Co-occurrence of microcystin and anatoxin-a in the freshwater lake Aydat (France): Analytical and molecular approaches during a three-year survey

Ballot, 2010, First report of anatoxin-a-producing cyanobacterium Aphanizomenon issatschenkoi in northeastern Germany, Toxicon, 56, 964, 10.1016/j.toxicon.2010.06.021 Ballot, 2004, Cyanobacteria and cyanobacterial toxins in three alkaline Rift Valley lakes of Kenya—Lakes Bogoria, Nakuru and Elmenteita, J. Plankton. Res., 26, 925, 10.1093/plankt/fbh084 Ballot, 2005, Cyanobacteria and cyanobacterial toxins in the alkaline crater lakes Sonachi and Simbi, Kenya, Harmful Algae, 4, 139, 10.1016/j.hal.2004.01.001 Ballot, 2003, Cyanobacterial toxins in lake Baringo, Kenya, Limnologica, 33, 2, 10.1016/S0075-9511(03)80003-8 Barco, 2005, Optimization of intracellular microcystin extraction for their subsequent analysis by high-performance liquid chromatography, J. Chromatogr. A, 1074, 23, 10.1016/j.chroma.2005.03.087 Bourrelly, P. 1966. Les Algues d’Eau Douce. Les Algues vertes, Edition N Boubee & Cie, Paris Briand, 2008, Temporal variations in the dynamics of potentially microcystin-producing strains in a bloom-forming Planktothrix agardhii (cyanobacterium) population, Appl. Environ. Microbiol., 74, 3839, 10.1128/AEM.02343-07 Briand, 2009, Spatiotemporal changes in the genetic diversity of a bloom-forming Microcystis aeruginosa (cyanobacteria) population, ISME J., 3, 419, 10.1038/ismej.2008.121 Cadel-Six, 2009, Identification of a polyketide synthase coding sequence specific for anatoxin-a-producing Oscillatoria cyanobacteria, Appl. Environ. Microbiol., 75, 4909, 10.1128/AEM.02478-08 Cadel-Six, 2007, Different genotypes of anatoxin-producing cyanobacteria coexist in the Tarn River, France, Appl. Environ. Microbiol., 73, 7605, 10.1128/AEM.01225-07 Carrasco, 2007, Anatoxin-a occurrence and potential cyanobacterial anatoxin-a producers in Spanish reservoirs, J. Phycol., 43, 1120, 10.1111/j.1529-8817.2007.00402.x Christiansen, 2003, Microcystin biosynthesis in Planktothrix: genes, evolution, and manipulation, J. Bacteriol., 185, 564, 10.1128/JB.185.2.564-572.2003 Dittmann, 1997, Insertional mutagenesis of a peptide synthetase gene that is responsible for hepatotoxin production in the cyanobacterium Microcystis aeruginosa PCC 7806, Mol. Microbiol., 26, 779, 10.1046/j.1365-2958.1997.6131982.x Duy, 2000, Toxicology and Risk assessment of freshwater cyanobacterial (blue-green algal) toxins in water, 113, 10.1007/978-1-4757-6429-1_3 Edwards, 1992, Identification of anatoxin-a in benthic cyanobacteria (blue-green algae) and in associated dog poisonings at Loch Insh, Scotland, Toxicon, 30, 1165, 10.1016/0041-0101(92)90432-5 Faassen, 2012, First report of (homo)anatoxin-a and dog neurotoxicosis after ingestion of benthic cyanobacteria in The Netherlands, Toxicon, 60, 378, 10.1016/j.toxicon.2012.04.335 Fastner, 1998, Optimised extraction of microcystins from field samples—a comparison of different solvents and procedures, Water Res., 32, 3177, 10.1016/S0043-1354(98)00073-6 Frangeul, 2008, Highly plastic genome of Microcystis aeruginosa PCC 7806, a ubiquitous toxic freshwater cyanobacterium, BMC Genomics, 9, 274, 10.1186/1471-2164-9-274 Furey, 2005, Strategies to avoid the mis-identification of anatoxin-a using mass spectrometry in the forensic investigation of acute neurotoxic poisoning, J. Chromatogr. A, 1082, 91, 10.1016/j.chroma.2005.05.040 Geitler, 1932, 1196 Gerphagnon, 2013, Fungal parasitism: life cycle, dynamics and impact on cyanobacterial blooms, PloS one, 8, e60894, 10.1371/journal.pone.0060894 Gilroy, 2000, Assessing potential health risks from microcystin toxins in blue-green algae dietary supplements, Environ. Health Perspect., 108, 435, 10.1289/ehp.00108435 Gobler, 2007, Interactive influences of nutrient loading, zooplankton grazing, and microcystin synthetase gene expression on cyanobacterial bloom dynamics in a eutrophic New York lake, Harmful Algae, 6, 119, 10.1016/j.hal.2006.08.003 Graham, 2010, Cyanotoxin mixtures and taste-and-odor compounds in cyanobacterial blooms from the Midwestern United States, Environ. Sci. Technol., 44, 7361, 10.1021/es1008938 Gugger, 2005, First report in a river in France of the benthic cyanobacterium Phormidium favosum producing anatoxin-a associated with dog neurotoxicosis, Toxicon, 45, 919, 10.1016/j.toxicon.2005.02.031 Hedman, 2008, New measurements of cyanobacterial toxins in natural waters using high performance liquid chromatography coupled to tandem mass spectrometry, J. Environ. Qual., 37, 1817, 10.2134/jeq2007.0368 Henriksen, 1997, Detection of an anatoxin-a (s)-like anticholinesterase in natural blooms and cultures of cyanobacteria/blue-green algae from Danish lakes and in the stomach contents of poisoned birds, Toxicon, 35, 901, 10.1016/S0041-0101(96)00190-0 Hisbergues, 2003, PCR-based identification of microcystin-producing genotypes of different cyanobacterial genera, Arch. Micrbiol., 180, 402, 10.1007/s00203-003-0605-9 Hodoki, 2013, Anatoxin-a-producing Raphidiopsis mediterranea Skuja var. grandis Hill is one ecotype of non-heterocytous Cuspidothrix issatschenkoi (Usačev) Rajaniemi et al. in Japanese lakes, Harmful Algae, 21, 44, 10.1016/j.hal.2012.11.007 Hotto, 2008, Spatial and temporal diversity of microcystins and microcystin-producing genotypes in Oneida Lake, NY, Harmful Algae, 7, 671, 10.1016/j.hal.2008.02.001 Humbert, 2013, A tribute to disorder in the genome of the bloom-forming freshwater cyanobacterium Microcystis aeruginosa, PloS One, 8, e70747, 10.1371/journal.pone.0070747 Jochimsen, 1998, Liver failure and death after exposure to microcystins at a hemodialysis center in Brazil, N. Engl. J. Med., 338, 873, 10.1056/NEJM199803263381304 Kaebernick, 2000, Light and the transcriptional response of the microcystin biosynthesis gene cluster, Appl. Environ. Microbiol., 66, 3387, 10.1128/AEM.66.8.3387-3392.2000 Kaneko, 2007, Complete genomic structure of the bloom-forming toxic cyanobacterium Microcystis aeruginosa NIES-843, DNA Res., 14, 247, 10.1093/dnares/dsm026 Kardinaal, 2007, Competition for light between toxic and nontoxic strains of the harmful cyanobacterium Microcystis, Appl. Environ. Microbiol., 73, 2939, 10.1128/AEM.02892-06 Komárek, J., 1998. Cyanoprokaryota Teil 1/Part 1: Chroococcales, Süßwasserflora von Mitteleuropa, Band 19/1. Krienitz, 2003, Contribution of hot spring cyanobacteria to the mysterious deaths of Lesser Flamingos at Lake Bogoria, Kenya, FEMS Microbiol. Ecol., 43, 141, 10.1111/j.1574-6941.2003.tb01053.x Kurmayer, 2003, Application of real-time PCR for quantification of microcystin genotypes in a population of the toxic cyanobacterium Microcystis sp, Appl. Environ. Microbiol., 69, 6723, 10.1128/AEM.69.11.6723-6730.2003 Lafforgue, 1995, Selective mechanisms controlling algal succession in Aydat lake, Water Sci. Technol., 32, 117, 10.2166/wst.1995.0173 Lance, 2010, Impact of toxic cyanobacteria on gastropods and microcystin accumulation in a eutrophic lake (Grand-Lieu France) with special reference to Physa (= Physella) acuta, Sci. Total Environ., 408, 3560, 10.1016/j.scitotenv.2010.04.050 Lepistö, 2005, Occurrence and toxicity of cyanobacterial blooms dominated by Anabaena lemmermannii P. Richter and Aphanizomenon spp. in boreal lakes in 2003, Algol. Stud., 117, 315, 10.1127/1864-1318/2005/0117-0315 Li, 2010, Cyanobacterial population and harmful metabolites dynamics during a bloom in Yanghe Reservoir, North China, Harmful Algae, 9, 481, 10.1016/j.hal.2010.03.003 Long, 2001, Cellular microcystin content in N-limited Microcystis aeruginosa can be predicted from growth rate, Appl. Environ. Microbiol., 67, 278, 10.1128/AEM.67.1.278-283.2001 Mann, 2012, Toxicon, 60, 1404, 10.1016/j.toxicon.2012.10.006 Méjean, 2010, The genome sequence of the cyanobacterium Oscillatoria sp. PCC 6506 reveals several gene clusters responsible for the biosynthesis of toxins and secondary metabolites, J. Bacteriol., 192, 5264, 10.1128/JB.00704-10 Merel, 2013, State of knowledge and concerns on cyanobacterial blooms and cyanotoxins, Environ. Int., 59, 303, 10.1016/j.envint.2013.06.013 Nonneman, 2002, A PCR-based test to assess the potential for microcystin occurence in channel catfish production ponds, J. Phycol., 38, 230, 10.1046/j.1529-8817.2002.01138.x Nübel, 1997, PCR primers to amplify 16S rRNA genes from cyanobacteria, Appl. Environ. Microbiol., 63, 3327, 10.1128/AEM.63.8.3327-3332.1997 Olson, 1951, Toxic plankton, 86 Osswald, 2007, Toxicology and detection methods of the alkaloid neurotoxin produced by cyanobacteria anatoxin-a, Environ. Int., 33, 1070, 10.1016/j.envint.2007.06.003 Paerl, 2011, Controlling harmful cyanobacterial blooms in a world experiencing anthropogenic and climatic-induced change, Sci. Total Environ., 409, 1739, 10.1016/j.scitotenv.2011.02.001 Park, 1993, Hepatotoxin (microcystin) and neurotoxin (anatoxin-a) contained in natural blooms and strains of cyanobacteria from Japanese freshwaters, Nat. Toxins, 1, 353, 10.1002/nt.2620010606 Park, 1998, Hepatotoxic microcystins and neurotoxic anatoxin-a in cyanobacterial blooms from Korean lakes, Environ. Toxic. Water, 13, 225, 10.1002/(SICI)1098-2256(1998)13:3<225::AID-TOX4>3.0.CO;2-9 Pawlik-Skowrońska, 2004, Relationship between Cyanobacterial bloom composition and anatoxin-a and microcystin occurrence in the eutrophic dam reservoir (SE Poland), Pol. J. Ecol., 52, 479 R Development Core Team (2011). R: A Language and Environment for Statistical Computing. Vienna, Austria: the R Foundation for Statistical Computing. ISBN: 3-900051-07-0. Available online at 〈http://www.R-project.org/〉. Rantala-Ylinen, 2011, Anatoxin-a synthetase gene cluster of the cyanobacterium Anabaena sp. strain 37 and molecular methods to detect potential producers, Appl. Environ. Microbiol., 77, 7271, 10.1128/AEM.06022-11 Rapala, 1998, Assessment of environmental conditions that favor hepatotoxic and neurotoxic Anabaena spp. strains cultured under light limitation at different temperatures, Microbial. Ecol., 36, 181, 10.1007/s002489900105 Rouhiainen, 2004, Genes coding for hepatotoxic heptapeptides (microcystins) in the cyanobacterium Anabaena strain 90, Appl. Environ. Microbiol., 70, 686, 10.1128/AEM.70.2.686-692.2004 Ruiz, 2013, First report of microcystins and anatoxin-a co-occurrence in San Roque reservoir (Córdoba, Argentina), Water Air Soil Pollut., 224, 1, 10.1007/s11270-013-1593-2 Sabart, 2013, The importance of small colonies in sustaining Microcystis population exposed to mixing conditions: an exploration through colony size, genotypic composition and toxic potential, Environ. Microbiol. Rep., 5, 747 Sabart, 2010, Spatiotemporal variations in microcystin concentrations and in the proportions of microcystin-producing cells in several Microcystis aeruginosa populations, Appl. Environ. Micrbiol., 76, 4750, 10.1128/AEM.02531-09 Srivastava, 2012, Dynamics of microcystin production and quantification of potentially toxigenic Microcystis sp. using real-time PCR, Water Res., 46, 817, 10.1016/j.watres.2011.11.056 Tillett, 2000, Structural organization of microcystin biosynthesis in Microcystis aeruginosa PCC7806: an integrated peptide–polyketide synthetase system, Chem. Biol., 7, 753, 10.1016/S1074-5521(00)00021-1 Utermöhl, 1958, Zur vervollkommnung der quantitativen phytoplankton-methodik, Mitt. Int. Ver. Theor. Angew. Limnol., 9, 1 Vaitomaa, 2003, Quantitative real-time PCR for determination of microcystin synthetase E copy numbers for Microcystis and Anabaena in lakes, Appl. Environ. Microbiol., 69, 7289, 10.1128/AEM.69.12.7289-7297.2003 Vezie, 1998, Variation of microcystin content of cyanobacterial blooms and isolated strains in Lake Grand-Lieu (France), Microb. Ecol., 35, 126, 10.1007/s002489900067 Welker, 2006, Cyanobacterial peptides—nature's own combinatorial biosynthesis, FEMS Microbiol. Rev., 30, 530, 10.1111/j.1574-6976.2006.00022.x Welker, 2003, Toxic Microcystis in shallow lake Müggelsee (Germany)—dynamics, distribution, diversity, Arch. Hydrobiol., 157, 227, 10.1127/0003-9136/2003/0157-0227 Whitton, 2002 Wood, 2007, First report of homoanatoxin-a and associated dog neurotoxicosis in New Zealand, Toxicon, 50, 292, 10.1016/j.toxicon.2007.03.025 Yoshida, 2007, Dynamics of microcystin-producing and non-microcystin-producing Microcystis populations is correlated with nitrate concentration in a Japanese lake, FEMS Microbiol. Lett., 266, 49, 10.1111/j.1574-6968.2006.00496.x