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Potentially Toxic Benthic Microorganisms in Freshwater and Marine Ecosystems

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

Deadline for manuscript submissions: closed (31 December 2019) | Viewed by 59024

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Special Issue Editors

Dr. Philipp Hess

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Guest Editor

Laboratoire Phycotoxines, Ifremer, Nantes, France
Interests: marine algal; bacterial and cyanobacterial toxins; mass spectrometric analysis of and biological assays for toxins and related metabolites; ecophysiology of toxin production and biosynthesis; HABs and climate change; reference materials; monitoring and risk evaluation
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Dr. Jean-Francois Humbert

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Institute of Ecology and Environmental Sciences of Paris (iEES Paris), Sorbonne University, Paris, France
Interests: cyanobacteria; cyanotoxins; ecology; microbial interactions; comparative genomics; cyanobacteria and cyanotoxin monitoring; risk managment

Special Issue Information

Dear Colleagues,

Benthic, epilitic, and epiphytic habitats in aquatic ecosystems are a way of life shared by numerous potentially-toxic microalgae and cyanobacteria, both in freshwater and marine ecosystems. In these latter ones, potentially toxic benthic microalgae have been extensively studied. While recent papers have shown the interest to better understand their benthic ecology, in particular their positive and negative interactions with other species into the biofilms, many aspects remain to be clarified: comparative risk of benthic and planktonic phase, species identification and distribution, toxin identity, etc.

In freshwater ecosystems, benthic cyanobacteria have received much less attention than planktonic species. Still, in the recent years, massive developments of river biofilms dominated by toxic cyanobacteria have been reported in several countries (New Zealand, France, USA, etc.), suggesting that changes in local or global environmental conditions might promote the recent increase of these events. Proliferations of benthic cyanobacteria have led to death of several dozen dogs in all these countries due to the production of anatoxins.

Consequently, increased knowledge is needed by scientists, ecosystem managers and other stakeholders to better comprehend the ecology and toxicity of these benthic cyanobacteria and microalgae and to finally limit the sanitary risks associated with their proliferations.

The aim of the current Special Issue is to gather the most recent research on benthic cyanobacteria and microalgae proliferating in marine and freshwater ecosystems and on their toxins. All papers dealing with the taxonomy, genetic diversity, ecology and toxicity of biofilms dominated by potentially-toxic cyanobacteria and microalgae and on risk assessment and management associated with such assemblages will be considered in this Special Issue.

Dr. Philipp Hess
Dr. Jean-Francois Humbert
Guest Editors

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Keywords

Benthic cyanobacteria and microalgae
marine and freshwater ecosystems
taxonomy
ecology
toxicity

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Published Papers (11 papers)

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Research

15 pages, 2344 KiB

Open AccessEditor’s ChoiceArticle

Toxicity Characterisation of Gambierdiscus Species from the Canary Islands

by Araceli E. Rossignoli, Angels Tudó, Isabel Bravo, Patricio A. Díaz, Jorge Diogène and Pilar Riobó

Toxins 2020, 12(2), 134; https://doi.org/10.3390/toxins12020134 - 21 Feb 2020

Cited by 33 | Viewed by 4968

Abstract

In the last decade, several outbreaks of ciguatera fish poisoning (CFP) have been reported in the Canary Islands (central northeast Atlantic Ocean), confirming ciguatera as an emerging alimentary risk in this region. Five Gambierdiscus species, G. australes, G. excentricus, G. silvae, G. carolinianus and G. caribaeus, have been detected in macrophytes from this area and are known to produce the ciguatoxins (CTXs) that cause CFP. A characterization of the toxicity of these species is the first step in identifying locations in the Canary Islands at risk of CFP. Therefore, in this study the toxicity of 63 strains of these five Gambierdiscus species were analysed using the erythrocyte lysis assay to evaluate their maitotoxin (MTX) content. In addition, 20 of the strains were also analysed in a neuroblastoma Neuro-2a (N2a) cytotoxicity assay to determine their CTX-like toxicity. The results allowed the different species to be grouped according to their ratios of CTX-like and MTX-like toxicity. MTX-like toxicity was especially high in G. excentricus and G. australes but much lower in the other species and lowest in G. silvae. CTX-like toxicity was highest in G. excentricus, which produced the toxin in amounts ranging between 128.2 ± 25.68 and 510.6 ± 134.2 fg CTX1B equivalents (eq) cell⁻¹ (mean ± SD). In the other species, CTX concentrations were as follows: G. carolinianus (100.84 ± 18.05 fg CTX1B eq cell⁻¹), G. australes (31.1 ± 0.56 to 107.16 ± 21.88 fg CTX1B eq cell⁻¹), G. silvae (12.19 ± 0.62 to 76.79 ± 4.97 fg CTX1B eq cell⁻¹) and G. caribaeus (<LOD to 90.37 ± 15.89 fg CTX1B eq cell⁻¹). Unlike the similar CTX-like toxicity of G. australes and G. silvae strains from different locations, G. excentricus and G. caribaeus differed considerably according to the origin of the strain. These differences emphasise the importance of species identification to assess the regional risk of CFP. Full article

(This article belongs to the Special Issue Potentially Toxic Benthic Microorganisms in Freshwater and Marine Ecosystems)

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10 pages, 884 KiB

Open AccessEditor’s ChoiceArticle

Acute Oral Toxicity of Pinnatoxin G in Mice

by Silvio Sosa, Marco Pelin, Federica Cavion, Fabienne Hervé, Philipp Hess and Aurelia Tubaro

Toxins 2020, 12(2), 87; https://doi.org/10.3390/toxins12020087 - 28 Jan 2020

Cited by 26 | Viewed by 4092

Abstract

Pinnatoxin G (PnTx-G) is a marine cyclic imine toxin produced by the dinoflagellate Vulcanodinium rugosum, frequently detected in edible shellfish from Ingril Lagoon (France). As other pinnatoxins, to date, no human poisonings ascribed to consumption of PnTx-G contaminated seafood have been reported, despite its potent antagonism at nicotinic acetylcholine receptors and its high and fast-acting toxicity after intraperitoneal or oral administration in mice. The hazard characterization of PnTx-G by oral exposure is limited to a single acute toxicity study recording lethality and clinical signs in non-fasted mice treated by gavage or through voluntary food ingestion, which showed differences in PnTx-G toxic potency. Thus, an acute toxicity study was carried out using 3 h-fasted CD-1 female mice, administered by gavage with PnTx-G (8–450 µg kg⁻¹). At the dose of 220 µg kg⁻¹ and above, the toxin induced a rapid onset of clinical signs (piloerection, prostration, hypothermia, abdominal breathing, paralysis of the hind limbs, and cyanosis), leading to the death of mice within 30 min. Except for moderate mucosal degeneration in the small intestine recorded at doses of 300 µg kg⁻¹, the toxin did not induce significant morphological changes in the other main organs and tissues, or alterations in blood chemistry parameters. This acute oral toxicity study allowed to calculate an oral LD₅₀ for PnTx-G equal to 208 μg kg⁻¹ (95% confidence limits: 155–281 µg kg⁻¹) and to estimate a provisional NOEL of 120 µg kg⁻¹. Full article

(This article belongs to the Special Issue Potentially Toxic Benthic Microorganisms in Freshwater and Marine Ecosystems)

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22 pages, 6180 KiB

Open AccessEditor’s ChoiceArticle

Ostreopsis cf. ovata (Dinophyceae) Molecular Phylogeny, Morphology, and Detection of Ovatoxins in Strains and Field Samples from Brazil

by Silvia M. Nascimento, Raquel A. F. Neves, Gabriela A. L. De’Carli, Geovanna T. Borsato, Rodrigo A. F. da Silva, Guilherme A. Melo, Agatha M. de Morais, Thais C. Cockell, Santiago Fraga, Adriana D. Menezes-Salgueiro, Luiz L. Mafra, Philipp Hess and Fabiano Salgueiro

Toxins 2020, 12(2), 70; https://doi.org/10.3390/toxins12020070 - 22 Jan 2020

Cited by 19 | Viewed by 3695

Abstract

Recurrent blooms of Ostreopsis cf. ovata have been reported in Brazil and the Mediterranean Sea with associated ecological, and in the latter case, health impacts. Molecular data based on the D1–D3 and D8–D10 regions of the LSU rDNA and ITS loci, and the morphology of O. cf. ovata isolates and field populations from locations along the Brazilian tropical and subtropical coastal regions and three oceanic islands are presented. Additional ITS sequences from three single cells from the tropical coast are provided. Toxin profiles and quantities of PLTX and their analogues; OVTXs; contained in cells from two clonal cultures and two field blooms from Rio de Janeiro were investigated. Morphology was examined using both light and epifluorescence microscopy. Morphometric analysis of different strains and field populations from diverse locations were compared. Molecular analysis showed that six of the seven sequences grouped at the large “Atlantic/Mediterranean/Pacific” sub-clade, while one sequence branched in a sister clade with sequences from Madeira Island and Greece. The toxin profile of strains and bloom field samples from Rio de Janeiro were dominated by OVTX-a and -b, with total cell quotas (31.3 and 39.3 pg cell⁻¹) in the range of that previously reported for strains of O. cf. ovata. Full article

(This article belongs to the Special Issue Potentially Toxic Benthic Microorganisms in Freshwater and Marine Ecosystems)

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23 pages, 1793 KiB

Open AccessEditor’s ChoiceArticle

Intraspecific Variability in the Toxin Production and Toxin Profiles of In Vitro Cultures of Gambierdiscus polynesiensis (Dinophyceae) from French Polynesia

by Sébastien Longo, Manoella Sibat, Jérôme Viallon, Hélène Taiana Darius, Philipp Hess and Mireille Chinain

Toxins 2019, 11(12), 735; https://doi.org/10.3390/toxins11120735 - 17 Dec 2019

Cited by 42 | Viewed by 4928

Abstract

Ciguatera poisoning (CP) is a foodborne disease caused by the consumption of seafood contaminated with ciguatoxins (CTXs) produced by dinoflagellates in the genera Gambierdiscus and Fukuyoa. The toxin production and toxin profiles were explored in four clones of G. polynesiensis originating from different islands in French Polynesia with contrasted CP risk: RIK7 (Mangareva, Gambier), NHA4 (Nuku Hiva, Marquesas), RAI-1 (Raivavae, Australes), and RG92 (Rangiroa, Tuamotu). Productions of CTXs, maitotoxins (MTXs), and gambierone group analogs were examined at exponential and stationary growth phases using the neuroblastoma cell-based assay and liquid chromatography–tandem mass spectrometry. While none of the strains was found to produce known MTX compounds, all strains showed high overall P-CTX production ranging from 1.1 ± 0.1 to 4.6 ± 0.7 pg cell⁻¹. In total, nine P-CTX analogs were detected, depending on strain and growth phase. The production of gambierone, as well as 44-methylgamberione, was also confirmed in G. polynesiensis. This study highlighted: (i) intraspecific variations in toxin production and profiles between clones from distinct geographic origins and (ii) the noticeable increase in toxin production of both CTXs, in particular CTX4A/B, and gambierone group analogs from the exponential to the stationary phase. Full article

(This article belongs to the Special Issue Potentially Toxic Benthic Microorganisms in Freshwater and Marine Ecosystems)

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17 pages, 5539 KiB

Open AccessArticle

Morphology and Phylogenetics of Benthic Prorocentrum Species (Dinophyceae) from Tropical Northwestern Australia

by Arjun Verma, Aniuska Kazandjian, Chowdhury Sarowar, D. Tim Harwood, J. Sam Murray, Insa Pargmann, Mona Hoppenrath and Shauna A. Murray

Toxins 2019, 11(10), 571; https://doi.org/10.3390/toxins11100571 - 30 Sep 2019

Cited by 12 | Viewed by 7075

Abstract

Approximately 70 species of Prorocentrum are known, of which around 30 species are associated with benthic habitats. Some produce okadaic acid (OA), dinophysistoxin (DTX) and their derivatives, which are involved in diarrhetic shellfish poisoning. In this study, we isolated and characterized Prorocentrum concavum and P. malayense from Broome in north Western Australia using light and scanning electron microscopy as well as molecular sequences of large subunit regions of ribosomal DNA, marking the first record of these species from Australian waters. The morphology of the motile cells of P. malayense was similar to P. concavum in the light microscopy, but differed by the smooth thecal surface, the pore pattern and the production of mucous stalk-like structures and a hyaline sheath around the non-motile cells. P. malayense could also be differentiated from other closely related species, P. leve and P. foraminosum, despite the similarity in thecal surface and pore pattern, by its platelet formula and morphologies. We tested the production of OA and DTXs from both species, but found that they did not produce detectable levels of these toxins in the given culturing conditions. This study aids in establishing more effective monitoring of potential harmful algal taxa in Australian waters for aquaculture and recreational purposes. Full article

(This article belongs to the Special Issue Potentially Toxic Benthic Microorganisms in Freshwater and Marine Ecosystems)

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22 pages, 6852 KiB

Open AccessEditor’s ChoiceArticle

Ostreopsis cf. ovata Bloom in Currais, Brazil: Phylogeny, Toxin Profile and Contamination of Mussels and Marine Plastic Litter

by Carlos Eduardo J. A. Tibiriçá, Isabel P. Leite, Talita V. V. Batista, Luciano F. Fernandes, Nicolas Chomérat, Fabienne Herve, Philipp Hess and Luiz L. Mafra

Toxins 2019, 11(8), 446; https://doi.org/10.3390/toxins11080446 - 27 Jul 2019

Cited by 46 | Viewed by 8089

Abstract

Ostreopsis cf. ovata is a toxic marine benthic dinoflagellate responsible for harmful blooms affecting ecosystem and human health, mostly in the Mediterranean Sea. In this study we report the occurrence of a summer O. cf. ovata bloom in Currais, a coastal archipelago located on the subtropical Brazilian coast (~25° S). This bloom was very similar to Mediterranean episodes in many aspects: (a) field-sampled and cultivated O. cf. ovata cells aligned phylogenetically (ITS and LSU regions) along with Mediterranean strains; (b) the bloom occurred at increasing temperature and irradiance, and decreasing wind speed; (c) cell densities reached up to 8.0 × 10⁴ cell cm⁻² on fiberglass screen and 5.6 × 10⁵ cell g⁻¹ fresh weight on seaweeds; (d) and toxin profiles were composed mostly of ovatoxin-a (58%) and ovatoxin-b (32%), up to 35.5 pg PLTX-eq. cell⁻¹ in total. Mussels were contaminated during the bloom with unsafe toxin levels (up to 131 µg PLTX-eq. kg⁻¹). Ostreopsis cells attached to different plastic litter, indicating an alternate route for toxin transfer to marine fauna via ingestion of biofilm-coated plastic debris. Full article

(This article belongs to the Special Issue Potentially Toxic Benthic Microorganisms in Freshwater and Marine Ecosystems)

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17 pages, 2747 KiB

Open AccessEditor’s ChoiceArticle

Ciguatera-Causing Dinoflagellate Gambierdiscus spp. (Dinophyceae) in a Subtropical Region of North Atlantic Ocean (Canary Islands): Morphological Characterization and Biogeography

by Isabel Bravo, Francisco Rodriguez, Isabel Ramilo, Pilar Rial and Santiago Fraga

Toxins 2019, 11(7), 423; https://doi.org/10.3390/toxins11070423 - 19 Jul 2019

Cited by 22 | Viewed by 4818

Abstract

Dinoflagellates belonging to the genus Gambierdiscus produce ciguatoxins (CTXs), which are metabolized in fish to more toxic forms and subsequently cause ciguatera fish poisoning (CFP) in humans. Five species of Gambierdiscus have been described from the Canary Islands, where CTXs in fish have been reported since 2004. Here we present new data on the distribution of Gambierdiscus species in the Canary archipelago and specifically from two islands, La Palma and La Gomera, where the genus had not been previously reported. Gambierdiscus spp. concentrations were low, with maxima of 88 and 29 cells·g⁻¹ wet weight in samples from La Gomera and La Palma, respectively. Molecular analysis (LSUrRNA gene sequences) revealed differences in the species distribution between the two islands: only G. excentricus was detected at La Palma whereas four species, G. australes, G. caribaeus, G. carolinianus, and G. excentricus, were identified from La Gomera. Morphometric analyses of cultured cells of the five Canary Islands species and of field specimens from La Gomera included cell size and a characterization of three thecal arrangement traits: (1) the shape of the 2′ plate, (2) the position of Po in the anterior suture of the 2′ plate, and (3) the length–width relationship of the 2″″ plate. Despite the wide morphological variability within the culture and field samples, the use of two or more variables allowed the discrimination of two species in the La Gomera samples: G. cf. excentricus and G. cf. silvae. A comparison of the molecular data with the morphologically based classification demonstrated important coincidences, such as the dominance of G. excentricus, but also differences in the species composition of Gambierdiscus, as G. caribaeus was detected in the study area only by using molecular methods. Full article

(This article belongs to the Special Issue Potentially Toxic Benthic Microorganisms in Freshwater and Marine Ecosystems)

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27 pages, 7404 KiB

Open AccessArticle

Microcystis Chemotype Diversity in the Alimentary Tract of Bigheaded Carp

by Milán Riba, Attila Kiss-Szikszai, Sándor Gonda, Gergely Boros, Zoltán Vitál, Andrea Kériné Borsodi, Gergely Krett, Gábor Borics, Andrea Zsuzsanna Ujvárosi and Gábor Vasas

Toxins 2019, 11(5), 288; https://doi.org/10.3390/toxins11050288 - 22 May 2019

Cited by 11 | Viewed by 4181

Abstract

Most cyanobacterial organisms included in the genus Microcystis can produce a wide repertoire of secondary metabolites. In the mid-2010s, summer cyanobacterial blooms of Microcystis sp. occurred regularly in Lake Balaton. During this period, we investigated how the alimentary tract of filter-feeding bigheaded carps could deliver different chemotypes of viable cyanobacteria with specific peptide patterns. Twenty-five Microcystis strains were isolated from pelagic plankton samples (14 samples) and the hindguts of bigheaded carp (11 samples), and three bloom samples were collected from the scums of cyanobacterial blooms. An LC-MS/MS-based untargeted approach was used to analyze peptide patterns, which identified 36 anabaenopeptin, 17 microginin, and 13 microcystin variants. Heat map clustering visualization was used to compare the identified chemotypes. A lack of separation was observed in peptide patterns of Microcystis that originated from hindguts, water samples, and bloom-samples. Except for 13 peptides, all other congeners were detected from the viable and cultivated chemotypes of bigheaded carp. This finding suggests that the alimentary tract of bigheaded carps is not simply an extreme habitat, but may also supply the cyanobacterial strains that represent the pelagic chemotypes. Full article

(This article belongs to the Special Issue Potentially Toxic Benthic Microorganisms in Freshwater and Marine Ecosystems)

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15 pages, 1652 KiB

Open AccessArticle

Development and Application of a Quantitative PCR Assay to Assess Genotype Dynamics and Anatoxin Content in Microcoleus autumnalis-Dominated Mats

by Laura T. Kelly, Susanna A. Wood, Tara G. McAllister and Ken G. Ryan

Toxins 2018, 10(11), 431; https://doi.org/10.3390/toxins10110431 - 26 Oct 2018

Cited by 13 | Viewed by 3702

Abstract

Microcoleus is a filamentous cyanobacteria genus with a global distribution. Some species form thick, cohesive mats over large areas of the benthos in rivers and lakes. In New Zealand Microcoleus autumnalis is an anatoxin producer and benthic proliferations are occurring in an increasing number of rivers nationwide. Anatoxin content in M. autumnalis-dominated mats varies spatially and temporally, making understanding and managing proliferations difficult. In this study a M. autumnalis-specific TaqMan probe quantitative PCR (qPCR) assay targeting the anaC gene was developed. The assay was assessed against 26 non-M. autumnalis species. The assay had a detection range over seven orders of magnitude, with a limit of detection of 5.14 × 10⁻⁸ ng μL⁻¹. The anaC assay and a cyanobacterial specific 16S rRNA qPCR were then used to determine toxic genotype proportions in 122 environmental samples collected from 19 sites on 10 rivers in New Zealand. Anatoxin contents of the samples were determined using LC-MS/MS and anatoxin quota per toxic cell calculated. The percentage of toxic cells ranged from 0 to 30.3%, with significant (p < 0.05) differences among rivers. The anatoxin content in mats had a significant relationship with the percentage of toxic cells (R² = 0.38, p < 0.001), indicating that changes in anatoxin content in M. autumnalis-dominated mats are primarily related to the dominance of toxic strains. When applied to more extensive samples sets the assay will enable new insights into how biotic and abiotic parameters influence genotype composition, and if applied to RNA assist in understanding anatoxin production. Full article

(This article belongs to the Special Issue Potentially Toxic Benthic Microorganisms in Freshwater and Marine Ecosystems)

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15 pages, 1440 KiB

Open AccessArticle

Cyanotoxins and Cyanobacteria Cell Accumulations in Drinking Water Treatment Plants with a Low Risk of Bloom Formation at the Source

by Husein Almuhtaram, Yijing Cui, Arash Zamyadi and Ron Hofmann

Toxins 2018, 10(11), 430; https://doi.org/10.3390/toxins10110430 - 26 Oct 2018

Cited by 57 | Viewed by 8572

Abstract

Toxic cyanobacteria have been shown to accumulate in drinking water treatment plants that are susceptible to algal blooms. However, the risk for plants that do not experience algal blooms, but that receive a low influx of cells, is not well known. This study determined the extent of cell accumulation and presence of cyanotoxins across the treatment trains of four plants in the Great Lakes region. Samples were collected for microscopic enumeration and enzyme-linked immunosorbent assay (ELISA) measurements for microcystins, anatoxin-a, saxitoxin, cylindrospermopsin, and β-methylamino-L-alanine (BMAA). Low cell influxes (under 1000 cells/mL) resulted in significant cell accumulations (over 1 × 10⁵ cells/mL) in clarifier sludge and filter backwash samples. Microcystins peaked at 7.2 µg/L in one clarifier sludge sample, exceeding the raw water concentration by a factor of 12. Anatoxin-a was detected in the finished drinking water of one plant at 0.6 µg/L. BMAA may have been detected in three finished water samples, though inconsistencies among the BMAA ELISAs call these results into question. In summary, the results show that plants receiving a low influx of cells can be at risk of toxic cyanobacterial accumulation, and therefore, the absence of a bloom at the source does not indicate the absence of risk. Full article

(This article belongs to the Special Issue Potentially Toxic Benthic Microorganisms in Freshwater and Marine Ecosystems)

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14 pages, 1796 KiB

Open AccessFeature PaperArticle

Spatial and Temporal Variability in the Development and Potential Toxicity of Phormidium Biofilms in the Tarn River, France

by Isidora Echenique-Subiabre, Maxime Tenon, Jean-François Humbert and Catherine Quiblier

Toxins 2018, 10(10), 418; https://doi.org/10.3390/toxins10100418 - 17 Oct 2018

Cited by 12 | Viewed by 3527

Abstract

Proliferation of Phormidium biofilms in rivers is becoming a worldwide sanitation problem for humans and animals, due to the ability of these bacteria to produce anatoxins. To better understand the environmental conditions that favor the development of Phormidium biofilms and the production of anatoxins, we monitored the formation of these biofilms and their toxins for two years in the Tarn River, biofilms from which are known to have caused the deaths of multiple dogs. As previously observed in New Zealand, Phormidium biofilm development occurred in riffle areas. The coverage of these biofilms at the bottom of the river exhibited strong spatial and temporal variations, but was positively correlated with water temperature and depth. Anatoxin-a was detected in less than 50% of the biofilms. The concentrations of these toxins in the biofilms exhibited high spatiotemporal variability, with the highest concentrations being recorded at the end of the summer period at the upstream sampling sites. These findings suggest that the maturity of the biofilms, combined with the local environmental conditions, have an impact on the production of anatoxin, making risk assessment for these benthic proliferations challenging. Full article

(This article belongs to the Special Issue Potentially Toxic Benthic Microorganisms in Freshwater and Marine Ecosystems)

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