Skip to main content

Advertisement

SpringerLink
Log in

Identification of toxigenic Cyanobacteria of the genus Microcystis in the Curonian Lagoon (Baltic Sea)

  • Marine Biology
  • Published:
Oceanology Aims and scope

Abstract

In 2002–2008, seasonal (April–November) monitoring of the phytoplankton in the Russian part of the Curonian Lagoon at five fixed sites was performed. A total of 91 Cyanobacteria, 100 Bacillariophyta, 280 Chlorophyta, 21 Cryptophyta, and 24 Dinophyta species were found. Six potentially toxic species of cyanobacteria: Aphanizomenon flos-aquae, Anabaena sp., Microcystis aeruginosa, M. viridis, M. wesenbergii, and Planktothrix agardhii dominated the phytoplankton biomass and caused water blooms. The seasonal average phytoplankton biomass ranged from 30 to 137 g/m3. The cyanobacteria’s biomass varied from 10 to 113 g/m3 forming 30–82% of the total with a mean of 50%. With the aid of genetic markers (microcystin (mcy) and nodularin synthetases), six variants of the microcystin-producing gene mcyE from the genus Microcystis were identified. Due to the intensive and lengthy blooms of potentially toxic and toxigenic cyanobacteria, the environmental conditions in the Curonian Lagoon appear unfavorable. The water should be monitored for cyanotoxins with analytical methods in order to determine if the area is safe for recreational use.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. S. V. Aleksandrov and O. A. Dmitrieva, “Primary production and phytoplankton characteristics as eutrophication criteria of Kursiu Marios Lagoon, the Baltic Sea,” Water Resources 33(1), 97–103 (2006).

    Article  Google Scholar 

  2. S. V. Aleksandrov, Primary Production of Plankton in the Baltic Lagoons (the Vislinskii and Kurshskii Gulfs) (AtlantNIRO, Kalinigrad, 2010) [in Russian].

    Google Scholar 

  3. O. I. Belykh, A. S. Gladkikh, I. V. Tikhonova, and O. A. Dmitrieva, “Identification of the Genes Responsible for Toxin Synthesis in Cyanobacteria in Russian Reservoirs: Molecular-Biological Approach to Water Quality Assessment,” in The Tenth Congress of Hydrobiological Society, Russian Academy of Sciences, Abstract of Papers, Ed. by A. F. Alimov, et al. (Dal’nauka, Vladivostok, 2009), p. 39.

    Google Scholar 

  4. O. I. Belykh, I. V. Tikhonova, E. G. Sorokovikova, et al., “Detection of Toxic Microcystis in Lake Kotokelskoe (Buryatia),” Vestnic Tomsk State University, No. 330, 172–175 (2010).

  5. O. A. Dmitrieva, “Potentially Toxic Phytoplankton Species in Russian Area of the Kurshskii and Vislinskii Gulfs, the Baltic Sea,” in The Implications of the Study and Protection of Natural and Cultural Heritage in Kurshskaya Kosa National Park: Collection of Scientific Works (Ros. Gos. Univ., Kalinigrad, 2007), pp. 102–117.

    Google Scholar 

  6. V. V. Carmichael, V. M. Chernaenko, and I. Evans, “Cyclic Peptide Hepatotoxins of Freshwater Cyanobacteria (Blue-Green Algae) Collected in Blooming Reservoirs of Ukraine and European Russia),” Doklady RAN 330(5), 659–661 (1993).

    Google Scholar 

  7. Study Method of Biogeocenosises in Inland Reservoirs (Nauka, Moscow, 1975) [in Russian].

  8. S. N. Semenova and V. A. Smyslov, “Description of Phytocenosis of the Kurshskii Gulf (the Baltic Sea) in the Turn of XX–XXI Centuries,” in Collection of Scientific Transactions to the 40th Anniversary of Kaliningrad Branch of Hydrobiological Society, Russian Academy of Sciences; Hydrobiological Studies in the Baltic, Atlantic and Pacific Basins in the Turn of a Thousand Years (AtlantNIRO, Kaliningrad, 2005), pp. 17–64.

    Google Scholar 

  9. I. V. Tikhonova, A. S. Gladkikh, O. I. Belykh, and E. G. Sorokovikova, “Detection of potentially toxic cyanobacteria in Lake Baikal and reservoirs by polymerase chain reaction,” Bulletin of ESCC SB RAMS 2, 202–205 (2006).

    Google Scholar 

  10. P. I. Usachev, “Quantitative Method of Collection and Treatment of Phytoplankton,” in Transactions of All-Russian Hydrobiological Society (Akad. Nauk SSSR, Moscow, 1961), Vol. 11, pp. 411–415.

    Google Scholar 

  11. M. Balode and I. Purina, “Harmful Phytoplankton in the Gulf of Riga (the Baltic Sea),” in Harmful and Toxic Algal Blooms, Ed. by T. Yasumoto, et al. (Intergovernmental Oceanographic Commission of UNESCO, 1996), pp. 69–72.

  12. O. I. Belykh, E. G. Sorokovikova, G. A. Fedorova, et al., “Presence and Genetic Diversity of Microcystin-Producing Cyanobacteria (Anabaena and Microcystis) in Lake Kotokel (Russia, Lake Baikal Region),” Hydrobiologia 671, 241–252 (2011).

    Article  Google Scholar 

  13. Y. W. Chen, B. Q. Qin, and X. Y. Cai, “Prediction of Blue-Green Algal Bloom Using Stepwise Multiple Regressions between Algae and Related Environmental Factors in Meiliang Bay Lake Taihu,” J. Lake Science 13, 63–71 (2001).

    Google Scholar 

  14. I. Chorus and J. Bartram, Toxic Cyanobacteria in Water: A Guide to Public Health Significance, Monitoring and Management, Published on Behalf of WHO by E & FN Spon., (Chapman & Hall, London, 1999).

    Book  Google Scholar 

  15. D. P. Fewer, A. Tooming-Klunderud, J. Jokela, et al., “Natural Occurrence of Microcystin Synthetase Deletion Mutants Capable of Producing Microcystins in Strains of the Genus Anabaena (Cyanobacteria),” Microbiology 154, 1007–1014 (2008).

    Article  Google Scholar 

  16. N. A. Gaevsky, V. I. Kolmakov, O. I. Belykh, et al., “Ecological Development and Genetic Diversity of Microcystis aeruginosa from Artificial Reservoir in Russia,” J. Microbiology 49(5), 714–720 (2011).

    Article  Google Scholar 

  17. K. Halinen, J. Jokela, D. P. Fewer, et al., “Direct Evidence for Production of Microcystins by Anabaena Strains from the Baltic Sea,” AEM 73, 6543–6550 (2007).

    Google Scholar 

  18. P. Henriksen, “Toxic Freshwater Cyanobacteria in Denmark,” in Cyanotoxins — Occurrence, Causes, Consequences, Ed. by I. Chorus (Springer, Berlin, 2001), pp. 49–56.

    Google Scholar 

  19. S. Jonasson, S. Vintila, K. Sivonen, and R. El-Shehawy, “Expression of the Nodularin Synthetase Genes in the Baltic Sea Bloom-Former Cyanobacterium Nodularia spumigena Strain AV1,” FEMS Microbiol. Ecol. 65, 31–39 (2008).

    Article  Google Scholar 

  20. A.-D. Jungblut and A. B. Neilan, “Molecular Identification and Evolution of the Cyclic Peptide Hepatotoxins, Microcystin and Nodularin Synthetase Genes in Three Orders of Cyanobacteria,” Arch. Microbiol. 185 107–114 (2006).

    Article  Google Scholar 

  21. K. M. Karlsson, H. Kankaanpaa, M. Huttunen, and J. Meriluoto, “First Observation of Microcystin-LR in Pelagic Cyanobacterial Blooms in the Northern Baltic Sea,” Harmful Algae 4, 163–166 (2005).

    Article  Google Scholar 

  22. M. Kimura, “A Simple Method for Estimating Evolutionary Rate of Base Substitution through Comparative Studies of Nucleotide Sequences,” J. Mol. Evol. 16, 111–120 (1980).

    Article  Google Scholar 

  23. R. Kurmayer, E. Dittmann, J. Fastner, and I. Chorus, “Diversity of Microcystin Genes within a Population of the Toxic Cyanobacterium Microcystis spp. in Lake Wannsee (Berlin, Germany),” Microb. Ecol. 4, 107–118 (2002).

    Article  Google Scholar 

  24. R. Kurmayer, G. Christiansen, J. Fastner, and T. Börner, “Abundance of Active and Inactive Microcystin Genotypes in Populations of the Toxic Cyanobacterium Planktothrix spp.,” Environ. Microbiol. 6, 831–841 (2004).

    Article  Google Scholar 

  25. J. Lehtimäki, Characterization of Cyanobacterial Strains Originating from the Baltic Sea with Emphasis on Nodularia and Its Toxin, Nodularin (University of Helsinki, Helsinki, 2000).

    Google Scholar 

  26. B. Luckas, J. Dahlmann, K. Erler, et al., “Overview of Key Phytoplankton Toxins and Their Recent Occurrence in the North and Baltic Seas,” Environ. Toxicol. 20, 1–17 (2005).

    Article  Google Scholar 

  27. C. MacKintosh, K. A. Beattie, S. Klumpp, et al., “Cyanobacterial Microcystin-LR is a Potent and Specific Inhibitor of Protein Phosphatases 1 and 2A from Both Mammals and Higher Plants,” FEBS Lett. 264, 187–192 (1990).

    Article  Google Scholar 

  28. B. Marsalek, L. Blaha, J. Turanek, and J. Neca, “Microcystin-LR and Total Microcystins in Cyanobacterial Blooms in the Czech Republic 1993–1998,” in Cyanotoxins — Occurrence, Causes, Consequences, Ed. by I. Chorus (Springer-Verlag, Berlin, 2001), pp. 56–62.

    Google Scholar 

  29. H. Mazur and M. Plinski, “Nodularia spumigena Blooms and the Occurrence of Hepatotoxin in the Gulf of Gdansk,” Oceanologia 45, 305–316 (2003).

    Google Scholar 

  30. H. Mazur-Marzec, G. Browarczyk-Matusiak, K. Forycka, et al., “Morphological, Genetic, Chemical and Ecophysiological Characterization of Two Microcystis aeruginosa Isolates from the Vistula Lagoon, Southern Baltic,” Oceanologia 52, 127–146 (2010).

    Article  Google Scholar 

  31. M. C. Moffitt, S. I. Blackburn, and B. A. Neilan, “rRNA Sequences Reflect the Ecophysiology and Define the Toxic Cyanobacteria of the Genus Nodularia,” Int. J. Syst. Evol. Microbiol. 51, 505–512 (2001).

    Google Scholar 

  32. M. C. Moffitt and B. A. Neilan, “Characterization of the Nodularin Synthetase Gene Cluster and Proposed Evolution of Cyanobacterial Hepatotoxins,” AEM 70, 6353–6362 (2004).

    Google Scholar 

  33. I. Olenina, “Long-Term Changes in the Kursiu Maros Lagoon: Eutrophication and Phytoplankton Response,” Ecologija, No. 1, 56–65 (1998).

  34. B. Oudra, M. Loudiki, B. Sbiyyaa, et al., “Isolation, Characterization and Quantification of Microcystins (Heptapetides Hepatotoxins) in Microcystis aeruginosa Dominated Bloom of Lalla Takerkoust Lake-Reservoir (Morocco),” Toxicology 39, 1375–1381 (2001).

    Google Scholar 

  35. K. Ozawa, H. Fujioka, M. Muranaka, et al., “Spatial Distribution and Temporal Variation of Microcystis Species Composition and Microcystin Concentration in Lake Biwa,” Environ. Toxicol. 20, 270–276 (2005).

    Article  Google Scholar 

  36. A. Paldaviciene, H. Mazur-Marzec, and A. Razinkovas, “Toxic Cyanobacteria Blooms in the Lithuanian Part of the Curonian Lagoon,” Oceanologia 51, 203–216 (2009).

    Article  Google Scholar 

  37. D. Posada and K. L. Crandall, “MODELTEST: Testing the Model of DNA Substitution,” Bioinformatics 14, 817–818 (1998).

    Article  Google Scholar 

  38. A. Rantala, D. Fewer, M. Hisbergues, et al., “Phylogenetic Evidence for Early Evolution of Microcystin Synthesis,” PNAS 101, 568–573 (2004).

    Article  Google Scholar 

  39. A. Rantala, P. Rajaniemi-Wacklin, C. Lyra, et al., “Detection of Microcystin-Producing Cyanobacteria in Finnish Lakes with Genus-Specific Microcystin Synthetase Gene E (mcyE) PCR and Associations with Environmental Factors,” Appl. Environ. Microbiol. 72, 6101–6110 (2006).

    Article  Google Scholar 

  40. J. Rapala, K. Sivonen, R. Luukkainen, and S. I. Niemela, “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. Applied Phycol. 5, 581–591 (1993).

    Article  Google Scholar 

  41. R. D. Robarts and T. Zohary, “Temperature Effects on Photosynthetic Capacity, Respiration, and Growth Rates of Bloom-Forming Cyanobacteria,” N.Z. J. Mar. Freshwat. Res. 21, 391–399 (1987).

    Article  Google Scholar 

  42. L. Rouhiainen, T. Vakkilainen, B. L. Siemer, et al., “Genes Coding for Hepatotoxic Heptapeptides (Microcystins) in the Cyanobacterium Anabaena Strain 90,” Appl. Environ. Microbiol. 70(2), 686–692 (2004).

    Article  Google Scholar 

  43. K. Sivonen, M. Namikoshi, W. R. Evans, et al., “Isolation and Characterization of a Variety of Microcystins from Seven Strains of the Cyanobacterial Genus Anabaena,” Appl. Environ. Microbiol. 58, 2495–2500 (1992).

    Google Scholar 

  44. K. Sivonen and G. Jones, “Cyanobacterial Toxins,” in Toxic Cyanobacteria in Water: A Guide to Public Health Significance, Monitoring and Management, the World Health Organization, Ed. by I. Chorus, et al. (E & FN Spon., London, 1999), pp. 41–111.

    Google Scholar 

  45. H. Schmidt-Ries, “Untersuchungen zur Kennthis des Pelagies Eines Strange Wassres (Kurisches Haff),” in Zeitchriften fur Fisheri und deren Hilfwissenschiften, Vol. 37, No. 2, 325 (1940).

    Google Scholar 

  46. D. L. Swofford, PAUP: Phylogenetic Analysis Using Parsimony (and Other Methods), Ver. 4.0 (Mass, Sunderland, 2002).

  47. K. Tamura, J. Dudley, M. Nei, and S. Kumar, “MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) Software Ver. 4.0,” Mol. Biol. Evol. 24, 1596–1599 (2007).

    Article  Google Scholar 

  48. D. Tillett, D. L. Parker, and B. A. Neilan, “Detection of Toxigenicity by a Probe for the Microcystin Synthetase A Gene (mcyA) of the Cyanobacterial Genus Microcystis: Comparison of Toxicities with 16S rRNA and Phycocyanin Operon (Phycocyanin Intergenic Spacer) Phylogenies,” Appl. Environ. Microbiol. 67, 2810–2818 (2001).

    Article  Google Scholar 

  49. R. A. Vollenweider and J. Kerekes, “Eutrophication of Waters: Monitoring Assessment and Control,” in Paris: Organization for Economic Co-Operation and Development (OECD), 156 (1982).

  50. A. J. Van der Westhuizen and J. N. Eloff, “Effect of Temperature and Light on the Toxicity and Growth of the Blue-Green Alga Microcystis aeruginosa (UV-006),” Planta 163, 55–59 (1985).

    Article  Google Scholar 

  51. M. F. Watanabe, S. Oishi, K.-I. Harada, et al., “Toxins Contained in Microcystis Species of Cyanobacteria (Blue-Green Algae),” Toxicon 26, 1017–1025 (1988).

    Article  Google Scholar 

  52. World Health Organization: Guidelines for Drinking-Water Quality, 3rd ed., (World Health Organization, Geneva, 2004), Vol. 1, pp. 407–408.

  53. M. Yasuno, Y. Sugaya, K. Kaya, and M. M. Watanabe, “Variations in the Toxicity of Microcystis Species to Moina macrocopa,” Phycol. Res. 46,Suppl., 31–36 (1998).

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Limnological Institute, Siberian Branch, Russian Academy of Sciences, ul. Ulan-Batorskaya 3, Irkutsk, 664033, Russia

    O. I. Belykh, A. S. Gladkikh & E. G. Sorokovikova

  2. Atlantic Scientific Research Institute of Fisheries and Oceanography (AtlantNIRO), ul. Dm. Donskoi 5, Kaliningrad, 236000, Russia

    O. A. Dmitrieva

Authors
  1. O. I. Belykh
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. O. A. Dmitrieva
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. S. Gladkikh
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. E. G. Sorokovikova
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to O. I. Belykh.

Additional information

Original Russian Text © O.I. Belykh, O.A. Dmitrieva, A.S. Gladkikh, E.G. Sorokovikova, 2013, published in Okeanologiya, 2013, Vol. 53, No. 1, pp. 78–87.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Belykh, O.I., Dmitrieva, O.A., Gladkikh, A.S. et al. Identification of toxigenic Cyanobacteria of the genus Microcystis in the Curonian Lagoon (Baltic Sea). Oceanology 53, 71–79 (2013). https://doi.org/10.1134/S0001437013010025

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0001437013010025

Keywords

Search

Navigation