Variability of Microcystins and Its Synthetase Gene Cluster in Microcystis and Planktothrix Waterblooms in Shallow Lakes of Hungary


Waterbloom samples of Microcystis aeruginosa and Planktothrix agardhii were collected from a variety of ponds, lakes and reservoirs in Hungary. Samples were tested with matrix-assisted laser desorption/ionization–time-of-flight mass spectrometry (MALDI-TOF MS) to identify the microcystin forms. The concentration of the microcystins was measured with capillary electrophoresis and the toxicity was tested by sinapis test. DNA was extracted from the samples and tested using a range of primers linked to the biosynthesis of microcystin. All of the fourteen collected samples gave positive results for the presence of the mcy genes with PCR products with sizes between of 425 and 955 bp, respectively, indicating the presence of the genes implicated in the production of microcystins. The results showed that a wide range of microcystin (MC) forms were detected in the Microcystis containing samples, among which MC-LR, -RR, and -YR were the most common. The highest MC concentration was 15,701 mg g−1, which was detected in an angling pond. The samples containing Planktothrix agardhii were less toxic, and the most common form in this species was the Asp3-MC-LR.


  1. 1.

    Bacsi, I., Suranyi, Gy., Gonda, S., Gyemant, Gy., Vasas, G. (2011) Observation of sward destruction caused by irrigation with toxic microcystis morphospecies containing water in Southern Hungary. Bull. Environ. Contam. Toxicol. 86, 232–237.

    CAS  Article  Google Scholar 

  2. 2.

    Ballot, A., Pflugmacher, S., Wiegand, C., Kotut, K., Krienitz, L. (2003) Cyanobacterial toxins in Lake Baringo, Kenya. Limnologica 33, 2–9.

    CAS  Article  Google Scholar 

  3. 3.

    Belykh, O. I., Sorokovikova, E. G., Fedorova, G. A., Kaluzhnaya, O. V., Korneva, E. S., Sakirko, M. V., Sherbakova, T. A. (2011) Presence and genetic diversity of microcystin-producing cyanobacteria (Anabaena and Microcystis) in Lake Kotokel (Russia, Lake Baikal Region). Hydrobiologia 671, 241–252.

    CAS  Article  Google Scholar 

  4. 4.

    Chorus, I., Bartam, J. (1999) Toxic Cyanobacteria in Water–A Guide to their Public Health Consequences, Monitoring and Management. E and FN Spon, London.

    Book  Google Scholar 

  5. 5.

    Fastner, J., Erhard, M., Döhren, H. (2001) Determination of oligopeptide diversity within a natural population of Microcystis spp. (cyanobacteria) by typing single colonies by matrix-assisted laser desorption ionization-time of flight mass spectrometry. Appl. Environ. Microbiol. 67, 5069–5076.

    CAS  Article  Google Scholar 

  6. 6.

    Komárek, J., Anagnostidis, K. (2005) Cyanoprokaryota 2. Teil/2nd part: Oscillatoriales. In: Büdel, B., Gärtner, G., Krienitz, L., Schagerl, M. (eds) Süsswasser Flora von Mitteleuropa, Vol 19(2). Elsevier, Heidelberg, p. 759.

    Google Scholar 

  7. 7.

    Kós, P., Gorzó, G., Surányi, G., Borbély, G. (1995) Simple and efficient method for isolation and measurement of cyanobacterial hepetotoxins by plant tests (Sinapis alba L.) Anal. Biochem. 225, 49–53.

    Article  Google Scholar 

  8. 8.

    Kosol, S., Schmidt, J., Kurmayer, R. (2009) Variation in peptide net production and growth among strains of the toxic cyanobacterium Planktothrix spp. European J. Phycol. 44(1), 49–62.

    CAS  Article  Google Scholar 

  9. 9.

    Lindholm, T., Vesterkvist, P., Spoof, L., Lundberg-Niinistö, C., Meriluoto, J. (2003) Microcystin occurrence in lakes in Åland, SW Finland. Hydrobiologia 505, 129–138.

    CAS  Article  Google Scholar 

  10. 10.

    Marsalek, B., Blaha, L. (2004) Comparison of 17 biotests for detection of cyanobacterial toxicity. Environ. Toxicol. 19, 310–317.

    CAS  Article  Google Scholar 

  11. 11.

    Martins, J., Saker, M. L., Moreira, C., Welker, M., Fastner, J., Vasconcelos, V. M. (2009) Peptide diversity in strains of the cyanobacterium Microcystis aeruginosa isolated from Portuguese water supplies. Appl. Microbiol. Biotechnol. 82, 951–961.

    CAS  Article  Google Scholar 

  12. 12.

    Mbedi, S., Welker, M., Fastner, J., Wiedner, C. (2005) Variability of the microcystin synthetase gene cluster in the genus Planktothrix (Oscillatoriales, Cyanobacteria). FEMS Microbiol. Lett. 245, 299–306.

  13. 13.

    Mikalsen, B., Boison, G., Skulberg, O. M., Fastner, J., Davies, W., Gabrielsen, T. M., Rudi, K., Jakobsen, K. S. (2003) Natural variation in the microcystin synthetase operon mcyABC and impact on microcystin production in microcystis strains. J. Bacteriol. 185, 2774–2785.

    CAS  Article  Google Scholar 

  14. 14.

    Ouahid, Y., Pérez-Silva, G., Campo, F. F. (2005) Identification of potentially toxic environmental Microcystis by individual and multiple PCR amplification of specific microcystin synthetase gene regions. Environ. Toxicol. 20, 235–242.

    CAS  Article  Google Scholar 

  15. 15.

    Reynolds, C. S., Walsby, A. E. (1975) Water blooms. Biologia Rev. 50, 437–481.

    CAS  Article  Google Scholar 

  16. 16.

    Sekadende, B. C., Lyimo, T. J., Kurmayer, R. (2005) Microcystin production by cyanobacteria in the Mwanza Gulf (Lake Victoria, Tanzania). Hydrobiologia 543, 299–304.

    CAS  Article  Google Scholar 

  17. 17.

    Somlyódy, L. (1998) Use of models for eutrophication management: the Kis-Balaton case. Water Sci. Technol. 37, 165–175.

    Article  Google Scholar 

  18. 18.

    Tillett, D., Dittmann, E., Erhard, M., Döhren, H., Borner, T., Neilan, B. A. (2000) Structural organization of microcystin biosynthesis in Microcystis aeruginosa PCC7806: an integrated peptide-poliketide synthetase system. Chem. Biol. 7, 753–764.

    CAS  Article  Google Scholar 

  19. 19.

    Vasas, G., Gáspár, A., Páger, Cs., Surányi, Gy., M-Hamvas, M., Máthé, Cs., Borbély, Gy. (2004) Analysis of cyanobacterial toxins (anatoxin-a, cylindrospermopsin, microcystin-LR) by capillary electrophoresis. Electrophoresis 25, 108–115.

    CAS  Article  Google Scholar 

  20. 20.

    Vasas, G., Szydlowska, D., Gáspár, A., Welker, M., Trojanowicz, M., Borbély, G. (2006) Determination of microcystins in environmental samples using capillary electrophoresis. J. Biochem. Biophys. Meth. 66, 87–97.

    CAS  Article  Google Scholar 

  21. 21.

    Vasas, G., Gáspár, A., Surányi, Gy., Batta, Gy., Gyémánt, Gy., M-Hamvas, M., Máthé, Cs., Grigorszky, I., Molnár, E., Borbély, G. (2002) Capillary electrophoretic assay and purification of cylindrospermopsin, a cyanobacterial toxin from Aphanizomenon ovalisporum by plant test (Blue-Green Sinapis Test). Anal. Biochem. 2, 95–103.

    Article  Google Scholar 

  22. 22.

    Vasas, G., Bacsi, I., Suranyi, Gy., M-Hamvas, M., Mathe, Cs., Nagy, S. A., Borbely, Gy. (2010) Isolation of viable cell mass from frozen Microcystis viridis bloom containing microcystin-RR. Hydrobiologia 639, 147–151.

    CAS  Article  Google Scholar 

  23. 23.

    Vasconcelos, V., Sivonen, K., Evans, W. R., Carmichael, W. W., Namikoshi, M. (1996) Hepatotoxic microcystin diversity in cyanobacterial blooms collected in portuguese freshwaters. Water Res. 30, 2377–2384.

    CAS  Article  Google Scholar 

  24. 24.

    Vörös, L., Padisák, J. (1991) Relationship between phytoplankton biomass and chlorophyll-a in some shallow lakes in Central Europe. Hydrobiologia 215, 111–119.

    Article  Google Scholar 

  25. 25.

    Welker, M., Maršálek, B., Šejnohová, L., Von Döhren, H. (2006) Detection and identification of oligopeptides in colonies: toward an understanding of metabolic diversity. Peptides 27, 2090–2103.

    CAS  Article  Google Scholar 

  26. 26.

    Welker, M., Döhren, H. (2006) Cyanobacterial peptides-nature’s own combinatorial biosynthesis. FEMS Microbiol. Rev. 30, 530–563.

    CAS  Article  Google Scholar 

  27. 27.

    Welker, M., Fastner, J., Erhard, M., Döhren, H. (2002) Application of MALDIi-TOF Ms in cyanotoxin research. Environ. Toxicol. 17, 367–374.

    CAS  Article  Google Scholar 

  28. 28.

    Welker, M., Brunke, M., Preussel, K., Lippert, I., Döhren, H. (2004) Diversity and distribution of (Cyanobacteria) oligo-peptide chemotypes from natural communities studied by single-colony mass spectrometry. Microbiology 150, 1785–1796.

    CAS  Article  Google Scholar 

  29. 29.

    Willame, R., Jurczak, T., Iffly, J.-F., Kull, T., Meriluoto, J., Hoffmann, L. (2005) Distribution of hepatotoxic cyanobacterial blooms in Belgium and Luxembourg. Hydrobiologia 551, 99–117.

    CAS  Article  Google Scholar 

  30. 30.

    Yasuno, M., Yoshio, S., Kaya, K., Watanabe, M. M. (1998) Variations in the toxicity of Microcystis species to Moina macrocopa. Phycol. Res. 46, 31–36.

    CAS  Article  Google Scholar 

Download references

Author information



Corresponding author

Correspondence to G. Vasas.

Rights and permissions

This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (, which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Farkas, O., Gyémant, G., Hajdú, G. et al. Variability of Microcystins and Its Synthetase Gene Cluster in Microcystis and Planktothrix Waterblooms in Shallow Lakes of Hungary. BIOLOGIA FUTURA 65, 227–239 (2014).

Download citation


  • Microcystis
  • Planktothrix
  • waterbloom
  • microcystins