Alteration of Cylindrospermopsin Content of Aphanizomenon ovalisporum (Cyanobacteria, Nostocales) due to Step-Down from Combined Nitrogen to Dinitrogen


In this study we show that cylindrospermopsin (a cyanotoxin) content of filaments of Aphanizomenon ovalisporum ILC164 depended on growth on combined nitrogen or nitrogen fixation. Our results also demonstrated that the shift down of cyanobacterial filaments from combined nitrogen to dinitrogen fixing condition resulted in a significant decrease of cylindrospermopsin pool size which resumed a growth rate dependent manner as the heterocyst and nitrogenase formation appeared. The current study indicated that alteration of nitrogen metabolism of Aphanizomenon ovalisporum (Forti) induced changes in cyanotoxin (cylindrospermopsin) metabolism. In addition, this is the first report that isolated heterocysts, the differentiated anaerobic cells for nitrogen fixation of cyanobacteria, did not contain cylindrospermopsin.

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G. Vasas, G. Surányi, I. Bácsi, M. M-Hamvas, C. Máthé, S. Gonda and G. Borbely, "Alteration of Cylindrospermopsin Content of Aphanizomenon ovalisporum (Cyanobacteria, Nostocales) due to Step-Down from Combined Nitrogen to Dinitrogen," Advances in Microbiology, Vol. 3 No. 8, 2013, pp. 557-564. doi: 10.4236/aim.2013.38075.

Conflicts of Interest

The authors declare no conflicts of interest.


[1] C. P. Wolk, “Heterocysts,” In: N. G. Carr and B. A. Whitton, Eds., The Biology of Cyanobacteria, University of California Press, 1982, pp. 359-386.
[2] W. J. Buikema and R. Haselkorn, “Molecular Genetics of Cyanobacterial Development,” Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 44, 1993, pp. 33-52.
[3] C. P. Wolk, A. Ernst and J. Elhai, “Heterocyst Metabolism and Development,” In: D. A. Bryant, Ed., The Molecular Biology of Cyanobacteria. Dordrecht, Kluwer Academic Publishers, The Netherlands, 1994. pp. 769-823.
[4] H. Böhme, “Regulation of Nitrogen Fixation in Heterocyst-Forming Cyanobacteria,” Trends in Plant Science, Vol. 3, 1998, pp. 346-351.
[5] D. G. Adams and P. S. Duggan, “Tansley Review No. 107. Heterocyst and Akinete Differentiation in Cyanobacteria,” New Phytologist, Vol. 144, 1999, pp. 3-33.
[6] A. Herrero, A. M. Muro-Pastor, A. Valladares and E. Flores, “Cellular Differentiation and the NtcA Transcription Factor in Filamentous Cyanobacteria,” FEMS Microbiology Reviews, Vol. 28, 2004, pp. 469-487.
[7] L. R. Oliver and G. G. Ganf, “Freshwater Blooms,” In: B. A. Whitton, and M. Potts, Eds., The Ecology of Cyanobacteria—Their Diversity in Time and Space, Kluwer Academic, Dordrecht, The Netherlands, 2000, pp. 149-194.
[8] I. R. Falconer, “Algal Toxins in Seafood and Drinking Water,” Academic Press, Waltham, 1993.
[9] I. Chorus and J. Bartram, Eds., “Toxic Cyanobacteria in Water: A Guide to Their Public Health Consequences, Monitoring and Management,” CRC Press, Boca Raton, 1999.
[10] C. S. Dow and U. K. Swoboda, “Cyanotoxins,” In: B. A. Whitton and M. Potts, Eds., The Ecology of Cyanobacteria, Kluwer Academic Publishers, The Netherlands, 2002, pp. 613-632..
[11] G. A. Codd and G. K. Poon, “Cyanobacterial Toxins,” In: L. J. Rogers and J. R. Gallon, Eds., Biochemistry of the Algae and Cyanobacteria, Oxford University Press, Oxford, 1989.
[12] P. R. Hawkins, M. T. Runnegar, A. R. Jackson and I. R. Falconer, “Severe Hepatotoxicity Caused by the Tropical Cyanobacterium (Blue-Green Alga) Cylindrospermopsis raciborskii (Woloszynska) Seenaya and Subba Raju Isolated from a Domestic water Supply Reservoir,” Applied Environmental Microbiology, Vol. 50, 1985, pp. 1292-1295.
[13] W. W. Carmichael, “Cyanobacteria Secondary Metabolites—The Cyanotoxins,” Journal of Applied Microbiology, Vol. 72, 2008, pp. 445-459.
[14] S. G. Bell and G. A. Codd, “Cyanobacterial Toxins and Human Health,” Reviews in Medical Microbiology, Vol. 5, 1994, pp. 256-264.
[15] M. L. Saker and D. J. Griffiths, “The Effect of Temperature on Growth and Cylindrospermopsin Content of Seven Isolates of Cylindrospermopsis raciborskii (Nostocales, Cyanophyceae) from Water Bodies in Northern Australia,” Phycologia, Vol. 39, 2000, pp. 349-354.
[16] R. Banker, S. Carmeli, O. Hadas, B. Teltsch, et al., “Identification of Cylindrospermopsin in Aphanizomenon ovalisporum (Cyanophyceae) Isolated from Lake Kinneret, Israel 1,” Journal of Phycology, Vol. 33, 1997, pp. 613-616.
[17] N. Tandeau de Marsac and J. Houmard, “Adaptation of Cyanobacteria to Environmental Stimuli: New Steps towards Molecular Mechanisms,” FEMS Microbiology Letters, Vol. 104, 1993, pp. 119-189.
[18] A. Herrero and E. Flores, Eds., “The Cyanobacteria: Molecular Biology, Genomics and Evolution,” Caister Academic Press, Norfolk, 2008.
[19] I. Bácsi, G. Vasas, G. Surányi, M. M-Hamvas, et al., “Alteration of Cylindrospermopsin Production in Sulfateor Phosphate-Starved Cyanobacterium Aphanizomenon ovalisporum,” FEMS Microbiology Letters, Vol. 259, 2006, pp. 303-310.
[20] D. G. Adams, “Heterocyst Formation in Cyanobacteria,” Current Opinion in Microbiology, Vol. 3, 2000, pp. 618624.
[21] P. Fay, “Heterocyst isolation,” Methods in Enzymology, Vol. 69, 1980, pp. 801-812.
[22] J. Udvardy, G. Borbely, A. Juhász and G. L. Farkas, “Thioredoxins and the Redox Modulation of Glucose-6-Phosphate Dehydrogenase in Anabaena sp. Strain PCC 7120 Vegetative Cells and Heterocysts,” Journal of Bacteriology, Vol. 157, 1984, pp. 681-683.
[23] U. K. Laemmli, “Cleavage of Structural Proteins during the Assembly of the Head of Bacteriophage T4,” Nature, Vol. 227, 1970, pp. 680-685.
[24] H. Towbin and J. Gordon, “Immunoblotting and Dot Immunobinding: Current Status and Outlook,” Journal of Immunological Methods, Vol. 72, 1984, pp. 313-340.
[25] S. Bradley and N. G. Carr, “Heterocyst Development in Anabaena cylindrica: The Necessity for Light as an Initial Trigger and Sequential Stages of Commitment,” Journal of General Microbiology, Vol. 101, 1977, pp. 291-297.
[26] J. Muenchhoff, K.S. Siddiqui, A. Poljak, M.J. Raftery, et al., “A Novel Prokaryotic l-Arginine: Glycine Amidinotransferase Is Involved in Cylindrospermopsin Biosynthesis,” FEBS Journal, Vol. 277, 2010, pp. 3844-3860.
[27] G. Vasas, A. Gáspár, G. Surányi, G. Batta, et al., “Capillary Electrophoretic Assay and Purification of Cylindrospermopsin, a Cyanobacterial Toxin from Aphanizomenon ovalisporum, by Plant Test (Blue-Green Sinapis Test),” Analytical Biochemistry, Vol. 302, 2002, pp. 95-103.
[28] G. Vasas, A. Gaspar, C. Pager, G. Suranyi, et al., “Analysis of Cyanobacterial Toxins (Anatoxin-A, Cylindrospermopsin, Microcystin-LR) by Capillary Electrophoresis,” Electrophoresis, Vol. 25, 2004, pp.108-115.
[29] X. Xu, J. Elhai and C. P. Wolk, “Transcriptional and Developmental Responses by Anabaena to Deprivation of Fixed Nitrogen,” In: A. Herrero and E. Flores, Eds., The Cyanobacteria: Molecular Biology, Genomics and Evolution, Caister Academic Press, Norfolk, 2008, pp. 383-422.
[30] P. R. Hawkins, N. R. Chandrasena, G. J. Jones, A. R. Humpage and I. R. Falconer, “Isolation and Toxicity of Cylindrospermopsis raciborskii from an Ornamental Lake,” Toxicon, Vol. 35, 1997, pp. 341-346.
[31] S. M. Froscio, A. R. Humpage, P. C. Burcham and I. R. Falconer, “Cell-Free Protein Synthesis Inhibition Assay for the Cyanobacterial Toxin Cylindrospermopsin,” Environmental Toxicology, Vol. 16, 2001, pp. 408-412.
[32] E. Valério, P. Pereira, M. L. Saker, S. Franca and R. Tenreiro, “Molecular Characterization of Cylindrospermopsis raciborskii Strains Isolated from Portuguese Freshwaters,” Harmful Algae, Vol. 4, 2005, pp. 1044-1052.
[33] J. S. Metcalf, A. Barakate and G. A. Codd, “Inhibition of Plant Protein Synthesis by the Cyanobacterial Hepato toxin, Cylindrospermopsin,” FEMS Microbiology Letters, Vol. 235, 2004, pp. 125-129.
[34] S. M. Froscio, A. R. Humpage, W. Wickramasinghe, G. Shaw and I .R. Falconer, “Interaction of the Cyanobacterial Toxin Cylindrospermopsin with the Eukaryotic Protein Synthesis System,” Toxicon, Vol. 51, 2008, pp.191-198.
[35] A. R. Humpage, M. Fenech, P. Thomas and I. R. Falconer, “Micronucleus Induction and Chromosome Loss in Transformed Human White Cells Indicate Clastogenic and Aneugenic Action of the Cyanobacterial Toxin, Cylindrospermopsin,” Mutation Research, Vol. 472, 2000, pp. 155-161.
[36] P. J. Murphy and C. W. Thomas, “The Synthesis and Biological Activity of the Marine Metabolite Cylindrospermopsin,” Chemical Society Reviews, Vol. 30, No. 5, 2001, pp. 303-312.
[37] A. Torokne, A. Palovics and M. Bankine, “Allergenic (Sensitization, Skin and Eye Irritation) Effects of Freshwater Cyanobacteria—Experimental Evidence,” Environmental Toxicology, Vol. 16, No. 6, 2001, 512-516.
[38] D. L. Burgoyne, T. K. Hemscheidt, R. E. Moore and M. T. Runnegar, “Biosynthesis of Cylindrospermopsin,” The Journal of Organic Chemistry, Vol. 65, No. 1, 2000, pp. 152-156.
[39] G. Shalev-Alon, A. Sukenik, O. Livnah, R. Schwarz and A. Kaplan, “A Novel Gene Encoding Amidinotransferase in the Cylindrospermopsin Producing Cyanobacterium Aphanizomenon ovalisporum,” FEMS Microbiology Letters, Vol. 209, No. 1, 2002, pp. 87-91.
[40] F. Neidhardt, “Escherichia coli and Salmonella typhimurium,” In: F. Neidhardt, J. Ingraham, K. Low, B. Magasanik, et al., Eds., “Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology,” Vol. 2, American Society for Microbiology, 1987, pp. 1313-1317.
[41] A. J. Van der Westhuizen and J. N. Eloff, “Effect of Culture Age and pH of Culture Medium on the Growth and Toxicity of the Blue-green Alga Microcystis aeruginosa,” Zeitschrift für Pflanzenphysiologie, Vol. 110, No. 2, 1983, pp. 157-163.
[42] P. T. Orr and G. J. Jones, “Relationship between Microcystin Production and Cell Division Rates in NitrogenLimited Microcystis aeruginosa Cultures,” Limnology and Oceanography, Vol. 43, No. 7, 1998, pp. 1604-1614.
[43] M. K. Rogalus and M. C. Watzin, “Evaluation of Sampling and Screening Techniques for Tiered Monitoring of Toxic Cyanobacteria in Lakes,” Harmful Algae, Vol. 7, No. 4, 2008, pp. 504-514.
[44] K. Sivonen, “Effects of Light, Temperature, Nitrate, Orthophosphate, and Bacteria on Growth of and Hepatotoxin Production by Oscillatoria agardhii Strains,” Applied and Environmental Microbiology, Vol. 56, No. 9, 1990, pp. 2658-2666.
[45] J. Rapala, K. Sivonen, C. Lyra and S. I. Niemel?, “Variation of Microcystins, Cyanobacterial Hepatotoxins, in Anabaena spp. as a Function of Growth Stimuli,” Applied Environmental Microbiology, Vol. 63, No. 6, 1997, pp. 2206-2212.
[46] H. Fleming and R. Haselkorn, “Differentiation in Nostoc muscorum: Nitrogenase Is Synthesized in Heterocysts,” Proceedings of the National Academy of Sciencesof the United States of America, Vol. 70, No. 10, 1973, pp. 2727-2731.
[47] H. Fleming and R. Haselkorn, “The Program of Protein Synthesis during Heterocyst Differentiation in NitrogenFixing Blue-Green Algae,” Cell, Vol. 3, No. 2, 1974, 159-170.
[48] S. Janaki and C. P. Wolk, “Synthesis of Nitrogenase by Isolated Heterocysts,” Biochimica et Biophysica Acta, Vol. 696, No. 2, 1982, pp. 187-192.
[49] E. Talpasayi and K. Kale, “Induction of Heterocysts in the Blue-Green Alga Anabaena Ambigua,” Current Science, Vol. 36, 1967, pp. 218-219.
[50] S. A. Kulasooriya, N. J. Lang and P. Fay, “The Heterocysts of Blue-Green Algae. III. Differentiation and Nitrogenase Activity,” Proceedings of the Royal Society of London, Series B, Vol. 181, No. 1063, 1972, pp. 199209.

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