Impact of environmental factors on the regulation of cyanotoxin production

Toxins

Volumn 6, Issue 7, 2014, Pages 1951-1978

  Boopathi, Thangavelu ^a   Ki, Jang Seu ^a  

^a Sangmyung University   (South Korea)

Author keywords

Anatoxins and saxitoxins; Cyanotoxin; Cylindrospermopsin; Microcystins; Nodularin

Indexed keywords

ANATOXIN; ANATOXIN A; APLYSIATOXIN; BACTERIAL TOXIN; CYANOTOXIN; CYLINDROSPERMOPSIN; HOMOANATOXIN A; MICROCYSTIN; MICROCYSTIN RR; NODULARIN; SAXITOXIN; UNCLASSIFIED DRUG; CYCLOPEPTIDE; MARINE TOXIN; TROPANE DERIVATIVE; URACIL;

ALGAL BLOOM; BACTERIAL GENE; CHEMICAL STRUCTURE; CYANOBACTERIUM; CYLINDROSPERMOPSIN SYNTHETASE GENE; ENVIRONMENTAL FACTOR; ENVIRONMENTAL IMPACT; GENETIC TRANSCRIPTION; HUMAN; NONHUMAN; REGULATORY MECHANISM; REVIEW; TOXICITY; TOXIN SYNTHESIS; ANALOGS AND DERIVATIVES; ANIMAL; CLIMATE CHANGE; ENVIRONMENT; METABOLISM;

ANIMALS; CLIMATE CHANGE; CYANOBACTERIA; ENVIRONMENT; HUMANS; MARINE TOXINS; MICROCYSTINS; PEPTIDES, CYCLIC; SAXITOXIN; TROPANES; URACIL;

EID: 84903381841     PISSN: None     EISSN: 20726651     Source Type: Journal    
DOI: 10.3390/toxins6071951     Document Type: Review

References (161)

1. Paerl, H.W.; Paul, V.J. Climate change: Links to global expansion of harmful cyanobacteria. Water Res. 2012, 46, 1349-1363.
2. Knoll, A.H. Cyanobacteria and Earth History. In The Cyanobacteria: Molecular Biology, Genomics, and Evolution; Herrero, A., Flores, E., Eds.; Caister Academic Press: Norfolk, UK, 2008; p. 484.
3. Schopf, J.W. The Fossil Record: Tracing the Roots of the Cyanobacterial Lineage. In The Ecology of Cyanobacteria; Whitton, B., Potts, M., Eds.; Kluwer Academic Publishers: Dordrecht, The Netherlands, 2002; pp. 13-35.
4. Paerl, H.W.; Otten, T.G. Harmful cyanobacterial blooms: Causes, consequences, and controls. Microb. Ecol. 2013, 65, 995-1010.
5. Steffen, M.M.; Li, Z.; Effler, T.C.; Hauser, L.J.; Boyer, G.L.; Wilhelm, S.W. Comparative metagenomics of toxic freshwater Cyanobacteria bloom communities on two continents. PLoS One 2012, 7, e44002.
6. Suikkanen, S.; Pulina, S.; Engstrom-Ost, J.; Lehtiniemi, M.; Lehtinen, S.; Brutemark, A. Climate change and eutrophication induced shifts in northern summer plankton communities. PLoS One 2013, 8, e66475.
7. Paerl, H.W.; Huisman, J. Blooms like it hot. Science 2008, 320, 57-58.
8. Elliott, J.A. Is the future blue-green? A review of the current model predictions of how climate change could affect pelagic freshwater cyanobacteria. Water Res. 2012, 46, 1364-1371.
9. Corbel, S.; Mougin, C.; Bouaicha, N. Cyanobacterial toxins: Modes of actions, fate in aquatic and soil ecosystems, phytotoxicity and bioaccumulation in agricultural crops. Chemosphere 2014, 96, 1-15.
10. O'Neil, J.M.; Davis, T.W.; Burford, M.A.; Gobler, C.J. The rise of harmful cyanobacteria blooms: The potential roles of eutrophication and climate change. Harmful Algae 2012, 14, 313-334.
11. Cheung, M.Y.; Liang, S.; Lee, J. Toxin-producing cyanobacteria in freshwater: A review of the problems, impact on drinking water safety, and efforts for protecting public health. J. Microbiol. 2013, 51, 1-10.
12. Kaplan, A.; Harel, M.; Kaplan-Levy, R.N.; Hadas, O.; Sukenik, A.; Dittmann, E. The languages spoken in the water body (or the biological role of cyanobacterial toxins). Front. Microbiol. 2012, 3, 138:1-138:11.
13. Kaebernick, M.; Neilan, B.A. Ecological and molecular investigations of cyanotoxin production. FEMS Microbiol. Ecol. 2001, 35, 1-9.
14. Neilan, B.A.; Pearson, L.A.; Muenchhoff, J.; Moffitt, M.C.; Dittmann, E. Environmental conditions that influence toxin biosynthesis in cyanobacteria. Environ. Microbiol. 2013, 15, 1239-1253.
15. Pearson, L.; Mihali, T.; Moffitt, M.; Kellmann, R.; Neilan, B. On the chemistry, toxicology and genetics of the cyanobacterial toxins, microcystin, nodularin, saxitoxin and cylindrospermopsin. Mar. Drugs 2010, 8, 1650-1680.
16. Leão, P.N.; Vasconcelos, M.T.; Vasconcelos, V.M. Allelopathy in freshwater cyanobacteria. Crit. Rev. Microbiol. 2009, 35, 271-282.
17. Leão, P.N.; Vasconcelos, M.T.S.; Vasconcelos, V.M. Allelopathic activity of cyanobacteria on green microalgae at low cell densities. Eur. J. Phycol. 2009, 44, 347-355.
18. Kleinteich, J.; Wood, S.A.; Kupper, F.C.; Camacho, A.; Quesada, A.; Frickey, T.; Dietrich, D.R. Temperature-related changes in polar cyanobacterial mat diversity and toxin production. Nat. Clim. Chang. 2012, 2, 356-360.
19. Eiler, A.; Drakare, S.; Bertilsson, S.; Pernthaler, J.; Peura, S.; Rofner, C.; Simek, K.; Yang, Y.; Znachor, P.; Lindstrâm, E.S. Unveiling distribution patterns of freshwater phytoplankton by a next generation sequencing based approach. PLoS One 2013, 8, e53516.
20. Park, S.; Brett, M.T.; Muller-Solger, A.; Goldman, C.R. Climatic forcing and primary productivity in a subalpine lake: Interannual variability as a natural experiment. Limnol. Oceanogr. 2004, 49, 614-619.
21. Kosten, S.; Huszar, V.L.M.; Bécares, E.; Costa, L.S.; van Donk, E.; Hansson, L.-A.; Jeppesen, E.; Kruk, C.; Lacerot, G.; Mazzeo, N.; et al. Warmer climates boost cyanobacterial dominance in shallow lakes. Glob. Chang. Biol. 2012, 18, 118-126.
22. Wilhelm, S.W.; Farnsley, S.E.; LeCleir, G.R.; Layton, A.C.; Satchwell, M.F.; DeBruyn, J.M.; Boyer, G.L.; Zhu, G.; Paerl, H.W. The relationships between nutrients, cyanobacterial toxins and the microbial community in Taihu (Lake Tai), China. Harmful Algae 2011, 10, 207-215.
23. Kuiper-Goodman, T.; Falconer, I.; Fitzgerald, J. Human Health Aspects. In Toxic Cyanobacteria in Water: A Guide to Their Public Health Consequences, Monitoring and Management; Chorus, I., Bartram, J., Eds.; E & FN Spon Publishers: London, UK, 1999; p. 36.
24. Van Apeldoorn, M.E.; van Egmond, H.P.; Speijers, G.J.; Bakker, G.J. Toxins of cyanobacteria. Mol. Nutr. Food. Res. 2007, 51, 7-60.
25. Carmichael, W.W. Health effects of toxin-producing cyanobacteria: "The CyanoHAB". Hum. Ecol. Risk Assess. 2001, 7, 1393-1407.
26. Zilliges, Y.; Kehr, J.-C.; Meissner, S.; Ishida, K.; Mikkat, S.; Hagemann, M.; Kaplan, A.; Börner, T.; Dittmann, E. The cyanobacterial hepatotoxin microcystin binds to proteins and increases the fitness of Microcystis under oxidative stress conditions. PLoS One 2011, 6, e17615.
27. Kurmayer, R. The toxic cyanobacterium Nostoc sp. strain 152 produces highest amounts of microcystin and nostophycin under stress conditions. J. Phycol. 2011, 47, 200-207.
28. Fischer, W.J.; Dietrich, D.R. Pathological and biochemical characterization of microcystin-induced hepatopancreas and kidney damage in carp (Cyprinus carpio). Toxicol. Appl. Pharmacol. 2000, 164, 73-81.
29. Fischer, W.J.; Altheimer, S.; Cattori, V.; Meier, P.J.; Dietrich, D.R.; Hagenbuch, B. Organic anion transporting polypeptides expressed in liver and brain mediate uptake of microcystin. Toxicol. Appl. Pharmacol. 2005, 203, 257-263.
30. Jochimsen, E.M.; Carmichael, W.W.; An, J.; Cardo, D.M.; Cookson, S.T.; Holmes, C.E.; Antunes, M.B.; Filho, D.A.D.; Lyra, T.M.; Barreto, V.S.T. Liver failure and death after exposure to microcystins at a hemodialysis center in Brazil. N. Engl. J. Med. 1998, 338, 873-878.
31. Zeng, C.; Sun, H.; Xie, P.; Wang, J.; Zhang, G.; Chen, N.; Yan, W.; Li, G. The role of apoptosis in MCLR-induced developmental toxicity in zebrafish embryos. Aquat. Toxicol. 2014, 149, 25-32.
32. Niedermeyer, T.J.; Schmieder, P.; Kurmayer, R. Isolation of Microcystins from the Cyanobacterium Planktothrix rubescens Strain No80. Nat. Prod. Bioprospect. 2014, 4, 37-45.
33. Rastogi, R.P.; Sinha, R.P.; Incharoensakdi, A. The cyanotoxin-microcystins: Current overview. Rev. Environ. Sci. Biotechnol. 2014, 13, 215-249.
34. Gehringer, M.M.; Wannicke, N. Climate change and regulation of hepatotoxin production in Cyanobacteria. FEMS Microbiol. Ecol. 2014, 88, 1-25.
35. Neilan, B.A.; Pearson, L.A.; Moffitt, M.C.; Mihali, K.T.; Kaebernick, M.; Kellmann, R.; Pomati, F. The genetics and genomics of cyanobacterial toxicity. In Cyanobacterial Harmful Algal Blooms: State of the Science and Research Needs; Hudnell, H.K., Ed.; Springer: New York, NY, USA, 2008; pp. 417-452.
36. Kaasalainen, U.; Fewer, D.P.; Jokela, J.; Wahlsten, M.; Sivonen, K.; Rikkinen, J. Cyanobacteria produce a high variety of hepatotoxic peptides in lichen symbiosis. Proc. Natl. Acad. Sci. USA 2012, 109, 5886-5891.
37. Kaasalainen, U.; Fewer, D.P.; Jokela, J.; Wahlsten, M.; Sivonen, K.; Rikkinen, J. Lichen species identity and diversity of cyanobacterial toxins in symbiosis. New Phytol. 2013, 198, 647-651.
38. Moffitt, M.C.; Neilan, B.A. Characterization of the nodularin synthetase gene cluster and proposed theory of the evolution of cyanobacterial hepatotoxins. Appl. Environ. Microbiol. 2004, 70, 6353-6362.
39. Alexova, R.; Haynes, P.; Ferrari, B.; Neilan, B. Comparative protein expression in different strains of the bloom-forming cyanobacterium Microcystis aeruginosa. Mol. Cell. Proteomics 2011, 10, 3749-3765.
40. Wood, S.A.; Kuhajek, J.M.; Winton, M.; Phillips, N.R. Species composition and cyanotoxin production in periphyton mats from three lakes of varying trophic status. FEMS Microbiol. Ecol. 2012, 79, 312-326.
41. Rouhiainen, L.; Vakkilainen, T.; Siemer, B.L.; Buikema, W.; Haselkorn, R.; Sivonen, K. Genes coding for hepatotoxic heptapeptides (microcystins) in the cyanobacterium Anabaena strain 90. Appl. Environ. Microbiol. 2004, 70, 686-692.
42. Christiansen, G.; Fastner, J.; Erhard, M.; Börner, T.; Dittmann, E. Microcystin biosynthesis in Planktothrix: Genes, evolution, and manipulation. J. Bacteriol. 2003, 185, 564-572.
43. Kaebernick, M.; Dittmann, E.; Börner, T.; Neilan, B.A. Multiple alternate transcripts direct the biosynthesis of microcystin, a cyanobacterial. Appl. Environ. Microbiol. 2002, 68, 449-455.
44. Ginn, H.P.; Pearson, L.A.; Neilan, B.A. NtcA from Microcystis aeruginosa PCC 7806 is autoregulatory and binds to the microcystin promoter. Appl. Environ. Microbiol. 2010, 76, 4362-4368.
45. Alexova, R.; Fujii, M.; Birch, D.; Cheng, J.; Waite, T.D.; Ferrari, B.C.; Neilan, B.A. Iron uptake and toxin synthesis in the bloom-forming Microcystis aeruginosa under iron limitation. Environ. Microbiol. 2011, 13, 1064-1077.
46. Su, Z.; Olman, V.; Mao, F.; Xu, Y. Comparative genomics analysis of NtcA regulons in cyanobacteria: Regulation of nitrogen assimilation and its coupling to photosynthesis. Nucleic Acids Res. 2005, 33, 5156-5171.
47. Luque, I.; Vazquez-Bermudez, M.F.; Paz-Yepes, J.; Flores, E.; Herrero, A. In vivo activity of the nitrogen control transcription factor NtcA is subjected to metabolic regulation in Synechococcus sp. strain PCC 7942. FEMS Microbiol. Lett. 2004, 236, 47-52.
48. Ramasubramanian, T.S.; Wei, T.F.; Oldham, A.K.; Golden, J.W. Transcription of the Anabaena sp. strain PCC 7120 ntcA gene: Multiple transcripts and NtcA binding. J. Bacteriol. 1996, 178, 922-926.
49. Kuniyoshi, T.M.; Gonzalez, A.; Lopez-Gomollon, S.; Valladares, A.; Bes, M.T.; Fillat, M.F.; Peleato, M.L. 2-oxoglutarate enhances NtcA binding activity to promoter regions of the microcystin synthesis gene cluster. FEBS Lett. 2011, 585, 3921-3926.
50. Ermilova, E.V.; Forchhammer, K. PII signaling proteins of cyanobacteria and green algae. New features of conserved proteins. Russ. J. Plant Physiol. 2013, 60, 483-490.
51. Zhao, M.-X.; Jiang, Y.-L.; He, Y.-X.; Chen, Y.-F.; Teng, Y.-B.; Chen, Y.; Zhang, C.-C.; Zhou, C.-Z. Structural basis for the allosteric control of the global transcription factor NtcA by the nitrogen starvation signal 2-oxoglutarate. Proc. Natl. Acad. Sci. USA 2010, 107, 12487-12492.
52. Herrero, A.; Muro-Pastor, A.; Flores, E. Nitrogen control in cyanobacteria. J. Bacteriol. 2001, 183, 411-425.
53. Long, B.M.; Jones, G.J.; Orr, P.T. Cellular microcystin content in N-limited Microcystis aeruginosa can be predicted from growth rate. Appl. Environ. Microbiol. 2001, 67, 278-283.
54. Utkilen, H.; Gjølme, N. Toxin production by Microcystis aeruginosa as a function of light in continuous cultures and its ecological significance. Appl. Environ. Microbiol. 1992, 58, 1321-1325.
55. Downing, T.G.; Meyer, C.; Gehringer, M.M.; van de Venter, M. Microcystin content of Microcystis aeruginosa is modulated by nitrogen uptake rate relative to specific growth rate or carbon fixation rate. Environ. Toxicol. 2005, 20, 257-262.
56. Downing, T.G.; Sember, C.S.; Gehringer, M.M.; Leukes, W. Medium N:P ratios and specific growth rate comodulate microcystin and protein content in Microcystis aeruginosa PCC7806 and M. aeruginosa UV027. Microb. Ecol. 2005, 49, 468-473.
57. Sevilla, E.; Martin-Luna, B.; Vela, L.; Bes, M.T.; Peleato, M.L.; Fillat, M. Microcystin-LR synthesis as response to nitrogen: Transcriptional analysis of the mcyD gene in Microcystis aeruginosa PCC7806. Ecotoxicology 2010, 19, 1167-1173.
58. Tonk, L.; van de Waal, D.B.; Slot, P.; Huisman, J.; Matthijs, H.C.; Visser, P.M. Amino acid availability determines the ratio of microcystin variants in the cyanobacterium Planktothrix agardhii. FEMS Microbiol. Ecol. 2008, 65, 383-390.
59. Van de Waal, D.B.; Verspagen, J.M.H.; Lürling, M.; van Donk, E.; Visser, P.M.; Huisman, J. The ecological stoichiometry of toxins produced by harmful cyanobacteria: An experimental test of the carbon-nutrient balance hypothesis. Ecol. Lett. 2009, 12, 1326-1335.
60. Van de Waal, D.B.; Verspagen, J.M.H.; Finke, J.F.; Vournazou, V.; Immers, A.K.; Kardinaal, W.E.A.; Tonk, L.; Becker, S.; van Donk, E.; Visser, P.M.; et al. Reversal in competitive dominance of a toxic versus non-toxic cyanobacterium in response to rising CO2. ISME J. 2011, 5, 1438-1450.
61. Jahnichen, S.; Long, B.M.; Petzoldt, T. Microcystin production by Microcystis aeruginosa: Direct regulation by multiple environmental factors. Harmful Algae 2011, 12, 95-104.
62. Horst, G.P.; Sarnelle, O.; White, J.D.; Hamilton, S.K.; Kaul, R.B.; Bressie, J.D. Nitrogen availability increases the toxin quota of a harmful cyanobacterium, Microcystis aeruginosa. Water Res. 2014, 54, 188-198.
63. Monchamp, M.-E.; Pick, F.R.; Beisner, B.E.; Maranger, R. Nitrogen forms influence microcystin concentration and composition via changes in cyanobacterial community structure. PLoS One 2014, 9, e85573.
64. Ding, Y.; Song, L.; Sedmak, B. UVB Radiation as a potential selective factor favoring microcystin producing bloom forming cyanobacteria. PLoS One 2013, 8, e73919.
65. Kaebernick, M.; Neilan, B.A.; Börner, T.; Dittmann, E. Light and the transcriptional response of the microcystin biosynthesis gene cluster. Appl. Environ. Microbiol. 2000, 66, 3387-3392.
66. Tonk, L.; Visser, P.M.; Christiansen, G.; Dittmann, E.; Snelder, E.O.; Wiedner, C.; Mur, L.R.; Huisman, J. The microcystin composition of the cyanobacterium Planktothrix agardhii changes toward a more toxic variant with increasing light intensity. Appl. Environ. Microbiol. 2005, 71, 5177-5181.
67. Hansel, A.; Axelsson, R.; Lindberg, P.; Troshina, O.Y.; Wünschiers, R.; Lindblad, P. Cloning and characterisation of a hyp gene cluster in the filamentous cyanobacterium Nostoc sp. strain PCC 73102. FEMS Microbiol. Lett. 2001, 201, 59-64.
68. Sevilla, E.; Martin-Luna, B.; Bes, M.T.; Fillat, M.; Peleato, M.L. An active photosynthetic electron transfer chain required for mcyD transcription and microcystin synthesis in Microcystis aeruginosa PCC7806. Ecotoxicology 2012, 21, 811-819.
69. Phelan, R.R.; Downing, T.G. A growth advantage for microcystin production by Microcystis PCC7806 under high light. J. Phycol. 2011, 47, 1241-1246.
70. Deblois, C.P.; Juneau, P. Relationship between photosynthetic processes and microcystin in Microcystis aeruginosa grown under different photon irradiances. Harmful Algae 2010, 9, 18-24.
71. Sevilla, E.; Martin-Luna, B.; Vela, L.; Bes, M.T.; Fillat, M.F.; Peleato, M.L. Iron availability affects mcyD expression and microcystin-LR synthesis in Microcystis aeruginosa PCC7806. Environ. Microbiol. 2008, 10, 2476-2483.
72. Gehringer, M.M.; Adler, L.; Roberts, A.A.; Moffitt, M.C.; Mihali, T.K.; Mills, T.J.T.; Fieker, C.; Neilan, B.A. Nodularin, a cyanobacterial toxin, is synthesized in planta by symbiotic Nostoc sp. ISME J. 2012, 6, 1834-1847.
73. Mazur-Marzec, H.; Meriluoto, J.; Plinski, M.; Szafranek, J. Characterization of nodularin variants in Nodularia spumigena from the Baltic Sea using liquid chromatography/mass spectrometry/mass spectrometry. Rapid Commun. Mass Spectrom. 2006, 20, 2023-2032.
74. Camargo, S.; Valladares, A.; Flores, E.; Herrero, A. Transcription activation by NtcA in the absence of consensus NtcA-binding sites in an anabaena heterocyst differentiation gene promoter. J. Bacteriol. 2012, 194, 2939-2948.
75. Jonasson, S.; Vintila, S.; Sivonen, K.; El-Shehawy, R. Expression of the nodularin synthetase genes in the Baltic Sea bloom-former cyanobacterium Nodularia spumigena strain AV1. FEMS Microbiol. Ecol. 2008, 65, 31-39.
76. Vintila, S.; El-Shehawy, R. Ammonium ions inhibit nitrogen fixation but do not affect heterocyst frequency in the bloom-forming cyanobacterium Nodularia spumigena strain AV1. Microbiology 2007, 153, 3704-3712.
77. Meissner, S.; Fastner, J.; Dittmann, E. Microcystin production revisited: Conjugate formation makes a major contribution. Environ. Microbiol. 2013, 15, 1810-1820.
78. Vob, B.; Bolhuis, H.; Fewer, D.P.; Kopf, M.; Moke, F.; Haas, F.; El-Shehawy, R.; Hayes, P.; Bergman, B.; Sivonen, K.; et al. Insights into the physiology and ecology of the brackish-water-adapted cyanobacterium Nodularia spumigena CCY9414 based on a genome-transcriptome analysis. PLoS One 2013, 8, e60224.
79. Lehtimaki, J.; Moisander, P.; Sivonen, K.; Kononen, K. Growth, nitrogen fixation, and nodularin production by two baltic sea cyanobacteria. Appl. Environ. Microbiol. 1997, 63, 1647-1656.
80. Schembri, M.; Neilan, B.; Saint, C. Identification of genes implicated in toxin production in the cyanobacterium Cylindrospermopsis raciborskii. Environ. Toxicol. 2001, 16, 413-421.
81. Mazmouz, R.; Chapuis-Hugon, F.; Mann, S.; Pichon, V.; Mejean, A.; Ploux, O. Biosynthesis of cylindrospermopsin and 7-epicylindrospermopsin in Oscillatoria sp. strain PCC 6506: Identification of the cyr gene cluster and toxin analysis. Appl. Environ. Microbiol. 2010, 76, 4943-4949.
82. Harada, K.I.; Ohtani, I.; Iwamoto, K.; Suzuki, M.; Watanabe, M.F.; Watanabe, M.; Terao, K. Isolation of cylindrospermopsin from a cyanobacterium Umezakia natans and its screening method. Toxicon 1994, 32, 73-84.
83. Banker, R.; Carmeli, S.; Hadas, O.; Teltsch, B.; Porat, R.; Sukenik, A. Identification of cylindrospermopsin in Aphanizomenon ovalisporum (Cyanophyceae) isolated from lake Kinneret, Israel. J. Phycol. 1997, 33, 613-616.
84. Bittencourt-Oliveira, M.D.C.; Piccin-Santos, V.; Kujbida, P.; Moura, A.D.N. Cylindrospermopsin in Water Supply Reservoirs in Brazil Determined by Immunochemical and Molecular Methods. J. Water Resour. Prot. 2011, 3, 349-355.
85. Sinha, R.; Pearson, L.; Davis, T.; Muenchhoff, J.; Pratama, R.; Jex, A.; Burford, M.; Neilan, B. Comparative genomics of Cylindrospermopsis raciborskii strains with differential toxicities. BMC Genomics 2014, 15, doi:10.1186/1471-2164-15-83.
86. Ohtani, C.; Ikuko, M.; Runnegar, M. Cylindrospermopsin: A potent hepatotoxin from the blue-green alga Cylindrospermopsis raciborskii. J. Am. Chem. Soc. 1992, 114, 7941-7942.
87. Spoof, L.; Berg, K.; Rapala, J.; Lahti, K.; Lepist, L.; Metcalf, J.; Codd, G.; Meriluoto, J. First observation of cylindrospermopsin in Anabaena lapponica isolated from the boreal environment (Finland). Environ. Toxicol. 2006, 21, 552-560.
88. Sinha, R.; Pearson, L.; Davis, T.; Burford, M.; Orr, P.; Neilan, B. Increased incidence of Cylindrospermopsis raciborskii in temperate zones, is climate change responsible? Water Res. 2012, 46, 1408-1419.
89. Kinnear, S. Cylindrospermopsin: A decade of progress on bioaccumulation research. Mar. Drugs 2010, 8, 542-564.
90. Banker, R.; Carmeli, S.; Werman, M.; Teltsch, B.; Porat, R.; Sukenik, A. Uracil moiety is required for toxicity of the cyanobacterial hepatotoxin cylindrospermopsin. J. Toxicol. Environ. Health Part A 2001, 62, 281-288.
91. Banker, R.; Teltsch, B.; Sukenik, A.; Carmeli, S. 7-Epicylindrospermopsin, a toxic minor metabolite of the cyanobacterium Aphanizomenon ovalisporum from Lake Kinneret, Israel. J. Nat. Prod. 2000, 63, 387-389.
92. Li, R.; Carmichael, W.W.; Brittain, S.; Eaglesham, G.K.; Shaw, G.R.; Liu, Y.; Watanabe, M.M. First report of the cyanotoxins cylindrospermopsin and deoxycylindrospermopsin from Raphidiopsis curvata (Cyanobacteria). J. Phycol. 2001, 37, 1121-1126.
93. Briand, J.-F.; Jacquet, S.; Bernard, C.; Humbert, J.-F. Health hazards for terrestrial vertebrates from toxic cyanobacteria in surface water ecosystems. Vet. Res. 2003, 34, 361-377.
94. Chiswell, R.K.; Shaw, G.R.; Eaglesham, G.; Smith, M.J.; Norris, R.L.; Seawright, A.A.; Moore, M.R. Stability of cylindrospermopsin, the toxin from the cyanobacterium, Cylindrospermopsis raciborskii: Effect of pH, temperature, and sunlight on decomposition. Environ. Toxicol. 1999, 14, 155-161.
95. Wormer, L.; Cirés, S.; Carrasco, D.; Quesada, A. Cylindrospermopsin is not degraded by co-occurring natural bacterial communities during a 40-day study. Harmful Algae 2008, 7, 206-213.
96. Jiang, Y.; Xiao, P.; Yu, G.; Sano, T.; Pan, Q.; Li, R. Molecular basis and phylogenetic implications of deoxycylindrospermopsin biosynthesis in the cyanobacterium Raphidiopsis curvata. Appl. Environ. Microbiol. 2012, 78, 2256-2263.
97. Runnegar, M.T.; Xie, C.; Snider, B.B.; Wallace, G.A.; Weinreb, S.M.; Kuhlenkamp, J. In vitro hepatotoxicity of the cyanobacterial alkaloid cylindrospermopsin and related synthetic analogues. Toxicol. Sci. 2002, 67, 81-87.
98. Humpage, A.R.; Fontaine, F.; Froscio, S.; Burcham, P.; Falconer, I.R. Cylindrospermopsin genotoxicity and cytotoxicity: Role of cytochrome P-450 and oxidative stress. J. Toxicol. Environ. Health Part A 2005, 68, 739-753.
99. Froscio, S.M.; Humpage, A.R.; Burcham, P.C.; Falconer, I.R. Cylindrospermopsin induced protein synthesis inhibition and its dissociation from acute toxicity in mouse hepatocytes. Environ. Toxicol. 2003, 18, 243-251.
100. Runnegar, M.T.; Kong, S.-M.; Zhong, Y.-Z.; Ge, J.-L.; Lu, S.C. The role of glutathione in the toxicity of a novel cyanobacterial alkaloid cylindrospermopsin in cultured rat hepatocytes. Biochem. Biophys. Res. Commun. 1994, 201, 235-241.
101. Runnegar, M.T.; Kong, S.-M.; Zhong, Y.-Z.; Lu, S.C. Inhibition of reduced glutathione synthesis by cyanobacterial alkaloid cylindrospermopsin in cultured rat hepatocytes. Biochem. Pharmacol. 1995, 49, 219-225.
102. Bernard, C.; Harvey, M.; Briand, J.; Biré, R.; Krys, S.; Fontaine, J. Toxicological comparison of diverse Cylindrospermopsis raciborskii strains: Evidence of liver damage caused by a French C. raciborskii strain. Environ. Toxicol. 2003, 18, 176-186.
103. Falconer, I.R.; Humpage, A.R. Preliminary evidence for in vivo tumour initiation by oral administration of extracts of the blue green alga Cylindrospermopsis raciborskii containing the toxin cylindrospermopsin. Environ. Toxicol. 2001, 16, 192-195.
104. Rogers, E.; Zehr, R.; Gage, M.; Humpage, A.R.; Falconer, I.R.; Marr, M.; Chernoff, N. The cyanobacterial toxin, cylindrospermopsin, induces fetal toxicity in the mouse after exposure late in gestation. Toxicon 2007, 49, 855-864.
105. Saker, M.; Neilan, B.; Griffiths, D. Two morphological forms of Cylindrospermopsis raciborskii (cyanobacteria) isolated from Solomon Dam, Palm Island, Queensland. J. Phycol. 1999, 35, 599-606.
106. Byth, S. Palm Island mystery disease. Med. J. Aust. 1980, 2, 40-42.
107. Stuken, A.; Jakobsen, K. The cylindrospermopsin gene cluster of Aphanizomenon sp. strain 10E6: Organization and recombination. Microbiology 2010, 156, 2438-2451.
108. Mihali, T.K.; Kellmann, R.; Muenchhoff, J.; Barrow, K.D.; Neilan, B.A. Characterization of the gene cluster responsible for cylindrospermopsin biosynthesis. Appl. Environ. Microbiol. 2008, 74, 716-722.
109. Muenchhoff, J.; Siddiqui, K.S.; Poljak, A.; Raftery, M.J.; Barrow, K.D.; Neilan, B.A. A novel prokaryotic L-arginine:glycine amidinotransferase is involved in cylindrospermopsin biosynthesis. FEBS J. 2010, 277, 3844-3860.
110. Shalev-Malul, G.; Lieman-Hurwitz, J.; Viner-Mozzini, Y.; Sukenik, A.; Gaathon, A.; Lebendiker, M.; Kaplan, A. An AbrB-like protein might be involved in the regulation of cylindrospermopsin production by Aphanizomenon ovalisporum. Environ. Microbiol. 2008, 10, 988-999.
111. Davis, T.W.; Orr, P.T.; Boyer, G.L.; Burford, M.A. Investigating the production and release of cylindrospermopsin and deoxy-cylindrospermopsin by Cylindrospermopsis raciborskii over a natural growth cycle. Harmful Algae 2014, 31, 18-25.
112. Saker, M.L.; Neilan, B.A. Varied diazotrophies, morphologies, and toxicities of genetically similar isolates of Cylindrospermopsis raciborskii (nostocales, cyanophyceae) from Northern Australia. Appl. Environ. Microbiol. 2001, 67, 1839-1845.
113. Stucken, K. Physiogenomics of Cylindrospermopsis raciborskii and Raphidiopsis brookii with Emphasis on Cyanobacterial Evolution, Nitrogen Control and Toxin Biosynthesis. In Faculty of Biology and Chemistry; University of Bremen: Bremen, Germany, 2010; p. 222.
114. Bacsi, I.; Vasas, G.; Suranyi, G.; M-Hamvas, M.; Mathe, C.; Toth, E.; Grigorszky, I.; Gaspar, A.; Toth, S.; Borbely, G. Alteration of cylindrospermopsin production in sulfate-or phosphate-starved cyanobacterium Aphanizomenon ovalisporum. FEMS Microbiol. Lett. 2006, 259, 303-310.
115. Bar-Yosef, Y.; Sukenik, A.; Hadas, O.; Viner-Mozzini, Y.; Kaplan, A. Enslavement in the water body by toxic Aphanizomenon ovalisporum, inducing alkaline phosphatase in phytoplanktons. Curr. Biol. 2010, 20, 1557-1561.
116. Burford, M.A.; Davis, T.W.; Orr, P.T.; Sinha, R.; Willis, A.; Neilan, B.A. Nutrient-related changes in the toxicity of field blooms of the cyanobacterium, Cylindrospermopsis raciborskii. FEMS Microbiol. Ecol. 2014, doi:10.1111/1574-6941.12341.
117. Orr, P.T.; Rasmussen, J.P.; Burford, M.A.; Eaglesham, G.K.; Lennox, S.M. Evaluation of quantitative real-time PCR to characterise spatial and temporal variations in cyanobacteria, Cylindrospermopsis raciborskii (Woloszynska) Seenaya et Subba Raju and cylindrospermopsin concentrations in three subtropical Australian reservoirs. Harmful Algae 2010, 9, 243-254.
118. Mohamed, Z.A.; Al-Shehri, A.M. Assessment of cylindrospermopsin toxin in an arid Saudi lake containing dense cyanobacterial bloom. Environ. Monit. Assess. 2013, 185, 2157-2166.
119. Dyble, J.; Tester, P.A.; Litaker, R.W. Effects of light intensity on cylindrospermopsin production in the cyanobacterial HAB species Cylindrospermopsis raciborskii. Afr. J. Mar. Sci. 2006, 28, 309-312.
120. Bormans, M.; Lengronne, M.; Brient, L.; Duval, C. Cylindrospermopsin accumulation and release by the benthic cyanobacterium Oscillatoria sp. PCC 6506 under different light conditions and growth phases. Bull. Environ. Contam. Toxicol. 2014, 92, 243-247.
121. Wu, Z.; Shi, J.; Yang, S. The effect of pyrogallic acid on growth, oxidative stress, and gene expression in Cylindrospermopsis raciborskii (Cyanobacteria). Ecotoxicology 2013, 22, 271-278.
122. Cadel-Six, S.; Iteman, I.; Peyraud-Thomas, C.; Mann, S.; Ploux, O.; Mejean, A. Identification of a polyketide synthase coding sequence specific for anatoxin-a-producing Oscillatoria cyanobacteria. Appl. Environ. Microbiol. 2009, 75, 4909-4912.
123. Sivonen, K.; Jones, G. Cyanobacterial Toxins. In Toxic Cyanobacteria in Water; Chorus, I., Bartram, J., Eds.; WHO E & FN Spon Publishers: London, UK, 1999.
124. Osswald, J.; Rellan, S.; Gago, A.; Vasconcelos, V. Toxicology and detection methods of the alkaloid neurotoxin produced by cyanobacteria, anatoxin-a. Environ. Int. 2007, 33, 1070-1089.
125. Carmichael, W.; Gorham, P.; Biggs, D. Two laboratory case studies on the oral toxicity to calves of the freshwater cyanophyte (blue-green alga) Anabaena flos-aquae NRC-44-1. Can. Vet. J. 1977, 18, 71-75.
126. Kaminski, A.; Bober, B.; Lechowski, Z.; Bialczyk, J. Determination of anatoxin-a stability under certain abiotic factors. Harmful Algae 2013, 28, 83-87.
127. Carmichael, N. The toxins of cyanobacteria. Sci. Am. 1994, 270, 78-86.
128. Wood, S.A.; Selwood, A.I.; Rueckert, A.; Holland, P.T.; Milne, J.R.; Smith, K.F.; Smits, B.; Watts, L.F.; Cary, C.S. First report of homoanatoxin-a and associated dog neurotoxicosis in New Zealand. Toxicon 2007, 50, 292-301.
129. Henriksen, P.; Carmichael, W.W.; An, J.; Moestrup, O. 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 1997, 35, 901-913.
130. Edwards, C.; Beattie, K.A.; Scrimgeour, C.M.; Codd, G.A. Identification of anatoxin-A in benthic cyanobacteria (blue-green algae) and in associated dog poisonings at Loch Insh, Scotland. Toxicon 1992, 30, 1165-1175.
131. Duy, T.N.; Lam, P.K.; Shaw, G.R.; Connell, D.W. Toxicology and risk assessment of freshwater cyanobacterial (blue-green algal) toxins in water. Rev. Environ. Contam. Toxicol. 2000, 163, 113-185.
132. Merel, S.; Clement, M.; Thomas, O. State of the art on cyanotoxins in water and their behaviour towards chlorine. Toxicon 2010, 55, 677-691.
133. Sanchez, J.A.; Otero, P.; Alfonso, A.; Ramos, V.; Vasconcelos, V.; Araoz, R.; Molgo, J.; Vieytes, M.R.; Botana, L.M. Detection of anatoxin-a and three analogs in Anabaena spp. cultures: New fluorescence polarization assay and toxin profile by LC-MS/MS. Toxins 2014, 6, 402-415.
134. Rantala-Ylinen, A.; Kana, S.; Wang, H.; Rouhiainen, L.; Wahlsten, M.; Rizzi, E.; Berg, K.; Gugger, M.; Sivonen, K. Anatoxin-a synthetase gene cluster of the cyanobacterium Anabaena sp. strain 37 and molecular methods to detect potential producers. Appl. Environ. Microbiol. 2011, 77, 7271-7278.
135. Méjean, A.; Mann, S.; Maldiney, T.; Vassiliadis, G.; Lequin, O.; Ploux, O. Evidence that biosynthesis of the neurotoxic alkaloids anatoxin-a and homoanatoxin-a in the cyanobacterium Oscillatoria PCC 6506 occurs on a modular polyketide synthase initiated by L-proline. J. Am. Chem. Soc. 2009, 131, 7512-7513.
136. Peary, J.A.; Gorham, P.R. Influence of light and temperature on growth and toxin production by Anabaena flos-aquae. J. Phycol. 1966, 2, 1-3.
137. Gupta, N.; Bhaskar, A.S.B.; Rao, P.V.L. Growth characteristics and toxin production in batch cultures of Anabaena flos-aquae: Effects of culture media and duration. World J. Microbiol. Biotechnol. 2002, 18, 29-35.
138. Rapala, J.; Sivonen, K.; Luukkainen, R.; Niemelä, S. Anatoxin-a concentration in Anabaena and Aphanizomenon under different environmental conditions and comparison of growth by toxic and non-toxic Anabaena-strains-A laboratory study. J. Appl. Phycol. 1993, 5, 581-591.
139. Bumke-Vogt, C.; Mailahn, W.; Rotard, W.; Chorus, I. A highly sensitive analytical method for the neurotoxin anatoxin-a, using GC-ECD, and first application to laboratory cultures. Phycologia 1996, 35, 51-61.
140. Rapala, J.; Sivonen, K. Assessment of environmental conditions that favor hepatotoxic and neurotoxic Anabaena spp. strains cultured under light limitation at different temperatures. Microb. Ecol. 1998, 36, 181-192.
141. Araoz, R.; Nghiem, H.O.; Rippka, R.; Palibroda, N.; de Marsac, N.T.; Herdman, M. Neurotoxins in axenic oscillatorian cyanobacteria: Coexistence of anatoxin-a and homoanatoxin-a determined by ligand-binding assay and GC/MS. Microbiology 2005, 151, 1263-1273.
142. Kearns, K.D.; Hunter, M.D. Green algal extracellular products regulate antialgal toxin production in a cyanobacterium. Environ. Microbiol. 2000, 2, 291-297.
143. Wiese, M.; Dagostino, P.M.; Mihali, T.K.; Moffitt, M.C.; Neilan, B.A. Neurotoxic alkaloids: Saxitoxin and its analogs. Mar. Drugs 2010, 8, 2185-2211.
144. Strichartz, G. Structural determinants of the affinity of saxitoxin for neuronal sodium channels. Electrophysiological studies on frog peripheral nerve. J. Gen. Physiol. 1984, 84, 281-305.
145. Wang, J.; Salata, J.J.; Bennett, P.B. Saxitoxin is a gating modifier of HERG K+ channels. J. Gen. Physiol. 2003, 121, 583-598.
146. Su, Z.; Sheets, M.; Ishida, H.; Li, F.; Barry, W.H. Saxitoxin blocks L-type ICa. J. Pharmacol. Exp. Ther. 2004, 308, 324-329.
147. Nicholson, B.; Shaw, G.R.; Morrall, J.; Senogles, P.; Woods, T.; Papageorgiou, J.; Kapralos, C.; Wickramasinghe, W.; Davis, B.; Eaglesham, G. Chlorination for degrading saxitoxins (paralytic shellfish poisons) in water. Environ. Technol. 2003, 24, 1341-1348.
148. Jones, G.J.; Negri, A.P. Persistence and degradation of cyanobacterial paralytic shellfish poisons (PSPs) in freshwaters. Water Res. 1997, 31, 525-533.
149. Kellmann, R.; Mihali, T.; Jeon, Y.; Pickford, R.; Pomati, F.; Neilan, B. Biosynthetic intermediate analysis and functional homology reveal a saxitoxin gene cluster in cyanobacteria. Appl. Environ. Microbiol. 2008, 74, 4044-4053.
150. Stuken, A.; Campbell, R.; Quesada, A.; Sukenik, A.; Dadheech, P.; Wiedner, C. Genetic and morphologic characterization of four putative cylindrospermopsin producing species of the cyanobacterial genera Anabaena and Aphanizomenon. J. Plankton Res. 2009, 31, 465-480.
151. Soto-Liebe, K.; Murillo, A.A.; Krock, B.; Stucken, K.; Fuentes-Valdes, J.J.; Trefault, N.; Cembella, A.; Vasquez, M. Reassessment of the toxin profile of Cylindrospermopsis raciborskii T3 and function of putative sulfotransferases in synthesis of sulfated and sulfonated PSP toxins. Toxicon 2010, 56, 1350-1361.
152. Plominsky, Á.M.; Soto-Liebe, K.; Vásquez, M. Optimization of 2D-PAGE protocols for proteomic analysis of two nonaxenic toxin-producing freshwater cyanobacteria: Cylindrospermopsis raciborskii and Raphidiopsis sp. Lett. Appl. Microbiol. 2009, 49, 332-337.
153. Tsuchiya, S.; Cho, Y.; Konoki, K.; Nagasawa, K.; Oshima, Y.; Yotsu-Yamashita, M. Synthesis and identification of proposed biosynthetic intermediates of saxitoxin in the cyanobacterium Anabaena circinalis (TA04) and the dinoflagellate Alexandrium tamarense (Axat-2). Org. Biomol. Chem. 2014, 12, 3016-3020.
154. Mihali, T.; Kellmann, R.; Neilan, B. Characterisation of the paralytic shellfish toxin biosynthesis gene clusters in Anabaena circinalis AWQC131C and Aphanizomenon sp. NH-5. BMC Biochem. 2009, 10, 8:1-8:13.
155. Chislock, M.F.; Sharp, K.L.; Wilson, A.E. Cylindrospermopsis raciborskii dominates under very low and high nitrogen-to-phosphorus ratios. Water Res. 2014, 49, 207-214.
156. Yunes, J.S.; de la Rocha, S.; Giroldo, D.; Silveira, S.B.D.; Comin, R.; Bicho, M.D.S.; Melcher, S.S.; Sant'anna, C.L.; Vieira, A.A.H. Release of carbohydrates and proteins by a subtropical strain of Raphidiopsis brookii (cyanobacteria) able to produce saxitoxin at three nitrate concentrations. J. Phycol. 2009, 45, 585-591.
157. Kellmann, R.; Neilan, B.A. Biochemical characterization paralytic shellfish toxin biosynthesis in vitro. J. Phycol. 2007, 43, 497-508.
158. Carneiro, R.L.; Santos, M.E.V.D.; Pacheco, A.B.F.; Azevedo, S.M.F.D.O.E. Effects of light intensity and light quality on growth and circadian rhythm of saxitoxins production in Cylindrospermopsis raciborskii (Cyanobacteria). J. Plankton Res. 2009, 31, 481-488.
159. Castro, D.; Vera, D.; Lagos, N.; Garcia, C.; Vasquez, M. The effect of temperature on growth and production of paralytic shellfish poisoning toxins by the cyanobacterium Cylindrospermopsis raciborskii C10. Toxicon 2004, 44, 483-489.
160. Dias, E.; Pereira, P.; Franca, S. Production of paralytic shellfish toxin Aphanizomenon sp. LMECYA 31 (Cyanobacteria). J. Phycol. 2002, 38, 705-712.
161. Pomati, F.; Rossetti, C.; Manarolla, G.; Burns, B.P.; Neilan, B.A. Interactions between intracellular Na+ levels and saxitoxin production in Cylindrospermopsis raciborskii T3. Microbiology 2004, 150, 455-461.