Ultra High Performance Liquid Chromatography-Tandem Mass Spectrometry to quantify eight microcystin congeners and nodularin in algal food supplements. Our analytical method was successfully validated and applied on 35 food supplement samples. Nine out of these samples contained microcystin congeners, of which three exceeded 1 µg g−1, a previously proposed guideline value. Additionally, the mcyE gene was amplified and sequenced in ten products to identify the taxon responsible for the toxin production. For seven out of these ten samples, the mcyE gene could be amplified and associated to Microcystis sp. EFSA and posology consumption data for algal-based food supplements were both combined with our toxin prevalence data to establish different toxin exposure scenarios to assess health risks and propose new guideline values. Full article
(This article belongs to the Special Issue Cyanotoxins in the Food Chain)
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20 pages, 3658 KiB  
Article
Effects of Irrigation with Microcystin-Containing Water on Growth, Physiology, and Antioxidant Defense in Strawberry Fragaria vulgaris under Hydroponic Culture
by Mohammed Haida, Fatima El Khalloufi, Richard Mugani, El Mahdi Redouane, Alexandre Campos, Vitor Vasconcelos and Brahim Oudra
Toxins 2022, 14(3), 198; https://doi.org/10.3390/toxins14030198 - 07 Mar 2022
Cited by 4 | Viewed by 2638
Abstract
Over the last years, the use of artificial lakes and ponds to irrigate agricultural crops has been intensified and cultivation methods have been diversified. Hydroponics is a type of hydroculture which usually involves growing plants in an inert substrate, by using nutrient-enriched water [...] Read more.
Over the last years, the use of artificial lakes and ponds to irrigate agricultural crops has been intensified and cultivation methods have been diversified. Hydroponics is a type of hydroculture which usually involves growing plants in an inert substrate, by using nutrient-enriched water to support plant growth. However, irrigating plants in hydroponic-based culture must be accompanied by monitoring the quality of irrigation water. The human health risks involved are mainly related to the proliferation of microcystin-producing cyanobacteria that contaminate water used for irrigation purposes. Strawberry (Fragaria vulgaris L.) is a widely cultivated plant of an increased economically importance worldwide. Its fruits provide essential elements for human nutrition; therefore, the study of its sensitivity to microcystins (MCs) is of paramount importance. The objective of this study was to evaluate the effects of MCs in irrigation water on the growth, physiology, and antioxidant defense system in F. vulgaris. In this study, strawberry seedlings at the three-leaf stage were grown in pots containing perlite under controlled conditions. Plants were exposed to a crude extract of Microcystis aeruginosa bloom at different concentrations of MCs (1, 5, 10, and 20 μg/L) for 60 days of exposure. The results showed that the highest concentrations of 10 and 20 μg/L induced a decrease in growth parameters. They resulted in root/shoot length decrease as well as number of leaves, roots/leaves dry and fresh weight. Furthermore, MCs reduced chlorophyll/carotenoid content, stomatal conductance, fluorescence, and total protein content of strawberry plants. At the same time, a significant increase in Malondialdehyde (MDA) (an indicator of lipid peroxidation), polyphenol, and sugar content were recorded in strawberry plants exposed to MCs at 5, 10, and 20 μg/L compared with the control. Additionally, superoxide dismutase (SOD), catalase (CAT), peroxidase (POD), Polyphenoloxydase (PPO), and ascorbate peroxidase (APX) activities significantly increased in plants under MCs exposure. The oxidative stress was higher in plants exposed to 10 and 20 μg/L of MCs from the second harvest (after 60 days of exposure) compared to those from the first harvest (after 30 days). Overall, the results obtained in this study indicate an increasingly negative effect of MCs on strawberry plants grown in hydroponics even at concentrations (10 and 20 µg/L). This effect is more damaging on the roots after exposure (60 days). Full article
(This article belongs to the Special Issue Cyanotoxins in the Food Chain)
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