Cyanobacterial Toxins: Toxins Production and Risk Assessment

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

Deadline for manuscript submissions: closed (30 November 2023) | Viewed by 20803

Special Issue Editors


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Guest Editor
Interdisciplinary Centre of Marine and Environmental Research, University of Porto, Matosinhos, Portugal
Interests: cyanobacteria; cyanotoxins; environment; toxicology; natural products
Special Issues, Collections and Topics in MDPI journals

E-Mail Website
Guest Editor
1. Faculdade de Ciências da Universidade do Porto, 4169-007 Porto, Portugal
2. CIIMAR, Interdisciplinary Centre of Marine and Environmental Research of the University of Porto, 4450-208 Porto, Portugal
Interests: cyanobacteria; toxins; cyanotoxins; marine biotechnology; secondary metabolites; cyanobacterial blooms; ecotoxicology; environmental contamination
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

Cyanobacteria have long been a nuisance to our ecosystems through the production of harmful toxins denoted cyanotoxins. With extensive and continuously increasing reports on the toxin hazards to humans, domestic animals and wildlife it becomes imperative to discuss and present data on the continuous implications and repercussions of cyanotoxins globally. Plants, animals, invertebrates and humans are targets of cyanotoxins intoxications. Therefore its report and discussion is a need since particularly in the less developed countries these intoxications are poorly followed. Describing impacts of cyanotoxins in water quality and water management are also aims of this Special Issue. Risk assessment studies are imperative to tackle cyanotoxins harmful intoxication episodes globally in order to improve the social and economic benefits of our ecosystems. Therefore descriptions of toxic taxa, new and existing cyanotoxins, toxin production amounts in all types of samples, risk assessment and epidemiological studies are welcomed in this Special Issue.

Dr. Cristiana Moreira
Prof. Dr. Vitor Vasconcelos
Guest Editor

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Keywords

  • cyanobacteria
  • cyanotoxins
  • water quality
  • epidemiology
  • risk assessment
  • toxin production

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Published Papers (8 papers)

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Research

24 pages, 5982 KiB  
Article
Evaluation of the Removal and Effects of Cylindrospermopsin on Ripened Slow Sand Filters
by Daniel Valencia-Cárdenas, Thatiane Souza Tavares, Rafaella Silveira, Cristina Celia Silveira Brandão, Raquel Moraes Soares and Yovanka Pérez Ginoris
Toxins 2023, 15(9), 543; https://doi.org/10.3390/toxins15090543 - 2 Sep 2023
Cited by 1 | Viewed by 1300
Abstract
The occurrence of toxic blooms of cyanobacteria has been a matter of public health interest due to the cyanotoxins produced by these microorganisms. Cylindrospermopsin (CYN) is a cyanotoxin of particular concern due to its toxic effects on humans. This study investigated the removal [...] Read more.
The occurrence of toxic blooms of cyanobacteria has been a matter of public health interest due to the cyanotoxins produced by these microorganisms. Cylindrospermopsin (CYN) is a cyanotoxin of particular concern due to its toxic effects on humans. This study investigated the removal and effects of CYN in ripened slow sand filters (SSFs) treating water from Paranoá Lake, Brasilia, Brazil. Four pilot-scale SSFs were ripened and operated for 74 days. Two contamination peaks with CYN were applied along the filtration run. The improvement of any of the evaluated water quality parameters was not affected by the presence of CYN in the raw water. The SSFs efficiently removed CYN, presenting concentrations lower than 0.8 µg/L in the filtered water. The microbiota of the SSFs were dominated by protozoa of the genus Euglypha and amoebas of the genera Arcella, Centropyxis, and Amoeba, together with some groups of rotifers. These microorganisms played a crucial role in removing total coliforms and E. coli. In addition, CYN was not identified as a determining factor in the microbiota composition. Full article
(This article belongs to the Special Issue Cyanobacterial Toxins: Toxins Production and Risk Assessment)
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11 pages, 1569 KiB  
Article
Purification and Activity of the Second Recombinant Enzyme for Biodegrading Linearized Microcystins by Sphingopyxis sp. USTB-05
by Junhui Teng, Meijie Song, Qianqian Xu, Qianwen Zou, Haiyang Zhang, Chunhua Yin, Xiaolu Liu, Yang Liu and Hai Yan
Toxins 2023, 15(8), 494; https://doi.org/10.3390/toxins15080494 - 4 Aug 2023
Cited by 2 | Viewed by 1604
Abstract
Hepatotoxic microcystins (MCs) are produced and released by the harmful bloom-forming cyanobacteria, which severely threaten drinking water safety and human health due to their high toxicity, widespread distribution, and structural stability. The linearized microcystinase (MlrB) further hydrolyses the poisonous linearized MCs produced by [...] Read more.
Hepatotoxic microcystins (MCs) are produced and released by the harmful bloom-forming cyanobacteria, which severely threaten drinking water safety and human health due to their high toxicity, widespread distribution, and structural stability. The linearized microcystinase (MlrB) further hydrolyses the poisonous linearized MCs produced by the microcystinase-catalysed MCs to form tetrapeptides. Here, the purification and activity of MlrB were investigated. The results showed that the linearized products generated by 12.5 mg/L MC-LR and MC-RR were removed by purified recombinant MlrB at a protein concentration of 1 mg/L within 30 min. The high catalytic activity of MlrB can be obtained via heterologous expression and affinity purification, which lays the foundation for further studies on the properties and mechanism of MCs biodegradation enzymes. Full article
(This article belongs to the Special Issue Cyanobacterial Toxins: Toxins Production and Risk Assessment)
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18 pages, 3901 KiB  
Article
Metabolomics Reveals Strain-Specific Cyanopeptide Profiles and Their Production Dynamics in Microcystis aeruginosa and M. flos-aquae
by Kimberlynn McDonald, Natasha DesRochers, Justin B. Renaud, Mark W. Sumarah and David R. McMullin
Toxins 2023, 15(4), 254; https://doi.org/10.3390/toxins15040254 - 31 Mar 2023
Cited by 5 | Viewed by 2071
Abstract
Cyanobacterial blooms that release biologically active metabolites into the environment are increasing in frequency as a result of the degradation of freshwater ecosystems globally. The microcystins are one group of cyanopeptides that are extensively studied and included in water quality risk management frameworks. [...] Read more.
Cyanobacterial blooms that release biologically active metabolites into the environment are increasing in frequency as a result of the degradation of freshwater ecosystems globally. The microcystins are one group of cyanopeptides that are extensively studied and included in water quality risk management frameworks. Common bloom-forming cyanobacteria produce incredibly diverse mixtures of other cyanopeptides; however, data on the abundance, distribution, and biological activities of non-microcystin cyanopeptides are limited. We used non-targeted LC-MS/MS metabolomics to study the cyanopeptide profiles of five Microcystis strains: four M. aeruginosa and one M. flos-aquae. Multivariate analysis and GNPS molecular networking demonstrated that each Microcystis strain produced a unique mixture of cyanopeptides. In total, 82 cyanopeptides from the cyanopeptolin (n = 23), microviridin (n = 18), microginin (n = 12), cyanobactin (n = 14), anabaenopeptin (n = 6), aeruginosin (n = 5), and microcystin (n = 4) classes were detected. Microcystin diversity was low compared with the other detected cyanopeptide classes. Based on surveys of the literature and spectral databases, most cyanopeptides represented new structures. To identify growth conditions yielding high amounts of multiple cyanopeptide groups, we next examined strain-specific cyanopeptide co-production dynamics for four of the studied Microcystis strains. When strains were cultivated in two common Microcystis growth media (BG-11 and MA), the qualitative cyanopeptides profiles remained unchanged throughout the growth cycle. For each of the cyanopeptide groups considered, the highest relative cyanopeptide amounts were observed in the mid-exponential growth phase. The outcomes of this study will guide the cultivation of strains producing common and abundant cyanopeptides contaminating freshwater ecosystems. The synchronous production of each cyanopeptide group by Microcystis highlights the need to make more cyanopeptide reference materials available to investigate their distributions and biological functions. Full article
(This article belongs to the Special Issue Cyanobacterial Toxins: Toxins Production and Risk Assessment)
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30 pages, 5024 KiB  
Article
Water Quality, Toxicity and Diversity of Planktonic and Benthic Cyanobacteria in Pristine Ancient Lake Khubsugul (Hövsgöl), Mongolia
by Olga I. Belykh, Ekaterina G. Sorokovikova, Irina V. Tomberg, Galina A. Fedorova, Anton V. Kuzmin, Andrey Yu. Krasnopeev, Maria Yu. Suslova, Sergey A. Potapov, Tatiana I. Belykh, Jadambaa Norovsuren, Agnia D. Galachyants and Irina V. Tikhonova
Toxins 2023, 15(3), 213; https://doi.org/10.3390/toxins15030213 - 10 Mar 2023
Cited by 5 | Viewed by 3052
Abstract
For the first time, microcystin-producing cyanobacteria have been detected in Khubsugul, which is ancient, pristine and one of the world’s largest lakes. The microcystin synthetase genes belonged to the genera Nostoc, Microcystis and possibly Snowella spp. No microcystins were found in the [...] Read more.
For the first time, microcystin-producing cyanobacteria have been detected in Khubsugul, which is ancient, pristine and one of the world’s largest lakes. The microcystin synthetase genes belonged to the genera Nostoc, Microcystis and possibly Snowella spp. No microcystins were found in the water of the lake. Using the HPLC-HRMS/TOF, five microcystin congeners were identified in biofilms from stony substrates sampled in the coastal zone. The concentration of microcystins in biofilms was low: 41.95 µg g−1 d. wt. by ELISA and 55.8 µg g−1 d. wt. using HPLC. The taxonomic composition of planktonic and benthic cyanobacterial communities was determined by means of microscopy and high-throughput sequencing of 16S rDNA amplicons. Nostocales cyanobacteria dominated benthos of Lake Khubsugul and Synechococcales—plankton. The abundance of cyanobacteria was low both in plankton and benthos; there was no mass development of cyanobacteria. Hydrochemical and microbiological analyses showed that the water in the lake was clean; the number of faecal microorganisms was significantly below the acceptable guideline values. Hydrochemical and hydrophysical parameters, and the concentration of chlorophyll a, were low and within the range of values recorded in the 1970s to 1990s, and corresponded to the oligotrophic state of the lake. There were no signs of anthropogenic eutrophication of the lake and no conditions for the cyanobacterial blooms. Full article
(This article belongs to the Special Issue Cyanobacterial Toxins: Toxins Production and Risk Assessment)
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11 pages, 3507 KiB  
Article
β-N-Methylamino-L-Alanine (BMAA) Modulates the Sympathetic Regulation and Homeostasis of Polyamines
by Milena Shkodrova, Milena Mishonova, Mariela Chichova, Iliyana Sazdova, Bilyana Ilieva, Dilyana Doncheva-Stoimenova, Neli Raikova, Milena Keremidarska-Markova and Hristo Gagov
Toxins 2023, 15(2), 141; https://doi.org/10.3390/toxins15020141 - 9 Feb 2023
Cited by 2 | Viewed by 2278
Abstract
The neurotoxin β-N-methylamino-L-alanine (BMAA) is a non-proteinogenic amino acid produced by cyanobacteria. Non-neuronal toxicity of BMAA is poorly studied with a reported increase in reactive oxygen species and a decrease in the antioxidant capacity of liver, kidney, and colorectal adenocarcinoma cells. The aim [...] Read more.
The neurotoxin β-N-methylamino-L-alanine (BMAA) is a non-proteinogenic amino acid produced by cyanobacteria. Non-neuronal toxicity of BMAA is poorly studied with a reported increase in reactive oxygen species and a decrease in the antioxidant capacity of liver, kidney, and colorectal adenocarcinoma cells. The aim of this research is to study the toxicity of BMAA (0.1–1 mM) on mitochondria and submitochondrial particles with ATPase activity, on the semicarbazide-sensitive amino oxidases (SSAOs) activity of rat liver, and on an in vitro model containing functionally active excitable tissues—regularly contracting heart muscle preparation with a preserved autonomic innervation. For the first time the BMAA-dependent inhibition of SSAO activity, the elimination of the positive inotropic effect of adrenergic innervation, and the direct and reversible inhibition of adrenaline signaling in ventricular myocytes with 1 mM BMAA were observed. Additionally, it is confirmed that 1 mM BMAA can activate mitochondrial ATPase indirectly. It is concluded that a higher dose of BMAA may influence multiple physiological and pathological processes as it slows down the degradation of biogenic amines, downregulates the sympathetic neuromediation, and embarrasses the cell signaling of adrenergic receptors. Full article
(This article belongs to the Special Issue Cyanobacterial Toxins: Toxins Production and Risk Assessment)
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19 pages, 5474 KiB  
Article
Confirmation Using Triple Quadrupole and High-Resolution Mass Spectrometry of a Fatal Canine Neurotoxicosis following Exposure to Anatoxins at an Inland Reservoir
by Andrew D. Turner, Florence R. I. Turner, Martha White, David Hartnell, Claire G. Crompton, Nicola Bates, Jan Egginton, Liz Branscombe, Adam M. Lewis and Benjamin H. Maskrey
Toxins 2022, 14(11), 804; https://doi.org/10.3390/toxins14110804 - 18 Nov 2022
Cited by 7 | Viewed by 3906
Abstract
Cyanobacterial blooms are often associated with the presence of harmful natural compounds which can cause adverse health effects in both humans and animals. One family of these compounds, known as anatoxins, have been linked to the rapid deaths of cattle and dogs through [...] Read more.
Cyanobacterial blooms are often associated with the presence of harmful natural compounds which can cause adverse health effects in both humans and animals. One family of these compounds, known as anatoxins, have been linked to the rapid deaths of cattle and dogs through neurotoxicological action. Here, we report the findings resulting from the death of a dog at a freshwater reservoir in SW England. Poisoning was rapid following exposure to material at the side of the lake. Clinical signs included neurological distress, diaphragmatic paralysis and asphyxia prior to death after 45 min of exposure. Analysis by HILIC-MS/MS of urine and stomach content samples from the dog revealed the detection of anatoxin-a and dihydroanatoxin-a in both samples with higher concentrations of the latter quantified in both matrices. Detection and quantitative accuracy was further confirmed with use of accurate mass LC-HRMS. Additional anatoxin analogues were also detected by LC-HRMS, including 4-keto anatoxin-a, 4-keto-homo anatoxin-a, expoxy anatoxin-a and epoxy homo anatoxin-a. The conclusion of neurotoxicosis was confirmed with the use of two independent analytical methods showing positive detection and significantly high quantified concentrations of these neurotoxins in clinical samples. Together with the clinical signs observed, we have confirmed that anatoxins were responsible for the rapid death of the dog in this case. Full article
(This article belongs to the Special Issue Cyanobacterial Toxins: Toxins Production and Risk Assessment)
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23 pages, 3454 KiB  
Article
Characterization of Potential Threats from Cyanobacterial Toxins in Lake Victoria Embayments and during Water Treatment
by Mark Olokotum, Jean-François Humbert, Catherine Quiblier, William Okello, Ronald Semyalo, Marc Troussellier, Benjamin Marie, Kathrin Baumann, Rainer Kurmayer and Cécile Bernard
Toxins 2022, 14(10), 664; https://doi.org/10.3390/toxins14100664 - 23 Sep 2022
Cited by 7 | Viewed by 2819
Abstract
Africa’s water needs are often supported by eutrophic water bodies dominated by cyanobacteria posing health threats to riparian populations from cyanotoxins, and Lake Victoria is no exception. In two embayments of the lake (Murchison Bay and Napoleon Gulf), cyanobacterial surveys were conducted to [...] Read more.
Africa’s water needs are often supported by eutrophic water bodies dominated by cyanobacteria posing health threats to riparian populations from cyanotoxins, and Lake Victoria is no exception. In two embayments of the lake (Murchison Bay and Napoleon Gulf), cyanobacterial surveys were conducted to characterize the dynamics of cyanotoxins in lake water and water treatment plants. Forty-six cyanobacterial taxa were recorded, and out of these, fourteen were considered potentially toxigenic (i.e., from the genera Dolichospermum, Microcystis, Oscillatoria, Pseudanabaena and Raphidiopsis). A higher concentration (ranging from 5 to 10 µg MC-LR equiv. L−1) of microcystins (MC) was detected in Murchison Bay compared to Napoleon Gulf, with a declining gradient from the inshore (max. 15 µg MC-LR equiv. L−1) to the open lake. In Murchison Bay, an increase in Microcystis sp. biovolume and MC was observed over the last two decades. Despite high cell densities of toxigenic Microcystis and high MC concentrations, the water treatment plant in Murchison Bay efficiently removed the cyanobacterial biomass, intracellular and dissolved MC to below the lifetime guideline value for exposure via drinking water (<1.0 µg MC-LR equiv. L−1). Thus, the potential health threats stem from the consumption of untreated water and recreational activities along the shores of the lake embayments. MC concentrations were predicted from Microcystis cell numbers regulated by environmental factors, such as solar radiation, wind speed in the N–S direction and turbidity. Thus, an early warning through microscopical counting of Microcystis cell numbers is proposed to better manage health risks from toxigenic cyanobacteria in Lake Victoria. Full article
(This article belongs to the Special Issue Cyanobacterial Toxins: Toxins Production and Risk Assessment)
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12 pages, 1550 KiB  
Article
Statistical Inferences Applying Non-Parametric Data on Cyanobacterial Investigations: Contributions to Water Quality and New Trends under Global Changes on Portuguese Freshwater Ecosystems
by Cristiana Moreira, Ana Matos, Aldo Barreiro, Cidália Gomes, Vitor Vasconcelos and Agostinho Antunes
Toxins 2022, 14(9), 638; https://doi.org/10.3390/toxins14090638 - 15 Sep 2022
Viewed by 1969
Abstract
Cyanobacteria are a bloom-forming ancient group of photosynthetic prokaryotes. A rise in temperature is a major contributor to its massive proliferation, namely on freshwater ecosystems, with social and economic impacts. Thus, reliable and cost-effective tools can permit the fast surveillance and assessment of [...] Read more.
Cyanobacteria are a bloom-forming ancient group of photosynthetic prokaryotes. A rise in temperature is a major contributor to its massive proliferation, namely on freshwater ecosystems, with social and economic impacts. Thus, reliable and cost-effective tools can permit the fast surveillance and assessment of temperature effects on potentially toxic cyanobacteria distribution and impacts. The occurrence of three potentially toxic cyanobacteria species was assessed on seven sampling points across three sampling years. Moreover, the association between the occurrence of those cyanobacteria species with climate change events was addressed. Here, we combined molecular and statistical methods to study the impacts of temperature on the occurrence of three globally occurring cyanotoxin-producing cyanobacteria species—Microcystis aeruginosa (microcystins), Raphidiopsis raciborskii (cylindrospermopsins and saxitoxins) and Planktothrix agardhii (microcystins and saxitoxins). Samples were collected on seven European temperate freshwater systems located on the North and Centre regions of Portugal, across three distinct sampling years with distinct ranges of air temperature. Data support that M. aeruginosa is still a common inhabitant of Portuguese freshwater ecosystems and a new trend was found on R. raciborskii recent invasion and establishment on the colder north ecosystems of Portugal. Additionally, the highest frequency of detection of both cyanobacteria was associated with warmer years. P. agardhii also revealed a new trend, being reported for the first time on North and Centre Regions of Portugal, however with no statistical relation with air temperature, demonstrating a higher ecological fitness. Distinct profiles of the statistical analysis on the three tested cyanobacteria species contribute to deepen the studies on other species as well as of our analyzed species on a global level. This assessment may help to anticipate possible repercussions on water quality and public health due to most probable alterations on cyanotoxins profile given the ecological fitness established among air temperature and PCR detection of potentially toxic cyanobacteria. Full article
(This article belongs to the Special Issue Cyanobacterial Toxins: Toxins Production and Risk Assessment)
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