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Myriam Bormans
UMR ECOBIO, 6553 CNRS, Université de Rennes 1, Campus de Beaulieu, Rennes, France

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Journal article
Published: 11 March 2021 in Toxicon
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Primary consumers in freshwater ecosystems, such as the zooplankton organism Daphnia magna, are highly affected by cyanobacteria, both as they may use it as a food source but also by cyanobacterial metabolites present in the water. Here, we investigate the impacts of cyanobacterial metabolites focussing on the environmental realistic scenario of the naturally released mixture without crushing cyanobacterial cells or their uptake as food. Therefore, D. magna were exposed to two concentrations of cell free cyanobacterial spent medium from Microcystis aeruginosa PCC 7806 to represent higher and lower ecologically-relevant concentrations of cyanobacterial metabolites. Including microcystin-LR, 11 metabolites have been detected of which 5 were quantified. Hypothesising concentration and time dependent negative impact, survival, gene expression marking digestion and metabolism, oxidative stress response, cell cycle and molting as well as activities of detoxification and antioxidant enzymes were followed for 7 days. D. magna suffered from oxidative stress as both catalase and glutathione S-transferase enzyme activities significantly decreased, suggesting enzyme exhaustibility after 3 and 7 days. Moreover, gene-expressions of the 4 stress markers (glutathione S-transferase, glutathione peroxidase, catalase and thioredoxin) were merely downregulated after 7 days of exposure. Energy allocation (expression of glyceraldehyde-3-phosphate dehydrogenase) was increased after 3 days but decreased as well after 7 days exposure. Cell cycle was impacted time dependently but differently by the two concentrations, along with an increasing downregulation of myosin heavy chain responsible for cell arrangement and muscular movements. Deregulation of nuclear hormone receptor genes indicate that D. magna hormonal steering including molting seemed impaired despite no detection of microviridin J in the extracts. As a consequence of all those responses and presumably of more than investigated molecular and physiological changes, D. magna survival was impaired over time, in a concentration dependent manner. Our results confirm that besides microcystin-LR, other secondary metabolites contribute to negative impact on D. magna survival and stress response.

ACS Style

Gorenka Bojadzija Savic; Hervé Colinet; Myriam Bormans; Christine Edwards; Linda A. Lawton; Enora Briand; Claudia Wiegand. Cell free Microcystis aeruginosa spent medium affects Daphnia magna survival and stress response. Toxicon 2021, 195, 37 -47.

AMA Style

Gorenka Bojadzija Savic, Hervé Colinet, Myriam Bormans, Christine Edwards, Linda A. Lawton, Enora Briand, Claudia Wiegand. Cell free Microcystis aeruginosa spent medium affects Daphnia magna survival and stress response. Toxicon. 2021; 195 ():37-47.

Chicago/Turabian Style

Gorenka Bojadzija Savic; Hervé Colinet; Myriam Bormans; Christine Edwards; Linda A. Lawton; Enora Briand; Claudia Wiegand. 2021. "Cell free Microcystis aeruginosa spent medium affects Daphnia magna survival and stress response." Toxicon 195, no. : 37-47.

Journal article
Published: 25 April 2020 in Harmful Algae
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Due to eutrophication, freshwater ecosystems frequently experience cyanobacterial blooms, many of which produce bioactive metabolites that can affect vertebrates and invertebrates life traits. Zooplankton are able to develop tolerance as a physiological response to cyanobacteria and their bioactive compounds, however, this comes with energetic cost that in turn influence Daphnia life traits and may impair populations. Vice versa, it has been suggested that Daphnia are able to reduce cyanobacterial dominance until a certain cyanobacterial density; it remains unclear whether Daphnia metabolites alone influence the physiological state and bioactive metabolites production of cyanobacteria. Hence, this study investigates mutual physiological reactions of toxic Microcystis aeruginosa PCC7806 and Daphnia magna. We hypothesize that a) the presence of D. magna will negatively affect growth, increase stress response and metabolites production in M. aeruginosa PCC7806 and b) the presence of M. aeruginosa PCC7806 will negatively affect physiological responses and life traits in D. magna. In order to test these hypotheses experiments were conducted in a specially designed co-culture chamber that allows exchange of the metabolites without direct contact. A clear mutual impact was evidenced. Cyanobacterial metabolites reduced survival of D. magna and decreased oxidative stress enzyme activity. Simultaneously, presence of D. magna did not affect photosynthetic activity. However, ROS increase and tendencies in cell density decrease were observed on the same day, suggesting possible energy allocation towards anti-oxidative stress enzymes, or other protection mechanisms against Daphnia infochemicals, as the strain managed to recover. Elevated concentration of intracellular and overall extracellular microcystin MC-LR, as well as intracellular concentrations of aerucyclamide A and D in the presence of Daphnia, indicating a potential protective or anti-grazing function. However, more research is needed to confirm these findings.

ACS Style

Gorenka Bojadzija Savic; Myriam Bormans; Christine Edwards; Linda Lawton; Enora Briand; Claudia Wiegand. Cross talk: Two way allelopathic interactions between toxic Microcystis and Daphnia. Harmful Algae 2020, 94, 101803 .

AMA Style

Gorenka Bojadzija Savic, Myriam Bormans, Christine Edwards, Linda Lawton, Enora Briand, Claudia Wiegand. Cross talk: Two way allelopathic interactions between toxic Microcystis and Daphnia. Harmful Algae. 2020; 94 ():101803.

Chicago/Turabian Style

Gorenka Bojadzija Savic; Myriam Bormans; Christine Edwards; Linda Lawton; Enora Briand; Claudia Wiegand. 2020. "Cross talk: Two way allelopathic interactions between toxic Microcystis and Daphnia." Harmful Algae 94, no. : 101803.

Journal article
Published: 27 March 2020 in Biodiversity Data Journal
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The Biological Field Station of Paimpont (Station Biologique de Paimpont, SBP), owned by the University of Rennes and located in the Brocéliande Forest of Brittany (France), has been hosting student scientific research and field trips during the last 60 years. The study area of the SBP is a landscape mosaic of 17 ha composed of gorse moors, forests, prairies, ponds and creeks. Land use has evolved over time. Historical surveys by students and researchers focused on insects and birds. With this study, we aimed to increase the range of taxa observations, document changes in species composition and landscape and provide a basis for interdisciplinary research perspectives. We gathered historical data, implemented an all-taxon biodiversity inventory (ATBI) in different habitats of the SBP study area, measured abiotic factors in the air, water and soil and performed a photographical landscape observation during the BioBlitz held in July 2017. During the 24 h BioBlitz, organised by the SBP and the EcoBio lab from the University of Rennes and the French National Center of Scientific Research (CNRS), different habitats were individually sampled. Seventy-seven experts, accompanied by 120 citizens and 12 young people participating in the European Volunteer Service, observed, identified and databased 660 species covering 5 kingdoms, 8 phyla, 21 classes, 90 orders and 247 families. In total, there were 1819 occurrences including records identified to higher taxon ranks, thereby adding one more kingdom and four more phyla. Historical data collection resulted in 1176 species and 4270 occurrences databased. We also recorded 13 climatic parameters, 10 soil parameters and 18 water parameters during the BioBlitz. Current habitats were mapped and socio-ecological landscape changes were assessed with a diachronic approach using 32 historical photographs and historical maps. The coupling of historical biodiversity data with new biotic and abiotic data and a photographic comparison of landscape changes allows an integrative understanding of how the SBP changed from agriculturally-used land to a managed natural area within the last 60 years. Hence, this BioBlitz represents an important holistic sampling of biodiversity for studies on trophic webs or on trophic interactions or on very diverse, but connected, habitats. The integration of social, biotic and abiotic data opens innovative research opportunities on the evolution of socio-ecosystems and landscapes.

ACS Style

Annegret Nicolai; Muriel Guernion; Sarah Guillocheau; Kevin Hoeffner; Pascaline Le Gouar; Nelly Ménard; Christophe Piscart; Dominique Vallet; Morgane Hervé; Elora Benezeth; Hughes Chedanne; Jérémie Blémus; Philippe Vernon; Daniel Cylly; Hoël Hotte; Grégoire Loïs; Barbara Mai; Grégoire Perez; Tiphaine Ouisse; Cécile Monard; Claudia Wiegand; Jean-Pierre Caudal; Alain Butet; Maxime Dahirel; Lou Barbe; Manon Balbi; Valérie Briand; Myriam Bormans; Maryvonne Charrier; Guillaume Bouger; Vincent Jung; Cécile Le Lann; Alexandrine Pannard; Julien Petillon; Yann Rantier; Dominique Marguerie; Kevin Tougeron; Pierre Devogel; Sébastien Dugravot; Thomas Dubos; Maël Garrin; Mathurin Carnet; Clément Gouraud; Audrey Chambet; Joël Esnault; Maxime Poupelin; Erik Welk; Astrid Bütof; Glenn Dubois; Guillaume Humbert; Odile Marie-Réau; Olivier Norvez; Gaëlle Richard; Benoît Froger; Céline Rochais; Martin Potthoff; Khaoula Ayati; Alain Bellido; Alain Rissel; Mathieu Santonja; Jacques-Olivier Farcy; Eric Collias; Lina Sene; Daniel Cluzeau; Régis Supper. Transdisciplinary Bioblitz: Rapid biotic and abiotic inventory allows studying environmental changes over 60 years at the Biological Field Station of Paimpont (Brittany, France) and opens new interdisciplinary research opportunities. Biodiversity Data Journal 2020, 8, e50451 .

AMA Style

Annegret Nicolai, Muriel Guernion, Sarah Guillocheau, Kevin Hoeffner, Pascaline Le Gouar, Nelly Ménard, Christophe Piscart, Dominique Vallet, Morgane Hervé, Elora Benezeth, Hughes Chedanne, Jérémie Blémus, Philippe Vernon, Daniel Cylly, Hoël Hotte, Grégoire Loïs, Barbara Mai, Grégoire Perez, Tiphaine Ouisse, Cécile Monard, Claudia Wiegand, Jean-Pierre Caudal, Alain Butet, Maxime Dahirel, Lou Barbe, Manon Balbi, Valérie Briand, Myriam Bormans, Maryvonne Charrier, Guillaume Bouger, Vincent Jung, Cécile Le Lann, Alexandrine Pannard, Julien Petillon, Yann Rantier, Dominique Marguerie, Kevin Tougeron, Pierre Devogel, Sébastien Dugravot, Thomas Dubos, Maël Garrin, Mathurin Carnet, Clément Gouraud, Audrey Chambet, Joël Esnault, Maxime Poupelin, Erik Welk, Astrid Bütof, Glenn Dubois, Guillaume Humbert, Odile Marie-Réau, Olivier Norvez, Gaëlle Richard, Benoît Froger, Céline Rochais, Martin Potthoff, Khaoula Ayati, Alain Bellido, Alain Rissel, Mathieu Santonja, Jacques-Olivier Farcy, Eric Collias, Lina Sene, Daniel Cluzeau, Régis Supper. Transdisciplinary Bioblitz: Rapid biotic and abiotic inventory allows studying environmental changes over 60 years at the Biological Field Station of Paimpont (Brittany, France) and opens new interdisciplinary research opportunities. Biodiversity Data Journal. 2020; 8 ():e50451.

Chicago/Turabian Style

Annegret Nicolai; Muriel Guernion; Sarah Guillocheau; Kevin Hoeffner; Pascaline Le Gouar; Nelly Ménard; Christophe Piscart; Dominique Vallet; Morgane Hervé; Elora Benezeth; Hughes Chedanne; Jérémie Blémus; Philippe Vernon; Daniel Cylly; Hoël Hotte; Grégoire Loïs; Barbara Mai; Grégoire Perez; Tiphaine Ouisse; Cécile Monard; Claudia Wiegand; Jean-Pierre Caudal; Alain Butet; Maxime Dahirel; Lou Barbe; Manon Balbi; Valérie Briand; Myriam Bormans; Maryvonne Charrier; Guillaume Bouger; Vincent Jung; Cécile Le Lann; Alexandrine Pannard; Julien Petillon; Yann Rantier; Dominique Marguerie; Kevin Tougeron; Pierre Devogel; Sébastien Dugravot; Thomas Dubos; Maël Garrin; Mathurin Carnet; Clément Gouraud; Audrey Chambet; Joël Esnault; Maxime Poupelin; Erik Welk; Astrid Bütof; Glenn Dubois; Guillaume Humbert; Odile Marie-Réau; Olivier Norvez; Gaëlle Richard; Benoît Froger; Céline Rochais; Martin Potthoff; Khaoula Ayati; Alain Bellido; Alain Rissel; Mathieu Santonja; Jacques-Olivier Farcy; Eric Collias; Lina Sene; Daniel Cluzeau; Régis Supper. 2020. "Transdisciplinary Bioblitz: Rapid biotic and abiotic inventory allows studying environmental changes over 60 years at the Biological Field Station of Paimpont (Brittany, France) and opens new interdisciplinary research opportunities." Biodiversity Data Journal 8, no. : e50451.

Journal article
Published: 18 March 2020 in Toxins
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The transfer of Microcystis aeruginosa from freshwater to estuaries has been described worldwide and salinity is reported as the main factor controlling the expansion of M. aeruginosa to coastal environments. Analyzing the expression levels of targeted genes and employing both targeted and non-targeted metabolomic approaches, this study investigated the effect of a sudden salt increase on the physiological and metabolic responses of two toxic M. aeruginosa strains separately isolated from fresh and brackish waters, respectively, PCC 7820 and 7806. Supported by differences in gene expressions and metabolic profiles, salt tolerance was found to be strain specific. An increase in salinity decreased the growth of M. aeruginosa with a lesser impact on the brackish strain. The production of intracellular microcystin variants in response to salt stress correlated well to the growth rate for both strains. Furthermore, the release of microcystins into the surrounding medium only occurred at the highest salinity treatment when cell lysis occurred. This study suggests that the physiological responses of M. aeruginosa involve the accumulation of common metabolites but that the intraspecific salt tolerance is based on the accumulation of specific metabolites. While one of these was determined to be sucrose, many others remain to be identified. Taken together, these results provide evidence that M. aeruginosa is relatively salt tolerant in the mesohaline zone and microcystin (MC) release only occurs when the capacity of the cells to deal with salt increase is exceeded.

ACS Style

Maxime Georges Des Aulnois; Damien Réveillon; Elise Robert; Amandine Caruana; Enora Briand; Arthur Guljamow; Elke Dittmann; Zouher Amzil; Myriam Bormans. Salt Shock Responses of Microcystis Revealed through Physiological, Transcript, and Metabolomic Analyses. Toxins 2020, 12, 192 .

AMA Style

Maxime Georges Des Aulnois, Damien Réveillon, Elise Robert, Amandine Caruana, Enora Briand, Arthur Guljamow, Elke Dittmann, Zouher Amzil, Myriam Bormans. Salt Shock Responses of Microcystis Revealed through Physiological, Transcript, and Metabolomic Analyses. Toxins. 2020; 12 (3):192.

Chicago/Turabian Style

Maxime Georges Des Aulnois; Damien Réveillon; Elise Robert; Amandine Caruana; Enora Briand; Arthur Guljamow; Elke Dittmann; Zouher Amzil; Myriam Bormans. 2020. "Salt Shock Responses of Microcystis Revealed through Physiological, Transcript, and Metabolomic Analyses." Toxins 12, no. 3: 192.

Article
Published: 04 March 2020 in Aquatic Ecology
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While transfer of freshwater cyanobacteria to estuaries has been observed worldwide, the associated transfer of cyanotoxins is less often reported, in particular the sediment contribution. During fall 2018, we monitored the co-occurrence of cyanobacteria and microcystin (MC) in both the water column and in surface sediments at five stations along a river continuum, from a freshwater reservoir to the coastal area in Brittany, France. Cyanobacteria dominated the phytoplankton community in the water column with high densities at the freshwater sites. Microcystis cells and intracellular MC transfer to estuarine and marine sites were observed with decreasing concentrations in accordance with flow dilution. Extracellular MC showed the opposite trend and increased from upstream to downstream in accordance with the lysing of the cells at elevated salinities. Surface sediment samples contained high densities of colonial Microcystis in freshwater and with decreasing concentrations along the salinity gradient, similar to cells concentrations in the water column. Intracellular MC was detected in sediment at all sites except at the marine outlet suggesting the survival of intact cells. Extracellular MC concentrations in sediment were up to five times higher than intracellular concentrations suggesting incomplete MC degradation. mcyB genes were present at all sites, while mcyA genes were absent at the marine outlet suggesting the presence of toxic strains along the estuary. The high densities of intact colonies of potentially toxic Microcystis in the estuarine sediment strongly suggest that sediments can act as an inoculum of cyanobacteria and cyanotoxins in estuaries.

ACS Style

Myriam Bormans; Véronique Savar; Benjamin Legrand; Emilien Mineaud; Elise Robert; Emilie Lance; Zouher Amzil. Cyanobacteria and cyanotoxins in estuarine water and sediment. Aquatic Ecology 2020, 54, 625 -640.

AMA Style

Myriam Bormans, Véronique Savar, Benjamin Legrand, Emilien Mineaud, Elise Robert, Emilie Lance, Zouher Amzil. Cyanobacteria and cyanotoxins in estuarine water and sediment. Aquatic Ecology. 2020; 54 (2):625-640.

Chicago/Turabian Style

Myriam Bormans; Véronique Savar; Benjamin Legrand; Emilien Mineaud; Elise Robert; Emilie Lance; Zouher Amzil. 2020. "Cyanobacteria and cyanotoxins in estuarine water and sediment." Aquatic Ecology 54, no. 2: 625-640.

Journal article
Published: 19 July 2019 in Toxins
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While the intracellular function of many toxic and bioactive cyanobacterial metabolites is not yet known, microcystins have been suggested to have a protective role in the cyanobacterial metabolism, giving advantage to toxic over nontoxic strains under stress conditions. The zooplankton grazer Daphnia reduce cyanobacterial dominance until a certain density, which may be supported by Daphnia exudates, affecting the cyanobacterial physiological state and metabolites' production. Therefore, we hypothesized that D. magna spent medium will impact the production of cyanobacterial bioactive metabolites and affect cyanobacterial photosynthetic activity in the nontoxic, but not the toxic strain. Microcystin (MC-LR and des-MC-LR) producing M. aeruginosa PCC7806 and its non-microcystin producing mutant were exposed to spent media of different D. magna densities and culture durations. D. magna spent medium of the highest density (200/L) cultivated for the shortest time (24 h) provoked the strongest effect. D.magna spent medium negatively impacted the photosynthetic activity of M. aeruginosa PCC7806, as well as the dynamics of intracellular and extracellular cyanobacterial metabolites, while its mutant was unaffected. In the presence of Daphnia medium, microcystin does not appear to have a protective role for the strain. On the contrary, extracellular cyanopeptolin A increased in M. aeruginosa PCC7806 although the potential anti-grazing role of this compound would require further studies.

ACS Style

Gorenka Bojadzija Savic; Christine Edwards; Enora Briand; Linda Lawton; Claudia Wiegand; Myriam Bormans. Daphnia magna Exudates Impact Physiological and Metabolic Changes in Microcystis aeruginosa. Toxins 2019, 11, 421 .

AMA Style

Gorenka Bojadzija Savic, Christine Edwards, Enora Briand, Linda Lawton, Claudia Wiegand, Myriam Bormans. Daphnia magna Exudates Impact Physiological and Metabolic Changes in Microcystis aeruginosa. Toxins. 2019; 11 (7):421.

Chicago/Turabian Style

Gorenka Bojadzija Savic; Christine Edwards; Enora Briand; Linda Lawton; Claudia Wiegand; Myriam Bormans. 2019. "Daphnia magna Exudates Impact Physiological and Metabolic Changes in Microcystis aeruginosa." Toxins 11, no. 7: 421.

Journal article
Published: 01 July 2019 in Harmful Algae
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The frequency of cyanobacterial proliferations in fresh waters is increasing worldwide and the presence of associated cyanotoxins represent a threat for ecosystems and human health. While the occurrence of microcystin (MC), the most widespread cyanotoxin, is well documented in freshwaters, only few studies have examined its occurrence in estuarine waters. In this study we evaluated the transfer of cyanobacteria and cyanotoxins along a river continuum from a freshwater reservoir through an interconnecting estuary to the coastal area in Brittany, France. We sampled regularly over 2 years at 5 stations along the river continuum and analysed for phytoplankton and cyanotoxins, together with physico-chemical parameters. Results show that cyanobacteria dominated the phytoplanktonic community with high densities (up to 2 × 106 cells mL-1) at the freshwater sites during the summer and autumn periods of both years, with a cell transfer to estuarine (up to 105 cells mL-1) and marine (2 × 103 cells mL-1) sites. While the temporal variation in cyanobacterial densities was mainly associated with temperature, spatial variation was due to salinity while nutrients were non-limiting for cyanobacterial growth. Cyanobacterial biomass was dominated by several species of Microcystis that survived intermediate salinities. Intracellular MCs were detected in all the freshwater samples with concentrations up to 60 μg L-1, and more intermittently with concentrations up to 1.15 μg L-1, at the most upstream estuarine site. Intracellular MC was only sporadically detected and in low concentration at the most downstream estuarine site and at the marine outlet (respectively <0.14 μg L-1 and <0.03 μg L-1). Different MC variants were detected with dominance of MC-LR, RR and YR and that dominance was conserved along the salinity gradient. Extracellular MC contribution to total MC was higher at the downstream sites in accordance with the lysing of the cells at elevated salinities. No nodularin (NOD) was detected in the particulate samples or in the filtrates.

ACS Style

Myriam Bormans; Zouher Amzil; Emilien Mineaud; Luc Brient; Véronique Savar; Elise Robert; Emilie Lance. Demonstrated transfer of cyanobacteria and cyanotoxins along a freshwater-marine continuum in France. Harmful Algae 2019, 87, 101639 .

AMA Style

Myriam Bormans, Zouher Amzil, Emilien Mineaud, Luc Brient, Véronique Savar, Elise Robert, Emilie Lance. Demonstrated transfer of cyanobacteria and cyanotoxins along a freshwater-marine continuum in France. Harmful Algae. 2019; 87 ():101639.

Chicago/Turabian Style

Myriam Bormans; Zouher Amzil; Emilien Mineaud; Luc Brient; Véronique Savar; Elise Robert; Emilie Lance. 2019. "Demonstrated transfer of cyanobacteria and cyanotoxins along a freshwater-marine continuum in France." Harmful Algae 87, no. : 101639.

Original articles
Published: 02 January 2018 in Inland Waters
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Phytoplankton community structure and their abiotic drivers are seldom studied in quarry lakes. We monitored the phytoplankton and physical and chemical conditions of a deep quarry lake for more than a year. The lake was meromictic and phosphorus concentrations remained low year-round. The phytoplankton community was dominated by a small Cosmarium species, identified by molecular techniques, which persisted throughout the year. Laboratory experiments were additionally performed to test which abiotic factors control the phytoplankton community of the lake: nutrients, water temperature, or their interaction. An increase of phosphorus alone increased biomass and changed the community structure, selecting low temperature adapted species, while higher temperature alone and increase in nitrates alone had no effect. Higher temperature associated with nutrient input increased biomass and led to a third community structure dominated by fast growing species with low sedimentation loss. Cosmarium sp. dominated treatments without phosphorus inputs at all temperatures but was easily outcompeted in phosphorus-replete conditions. The thermo-tolerance of Cosmarium sp., associated with a high affinity for phosphorus and low sinking losses, allows this species to dominate in situ year-round. Results from both in situ and laboratory experiments indicated that phosphorus exerts a stronger control than temperature on the phytoplankton community of the quarry lake during the entire year, similar to natural lakes.

ACS Style

A. Pannard; A. Guislain; M. Chorin; S. Mahé; G. Bouger; A. Crave; B. Le Rouzic; M. Bormans. Phosphorus more than temperature controls the phytoplankton community in a deep quarry lake: a combined field and laboratory approach. Inland Waters 2018, 8, 22 -35.

AMA Style

A. Pannard, A. Guislain, M. Chorin, S. Mahé, G. Bouger, A. Crave, B. Le Rouzic, M. Bormans. Phosphorus more than temperature controls the phytoplankton community in a deep quarry lake: a combined field and laboratory approach. Inland Waters. 2018; 8 (1):22-35.

Chicago/Turabian Style

A. Pannard; A. Guislain; M. Chorin; S. Mahé; G. Bouger; A. Crave; B. Le Rouzic; M. Bormans. 2018. "Phosphorus more than temperature controls the phytoplankton community in a deep quarry lake: a combined field and laboratory approach." Inland Waters 8, no. 1: 22-35.

Methods article
Published: 25 July 2017 in Frontiers in Environmental Science
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Microcystin (MC) is a common and widespread toxin which represents a health hazard to humans and animals. MC toxin concentrations are monitored by various direct or proxy techniques (HPLC, LC-MS/MS, ELISA, PPIA), however, these techniques do not discriminate producing species from non-producing ones. In order to simultaneously provide the identity and activity of cyanotoxin producing species in freshwater lakes, we applied simple, and fully detailed, whole cell fluorescent in situ hybridization enhanced by tyramid signal amplification (TSA-FISH). DNA oligonucleotide probes MICR3 and MCYA were targeting 16S rRNA and mcyA-mRNA, respectively. The mcyA gene is coding for the MC synthetase enzyme involved in MC synthesis. Controls were acquired with the general eubacterial 16S rRNA probe EUB338, for TSA-FISH assay, and standard HPLC and LC-MS/MS as standard methods for the measurements of MC concentration. Results obtained from monoclonal strains and natural samples demonstrated a specific identification of Microcystis species and were able to discriminate MC producing from non-producing ones. In addition, the MCYA probe allowed the specific detection of MC-synthetase mRNA within Planktothrix isothrix (Oscillatoriale) filaments. Two kinds of mcyA-mRNA labeling were observed in these cells, spots like and plasmid like, which illustrates the well-known plasticity of microbial genome to adapt to environmental stresses. We demonstrated that a simple TSA-FISH assay allows acquiring rapidly dual information of the presence and abundance of potentially toxic species, while identifying species actively producing MC-synthetase mRNA, a proxy of MC toxin. This technique has the potential to be developed into an effective environmental monitoring tool. In addition, detail visualization of cellular mRNAs is powerful for the acquisition of ecological and biomolecular studies of toxic cyanobacteria.

ACS Style

Luc Brient; Nihel Ben Gamra; Marine Periot; Marie Roumagnac; Perrine Zeller; Myriam Bormans; Annick Méjean; Olivier Ploux; Isabelle C. Biegala. Rapid Characterization of Microcystin-Producing Cyanobacteria in Freshwater Lakes by TSA-FISH (Tyramid Signal Amplification-Fluorescent In Situ Hybridization). Frontiers in Environmental Science 2017, 5, 1 .

AMA Style

Luc Brient, Nihel Ben Gamra, Marine Periot, Marie Roumagnac, Perrine Zeller, Myriam Bormans, Annick Méjean, Olivier Ploux, Isabelle C. Biegala. Rapid Characterization of Microcystin-Producing Cyanobacteria in Freshwater Lakes by TSA-FISH (Tyramid Signal Amplification-Fluorescent In Situ Hybridization). Frontiers in Environmental Science. 2017; 5 ():1.

Chicago/Turabian Style

Luc Brient; Nihel Ben Gamra; Marine Periot; Marie Roumagnac; Perrine Zeller; Myriam Bormans; Annick Méjean; Olivier Ploux; Isabelle C. Biegala. 2017. "Rapid Characterization of Microcystin-Producing Cyanobacteria in Freshwater Lakes by TSA-FISH (Tyramid Signal Amplification-Fluorescent In Situ Hybridization)." Frontiers in Environmental Science 5, no. : 1.

Article
Published: 30 June 2017 in Environmental Monitoring and Assessment
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Blooms of toxic cyanobacteria in Algerian reservoirs represent a potential health problem, mainly from drinking water that supplies the local population of Ain Zada (Bordj Bou Arreridj). The objective of this study is to monitor, detect, and identify the existence of cyanobacteria and microcystins during blooming times. Samples were taken in 2013 from eight stations. The results show that three potentially toxic cyanobacterial genera with the species Planktothrix agardhii were dominant. Cyanobacterial biomass, phycocyanin (PC) concentrations, and microcystin (MC) concentrations were high in the surface layer and at 14 m depth; these values were also high in the treated water. On 11 May 2013, MC concentrations were 6.3 μg/L in MC-LR equivalent in the drinking water. This study shows for the first time the presence of cyanotoxins in raw and treated waters, highlighting that regular monitoring of cyanobacteria and cyanotoxins must be undertaken to avoid potential health problems.

ACS Style

Amel Saoudi; Luc Brient; Sabrine Boucetta; Rachid Ouzrout; Myriam Bormans; Mourad Bensouilah. Management of toxic cyanobacteria for drinking water production of Ain Zada Dam. Environmental Monitoring and Assessment 2017, 189, 361 -361.

AMA Style

Amel Saoudi, Luc Brient, Sabrine Boucetta, Rachid Ouzrout, Myriam Bormans, Mourad Bensouilah. Management of toxic cyanobacteria for drinking water production of Ain Zada Dam. Environmental Monitoring and Assessment. 2017; 189 (7):361-361.

Chicago/Turabian Style

Amel Saoudi; Luc Brient; Sabrine Boucetta; Rachid Ouzrout; Myriam Bormans; Mourad Bensouilah. 2017. "Management of toxic cyanobacteria for drinking water production of Ain Zada Dam." Environmental Monitoring and Assessment 189, no. 7: 361-361.

Journal article
Published: 01 June 2017 in Harmful Algae
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International audienceBenthic cyanobacteria in rivers produce cyanotoxins and affect aquatic food webs, but knowledge of their ecology lags behind planktonic cyanobacteria. The buoyancy of benthic Anabaena spp. mats was studied to understand implications for Anabaena dispersal in the Eel River, California. Field experiments were used to investigate the effects of oxygen bubble production and dissolution on the buoyancy of Anabaena dominated benthic mats in response to light exposure. Samples of Anabaena dominated mats were harvested from the South Fork Eel River and placed in settling columns to measure floating and sinking velocities, or deployed into in situ ambient and low light treatments to measure the effect of light on flotation. Floating and sinking occurred within minutes and were driven by oxygen bubbles produced during photosynthesis, rather than intracellular changes in carbohydrates or gas vesicles. Light experiment results showed that in a natural ambient light regime, mats remained floating for at least 4days, while in low light mats begin to sink in <24h. Floating Anabaena samples were collected from five sites in the watershed and found to contain the cyanotoxins anatoxin-a and microcystin, with higher concentrations of anatoxin-a (median 560, max 30,693ng/gDW) than microcystin (median 30, max 37ng/gDW). The ability of Anabaena mats to maintain their buoyancy will markedly increase their downstream dispersal distances. Increased buoyancy also allows toxin-containing mats to collect along shorelines, increasing threats to human and animal public health

ACS Style

Keith Bouma-Gregson; Mary E. Power; Myriam Bormans. Rise and fall of toxic benthic freshwater cyanobacteria (Anabaena spp.) in the Eel river: Buoyancy and dispersal. Harmful Algae 2017, 66, 79 -87.

AMA Style

Keith Bouma-Gregson, Mary E. Power, Myriam Bormans. Rise and fall of toxic benthic freshwater cyanobacteria (Anabaena spp.) in the Eel river: Buoyancy and dispersal. Harmful Algae. 2017; 66 ():79-87.

Chicago/Turabian Style

Keith Bouma-Gregson; Mary E. Power; Myriam Bormans. 2017. "Rise and fall of toxic benthic freshwater cyanobacteria (Anabaena spp.) in the Eel river: Buoyancy and dispersal." Harmful Algae 66, no. : 79-87.

Erratum
Published: 01 October 2016 in Aquatic Ecology
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ACS Style

Bastiaan W. Ibelings; Jutta Fastner; Myriam Bormans; Petra M. Visser. Erratum to: Cyanobacterial blooms. Ecology, prevention, mitigation and control: Editorial to a CYANOCOST Special Issue. Aquatic Ecology 2016, 50, 735 -735.

AMA Style

Bastiaan W. Ibelings, Jutta Fastner, Myriam Bormans, Petra M. Visser. Erratum to: Cyanobacterial blooms. Ecology, prevention, mitigation and control: Editorial to a CYANOCOST Special Issue. Aquatic Ecology. 2016; 50 (4):735-735.

Chicago/Turabian Style

Bastiaan W. Ibelings; Jutta Fastner; Myriam Bormans; Petra M. Visser. 2016. "Erratum to: Cyanobacterial blooms. Ecology, prevention, mitigation and control: Editorial to a CYANOCOST Special Issue." Aquatic Ecology 50, no. 4: 735-735.

Article
Published: 25 August 2016 in Aquatic Ecology
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This is the Editorial to a Special Issue entitled “Cyanobacterial blooms. Ecology, prevention, mitigation and control”. The Special Issue is a product of a European COST Action, CYANOCOST. In this Special Issue, contributions describe methods currently available for the management of cyanobacterial blooms, a key issue threatening the ecological functioning of lakes and the ecosystem services they provide . Contributions start with a section on the prevention of blooms, through the restriction of nutrient availability for cyanobacterial development at three levels: (1) in the catchment, (2) at the inflow to the lake and (3) in-lake methods, including nutrient release from the sediment. Then follows a section on control of blooms where blooms could be formed in the lake, but the chosen treatment restricts cyanobacterial growth to a level where risks and negative effects are minimal, e.g., artificial mixing, flushing or biomanipulation. The Special Issue continues with contributions on mitigation where blooms do develop, but physical and chemical methods mitigate the negative effects. For effective control key traits of the dominant cyanobacteria, characteristics of the lake system and an adequate design of the control method must come together. Each contribution answers questions like: what is the proposed or proven working mechanism of a given method? What have been the successes and failures? What are the reasons for success or failure? How is success linked to characteristics of the waterbody being treated? The Special Issue is concluded with contributions aiming at social and political aspects of bloom management .

ACS Style

Bastiaan W. Ibelings; Jutta Fastner; Myriam Bormans; Petra M. Visser. Cyanobacterial blooms. Ecology, prevention, mitigation and control: Editorial to a CYANOCOST Special Issue. Aquatic Ecology 2016, 50, 327 -331.

AMA Style

Bastiaan W. Ibelings, Jutta Fastner, Myriam Bormans, Petra M. Visser. Cyanobacterial blooms. Ecology, prevention, mitigation and control: Editorial to a CYANOCOST Special Issue. Aquatic Ecology. 2016; 50 (3):327-331.

Chicago/Turabian Style

Bastiaan W. Ibelings; Jutta Fastner; Myriam Bormans; Petra M. Visser. 2016. "Cyanobacterial blooms. Ecology, prevention, mitigation and control: Editorial to a CYANOCOST Special Issue." Aquatic Ecology 50, no. 3: 327-331.

Review
Published: 20 August 2016 in Aquatic Ecology
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Nuisance, toxic cyanobacterial blooms are a persistent and globally expanding problem. Prevention of blooms requires that external and internal sources of nutrients are managed to levels where development of cyanobacterial blooms is restricted. Control of blooms, in which their presence is reduced to a level where they no longer pose a risk through additional measures such as biomanipulation or artificial mixing, demands that three elements come together: (1) understanding of the key ecological traits of the dominant cyanobacteria taxa, (2) system analysis of the lake, in particular its morphometry, water and nutrient balance, (3) adequate design and execution of the management methods of choice. All three elements are important for choosing effective management interventions and predicting their outcome. Mitigation of blooms reduces the risks and harmful effects of blooms if they cannot be prevented or sufficiently controlled, methods such as harvesting of surface scums or application of cyanocides may be used in those cases where water quality improvement is urgent. Ultimately, managing cyanobacterial blooms is most effective in the context of developing a Water Safety Plan. This is a risk assessment and management approach developed by the World Health Organization and provides a platform for bringing together the stakeholders who have a say about activities in the catchment causing eutrophication. Together, they can develop and implement control measures in the chain from catchment to drinking-water offtake which effectively mitigate eutrophication and thus protect humans and the lake ecosystem services they rely on from effects of toxic cyanobacteria.

ACS Style

Bastiaan W. Ibelings; Myriam Bormans; Jutta Fastner; Petra M. Visser. CYANOCOST special issue on cyanobacterial blooms: synopsis—a critical review of the management options for their prevention, control and mitigation. Aquatic Ecology 2016, 50, 595 -605.

AMA Style

Bastiaan W. Ibelings, Myriam Bormans, Jutta Fastner, Petra M. Visser. CYANOCOST special issue on cyanobacterial blooms: synopsis—a critical review of the management options for their prevention, control and mitigation. Aquatic Ecology. 2016; 50 (3):595-605.

Chicago/Turabian Style

Bastiaan W. Ibelings; Myriam Bormans; Jutta Fastner; Petra M. Visser. 2016. "CYANOCOST special issue on cyanobacterial blooms: synopsis—a critical review of the management options for their prevention, control and mitigation." Aquatic Ecology 50, no. 3: 595-605.

Journal article
Published: 01 August 2016 in Aquatic Toxicology
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Freshwater gastropods are increasingly exposed to multiple stressors in the field such as the herbicide glyphosate in Roundup formulations and cyanobacterial blooms either producing or not producing microcystins (MCs), potentially leading to interacting effects. Here, the responses of Lymnaea stagnalis to a 21-day exposure to non-MC or MC-producing (33 μg L−1) Planktothrix agardhii alone or in combination with the commercial formulation RoundUp® Flash at a concentration of 1 μg L−1 glyphosate, followed by 14 days of depuration, were studied via i) accumulation of free and bound MCs in tissues, and ii) activities of anti-oxidant (catalase CAT) and biotransformation (glutathione-S-transferase GST) enzymes. During the intoxication, the cyanobacterial exposure induced an early increase of CAT activity, independently of the MC content, probably related to the production of secondary cyanobacterial metabolites. The GST activity was induced by RoundUp® Flash alone or in combination with non MC-producing cyanobacteria, but was inhibited by MC-producing cyanobacteria with or without RoundUp® Flash. Moreover, MC accumulation in L. stagnalis was 3.2 times increased when snails were concomitantly exposed to MC-producing cyanobacteria with RoundUp®, suggesting interacting effects of MCs on biotransformation processes. The potent inhibition of detoxication systems by MCs and RoundUp® Flash was reversible during the depuration, during which CAT and GST activities were significantly higher in snails previously exposed to MC-producing cyanobacteria with or without RoundUp® Flash than in other conditions, probably related to the oxidative stress caused by accumulated MCs remaining in tissues.

ACS Style

Emilie Lance; Julia Desprat; Bente Frost Holbech; Claudia Gérard; Myriam Bormans; Linda A. Lawton; Christine Edwards; Claudia Wiegand. Accumulation and detoxication responses of the gastropod Lymnaea stagnalis to single and combined exposures to natural (cyanobacteria) and anthropogenic (the herbicide RoundUp® Flash) stressors. Aquatic Toxicology 2016, 177, 116 -124.

AMA Style

Emilie Lance, Julia Desprat, Bente Frost Holbech, Claudia Gérard, Myriam Bormans, Linda A. Lawton, Christine Edwards, Claudia Wiegand. Accumulation and detoxication responses of the gastropod Lymnaea stagnalis to single and combined exposures to natural (cyanobacteria) and anthropogenic (the herbicide RoundUp® Flash) stressors. Aquatic Toxicology. 2016; 177 ():116-124.

Chicago/Turabian Style

Emilie Lance; Julia Desprat; Bente Frost Holbech; Claudia Gérard; Myriam Bormans; Linda A. Lawton; Christine Edwards; Claudia Wiegand. 2016. "Accumulation and detoxication responses of the gastropod Lymnaea stagnalis to single and combined exposures to natural (cyanobacteria) and anthropogenic (the herbicide RoundUp® Flash) stressors." Aquatic Toxicology 177, no. : 116-124.

Journal article
Published: 25 February 2016 in MicrobiologyOpen
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The freshwater cyanobacteria, Microcystis sp., commonly form large colonies with bacteria embedded in their mucilage. Positive and negative interactions between Microcystis species and their associated bacteria have been reported. However, the potential role of bacteria in the production and degradation of cyanobacterial secondary metabolites has not been investigated. In this study, a Microcystis-associated bacterial community was isolated and added to the axenic M. aeruginosaPCC7806 liquid culture. After 3years of cocultivation, we studied the bacterial genetic diversity adapted to the PCC7806 strain and compared the intra- and extracellular concentration of major cyanopeptides produced by the cyanobacterial strain under xenic and axenic conditions. Mass spectrometric analyses showed that the intracellular concentration of peptides was not affected by the presence of bacteria. Interestingly, the produced peptides were detected in the axenic media but could not be found in the xenic media. This investigation revealed that a natural bacterial community, dominated by Alpha-proteobacteria, was able to degrade a wide panel of structurally varying cyclic cyanopeptides

ACS Style

Enora Briand; Jean-Francois Humbert; Kevin Tambosco; Myriam Bormans; William H. Gerwick. Role of bacteria in the production and degradation of Microcystis cyanopeptides. MicrobiologyOpen 2016, 5, 469 -478.

AMA Style

Enora Briand, Jean-Francois Humbert, Kevin Tambosco, Myriam Bormans, William H. Gerwick. Role of bacteria in the production and degradation of Microcystis cyanopeptides. MicrobiologyOpen. 2016; 5 (3):469-478.

Chicago/Turabian Style

Enora Briand; Jean-Francois Humbert; Kevin Tambosco; Myriam Bormans; William H. Gerwick. 2016. "Role of bacteria in the production and degradation of Microcystis cyanopeptides." MicrobiologyOpen 5, no. 3: 469-478.

Review
Published: 23 December 2015 in Aquatic Ecology
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The aim of this paper was to summarize the current knowledge on how physical methods can reduce or control internal P release from sediments in lakes and reservoirs. Particular emphasis is given to the role of internal phosphorus load in fueling cyanobacterial blooms which are predicted to increase in frequency and intensity in response to climate change and eutrophication. We present selective case studies (both successful and unsuccessful) to assess the applicability and efficiency of major physical approaches used for decades to reduce internal loading in different systems of various morphology. In particular, we concentrate on where and when (1) hypolimnetic aeration/oxygenation, (2) hypolimnetic withdrawal and (3) sediment dredging are likely to reduce cyanobacterial blooms and whether these methods have an adverse impact on other organisms. We conclude that each method has its strength and weakness depending on the system considered. Sufficient knowledge of all lake nutrient sources and their dynamics together with detailed lake and sediment characteristics is an essential prerequisite for choosing an appropriate control method. We also report that many experiences demonstrated that a combination of restoration methods is often more successful than a single method.

ACS Style

Myriam Bormans; Blahoslav Maršálek; Daniel Jančula. Controlling internal phosphorus loading in lakes by physical methods to reduce cyanobacterial blooms: a review. Aquatic Ecology 2015, 50, 407 -422.

AMA Style

Myriam Bormans, Blahoslav Maršálek, Daniel Jančula. Controlling internal phosphorus loading in lakes by physical methods to reduce cyanobacterial blooms: a review. Aquatic Ecology. 2015; 50 (3):407-422.

Chicago/Turabian Style

Myriam Bormans; Blahoslav Maršálek; Daniel Jančula. 2015. "Controlling internal phosphorus loading in lakes by physical methods to reduce cyanobacterial blooms: a review." Aquatic Ecology 50, no. 3: 407-422.

Journal article
Published: 17 October 2015 in Aquatic Ecology
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Freshwater cyanobacteria can produce large amount of mucilage, particularly during large blooms. The production of these carbon-rich exopolymers (EPS) should influence the carbon-to-nutrient ratios of the organic matter (OM), which are regularly used as a proxy for the herbivorous food quality. However, little is known about the consequences of EPS production on the carbon-to-nutrient ratio of the OM. Two EPS forms can be distinguished: the free fraction composed of soluble extracellular polymeric substances (S-EPS) and the particulate fraction corresponding to the transparent exopolymer particles (TEP). The aim of the study was to determine whether the TEP and S-EPS productions by cyanobacteria influence the carbon-to-nutrient ratios of the particulate OM (POM). Five cyanobacteria species were grown in batch culture and characterized in terms of photosynthetic activity, EPS production, and C, N, P contents. The variability in EPS production was compared with the variability in stoichiometry of the POM. Most of cyanobacteria live in association with heterotrophic bacteria (HB) within the mucilage. The effect of the presence/absence of HB on EPS production and the carbon-to-nutrient ratios of the POM was also characterized for the cyanobacteria Microcystis aeruginosa. We showed that TEP production increased the carbon-to-nutrient ratios of the POM in the absence of HB, while the stoichiometry did not significantly change when HB were present. The C:N ratio of the POM decreased with production of S-EPS by the five species. Lastly, the three colonial species (Chroococcales) tend to produce more TEP than the two filamentous species (Oscillatoriales), with the two picocyanobacteria being the most productive of both TEP and S-EPS.

ACS Style

Alexandrine Pannard; Julie Pédrono; Myriam Bormans; Enora Briand; Pascal Claquin; Yvan Lagadeuc. Production of exopolymers (EPS) by cyanobacteria: impact on the carbon-to-nutrient ratio of the particulate organic matter. Aquatic Ecology 2015, 50, 29 -44.

AMA Style

Alexandrine Pannard, Julie Pédrono, Myriam Bormans, Enora Briand, Pascal Claquin, Yvan Lagadeuc. Production of exopolymers (EPS) by cyanobacteria: impact on the carbon-to-nutrient ratio of the particulate organic matter. Aquatic Ecology. 2015; 50 (1):29-44.

Chicago/Turabian Style

Alexandrine Pannard; Julie Pédrono; Myriam Bormans; Enora Briand; Pascal Claquin; Yvan Lagadeuc. 2015. "Production of exopolymers (EPS) by cyanobacteria: impact on the carbon-to-nutrient ratio of the particulate organic matter." Aquatic Ecology 50, no. 1: 29-44.

Original research article
Published: 29 September 2015 in Frontiers in Microbiology
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Akinetes are spore-like non-motile cells that differentiate from vegetative cells of filamentous cyanobacteria from the order Nostocales. They play a key role in the survival and distribution of these species and contribute to their perennial blooms. Here we demonstrate variations in cellular ultrastructure during akinete formation concomitant with accumulation of cyanophycin; a copolymer of aspartate and arginine that forms storage granules. Cyanophycin accumulation is initiated in vegetative cells few days post exposure to akinete inducing conditions. This early-accumulated cyanophycin pool in vegetative cells disappeared as a nearby cell differentiates to an akinete and stores large pool of cyanophycin. During the akinete maturation, the cyanophycin pool is further increased and comprise up to 2% of the akinete volume. The cellular pattern of photosynthetic activity during akinete formation was study by a nano-metric scale secondary ion mass spectrometry (NanoSIMS) analysis of 13C-enriched cultures. Quantitative estimation of carbon assimilation in vegetative cells and akinetes (filament-attached and free) indicates that vegetative cells maintained their basal activity while differentiating akinetes gradually reduced their activity. Mature free akinetes practically lost their photosynthetic activity although small fraction of free akinetes were still photosynthetically active. Additional 13C pulse chase experiments indicated rapid carbon turnover during akinete formation and de novo synthesis of cyanophycin in vegetative cells 4 days post induction of akinete differentiation.

ACS Style

Assaf Sukenik; Iris Maldener; Thomas Delhaye; Yehudit Viner-Mozzini; Dotan Sela; Myriam Bormans. Carbon assimilation and accumulation of cyanophycin during the development of dormant cells (akinetes) in the cyanobacterium Aphanizomenon ovalisporum. Frontiers in Microbiology 2015, 6, 1067 .

AMA Style

Assaf Sukenik, Iris Maldener, Thomas Delhaye, Yehudit Viner-Mozzini, Dotan Sela, Myriam Bormans. Carbon assimilation and accumulation of cyanophycin during the development of dormant cells (akinetes) in the cyanobacterium Aphanizomenon ovalisporum. Frontiers in Microbiology. 2015; 6 ():1067.

Chicago/Turabian Style

Assaf Sukenik; Iris Maldener; Thomas Delhaye; Yehudit Viner-Mozzini; Dotan Sela; Myriam Bormans. 2015. "Carbon assimilation and accumulation of cyanophycin during the development of dormant cells (akinetes) in the cyanobacterium Aphanizomenon ovalisporum." Frontiers in Microbiology 6, no. : 1067.

Review
Published: 19 August 2015 in Aquatic Ecology
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Artificial mixing has been used as a measure to prevent the growth of cyanobacteria in eutrophic lakes and reservoirs for many years. In this paper, we give an overview of studies that report on the results of this remedy. Generally, artificial mixing causes an increase in the oxygen content of the water, an increase in the temperature in the deep layers but a decrease in the upper layers, while the standing crop of phytoplankton (i.e. the chlorophyll content per m2) often increases partly due to an increase in nutrients entrained from the hypolimnion or resuspended from the sediments. A change in composition from cyanobacterial dominance to green algae and diatoms can be observed if the imposed mixing is strong enough to keep the cyanobacteria entrained in the turbulent flow, the mixing is deep enough to limit light availability and the mixing devices are well distributed horizontally over the lake. Both models and experimental studies show that if phytoplankton is entrained in the turbulent flow and redistributed vertically over the entire depth, green algae and diatoms win the competition over (colonial) cyanobacteria due to a higher growth rate and reduced sedimentation losses. The advantage of buoyant cyanobacteria to float up to the illuminated upper layers is eradicated in a well-mixed system.

ACS Style

Petra M. Visser; Bastiaan Willem Ibelings; Myriam Bormans; Jef Huisman. Artificial mixing to control cyanobacterial blooms: a review. Aquatic Ecology 2015, 50, 423 -441.

AMA Style

Petra M. Visser, Bastiaan Willem Ibelings, Myriam Bormans, Jef Huisman. Artificial mixing to control cyanobacterial blooms: a review. Aquatic Ecology. 2015; 50 (3):423-441.

Chicago/Turabian Style

Petra M. Visser; Bastiaan Willem Ibelings; Myriam Bormans; Jef Huisman. 2015. "Artificial mixing to control cyanobacterial blooms: a review." Aquatic Ecology 50, no. 3: 423-441.