Skip to main content
Log in

Microcystins Induce Morphological and Physiological Changes in Selected Representative Phytoplanktons

  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Dissolved microcystins (MCs) are regularly present in water dominated by microcystin-producing, bloom-forming cyanobacteria. In vitro experiments with environmentally feasible concentrations (5 × 10−7 M) of the three most common microcystins, MC-LR, MC-RR, and MC-YR, revealed that they influence the metabolism of different representative phytoplanktons. At light intensities that are close to the cyanobacterial bloom environment (50 μmol m−2 s−1), they produce morphological and physiological changes in both microcystin-producing and -nonproducing Microcystis aeruginosa strains and also have similar effects on the green alga Scenedesmus quadricauda that is frequently present in cyanobacterial blooms. All three microcystin variants tested induce cell aggregation, increase in cell volume, and overproduction of photosynthetic pigments. All three effects appear to be related to each other but are not necessarily caused by the same mechanism. The biological activity of microcystins toward the light-harvesting complex of photobionts can be interpreted as a signal announcing the worsening of light conditions due to the massive proliferation of cyanobacteria. Although the function of microcystins is still unknown, it is evident that they have numerous effects on phytoplankton in nature. These effects depend on the individual organism as well as on the various intracellular and extracellular signaling pathways. The fact that dissolved microcystins also influence the physiology of microcystin-producing cyanobacteria leads us to the conclusion that the role of microcystins in the producing cells differs from the role in the water environment.

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

Access this article

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

Instant access to the full article PDF.

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6
Figure 7
Figure 8

Similar content being viewed by others

References

  1. Abe, T, Lawson, T, Weyers, JDB, Codd, GA (1996) Microcystin-LR inhibits photosynthesis of Phaseolus vulgaris primary leaves: implications for current spray irrigation practice. New Phytol 133: 651–658

    Article  CAS  Google Scholar 

  2. Allen, JF (1992) Protein phosphorylation in the regulation of photosynthesis. Biochim Biophys Acta 1098: 275–335

    Article  PubMed  CAS  Google Scholar 

  3. Campbell, D, Hurry, V, Clarke, AK, Gustafsson, P, Öquist, G (1998) Chlorophyll fluorescence analysis of cyanobacterial photosynthesis and acclimation. Microbiol Mol Biol Rev 62: 667–683

    PubMed  CAS  Google Scholar 

  4. Dittmann, E, Neilan, BA, Erhard, M, von Döhren, H, Börner, T (1997) Insertional mutagenesis of a peptide synthetase gene that is responsible for hepatotoxin production in the cyanobacterium Microcystis aeruginosa PCC 7806. Mol Microbiol 26: 779–787

    Article  PubMed  CAS  Google Scholar 

  5. Giardi, MT, Cona, A, Geiken, B (1995) Photosystem II core phosphorylation heterogeneity and the regulation of electron transfer in higher plants: a review. Bioelectrochem Bioenerg 38: 67–75

    Article  CAS  Google Scholar 

  6. Gliwicz, ZM (1990) Why do cladocerans fail to control algal blooms? Hydrobiol 200/201: 83–97

    Article  Google Scholar 

  7. Grach-Pogrebinsky, O, Sedmak, B, Carmeli, S (2003) Protease inhibitors from a Slovenian Lake Bled toxic waterbloom of the cyanobacterium Planktothrix rubescens. Tetrahedron 59: 8329–8336

    Article  CAS  Google Scholar 

  8. Hagmann, L, Jüttner, F (1996) Fischerellin A, a novel photosystem-II-inhibiting allelochemical of the cyanobacterium Fischerella muscicola with antifungal and herbicidal activity. Tetrahedron Lett 37: 6539–6542

    Article  CAS  Google Scholar 

  9. Haney, JF (1987) Field studies on zooplankton–cyanobacteria interactions. N Z J Marine Freshwater Res 21: 467–475

    Article  Google Scholar 

  10. Hesse, K, Dittmann, E, Börner, T (2001) Consequences of impaired microcystin production for light-dependent growth and pigmentation of Microcystis aeruginosa PCC 7806. FEMS Microbiol Ecol 39–43

  11. Hughes, EO, Gorham, PR, Zehnder, A (1958) Toxicity of an unialgal culture of Microcystis aeruginosa. Can J Microbiol 4: 225–236

    PubMed  CAS  Google Scholar 

  12. Jungmann, D, Ludwichowski, KU, Faltin, V, Benndorf, J (1996) A field study to investigate environmental factors that could effect microcystin synthesis of a Microcystis population in the Bautzen reservoir. Int Rev Gesamten Hydrobiol 81: 493–501

    CAS  Google Scholar 

  13. Kato, T, Watanabe, MF, Watanabe, M (1991) Alloenzyme divergence in Microcystis (Cyanophyceaea) and its taxonomic and phylogenetic inference. In: Hickel, B, Anagnostidis, K, Komarek, J (Eds.) Cyanophyta/Cyanobacteria—Morphology, Taxonomy, Ecology. Proceedings of the 11th Symposium of the IACR, Plon, Germany, 1989 (Arch Hydrobiol Suppl 92, Algological Studies 64: 129–140)

  14. Kolber, Z, Wyman, KD, Falkowski, PG (1990) Natural variability in photosynthetic energy conversion efficiency: a field study in the Gulf of Maine. Limnol Oceanogr 35: 72–79

    CAS  Google Scholar 

  15. Kromkamp, JC, Walsby, AE (1990) A computer model of buoyancy and vertical distributions in populations of Microcystis in two shallow lakes. J Plankton Res 13: 419–436

    Google Scholar 

  16. Kurmayer, R, Christiansen, G, Chorus, I (2003) The abundance of microcystin-producing genotypes correlates positively with colony size in Microcystis sp. and determines its microcystin net production in lake Wannsee. Appl Environ Microbiol 69(2): 787–795

    Article  PubMed  CAS  Google Scholar 

  17. Lazar, D (1999) Review—chlorophyll a fluorescence induction. Biochim Biophys Acta 1421: 1–28

    Article  Google Scholar 

  18. Lee, T, Tsuzuki, M, Takeuchi, T, Yokoyama, K, Karube, I (1994) In vivo fluorimetric method for early detection of cyanobacterial waterblooms. J Appl Phycol 6: 489–495

    Article  Google Scholar 

  19. Lin, CG (1972) Phytoplankton succession in Lake Valencia, Venezuela. Hydrobiologia 138: 189–203

    Google Scholar 

  20. MacKintosh, C, Beattie, KA, Klumpp, S, Cohen, P, Codd, GA (1990) Cyanobacterial microcystin-LR is a potent and specific inhibitor of protein phosphatases 1 and 2A from both mammalian and higher plants. FEBS 264: 187–192

    Article  CAS  Google Scholar 

  21. Papageorgiou, GC (1996) The photosynthesis of cyanobacteria (blue bacteria) from the perspective of signal analysis of chlorophyll a fluorescence. J Sci Ind Res 55: 596–617

    CAS  Google Scholar 

  22. Park, HD, Iwami, C, Watanabe, MF, Harada, KI, Okino, T, Hayashi, H (1998) Temporal variabilities of the concentrations of intra- and extracellular microcystin and toxic Microcystis species in a hypertrophic lake, Lake Suwa, Japan (1991–1994). Environ Toxicol Water Qual 13: 61–72

    Article  CAS  Google Scholar 

  23. Reynolds, CS (1975) Interrelations of photosynthetic behaviour and buoyancy regulation in a natural population of a blue-green alga. Freshwater Biol 5: 323–338

    Article  Google Scholar 

  24. Reynolds, CS (1984) The Ecology of Freshwater Phytoplankton. Cambridge University Press, Cambridge, p 384

    Google Scholar 

  25. Reynolds, CS, Thompson, JM, Ferguson, AJD, Wiseman, SW (1982) Loss processes in the population dynamics of phytoplankton maintained in closed systems. J Plankton Res 4: 561–600

    Article  Google Scholar 

  26. Sedmak, B, Kosi, G (1997) Microcystins in Slovene freshwaters (central Europe)—first report. Nat Toxins 5: 64–73

    PubMed  CAS  Google Scholar 

  27. Sedmak, B, Kosi, G (1998) The role of microcystins in heavy cyanobacterial bloom formation. J Plankton Res 20: 691–708

    Article  CAS  Google Scholar 

  28. Sedmak, B, Kosi, G (1998) Erratum. The role of microcystins in heavy cyanobacterial bloom formation. J Plankton Res 20: 1421

    Article  Google Scholar 

  29. Sedmak, B, Kosi, G (2002) Harmful cyanobacterial blooms in Slovenia-bloom types and microcystin producers. Acta Biol Slov 45: 17–30

    Google Scholar 

  30. Singh, DP, Tyagi, MB, Kumar, A, Thakur, JK, Kumar, A (2001) Antialgal activity of a hepatotoxin-producing cyanobacterium Microcystis aeruginosa. World J Microbiol Biotechnol 17: 15–22

    Article  CAS  Google Scholar 

  31. Sivonen, K (1990) Effects of light, temperature, nitrate, orthophosphate, and bacteria on growth of and hepatotoxin production by Oscillatoria agardhii strains. Appl Environ Microbiol 56: 2658–2666

    PubMed  CAS  Google Scholar 

  32. Smayda, TJ, Boleyn, BJ (1965) Experimental observations on the flotation of marine diatoms. I. Thalasiosira cf. nana, Thalassiosira rotula and Nitzschia seriata. Limnol Oceanogr 10: 499–509

    Article  Google Scholar 

  33. Sukenik, A, Eshkol, R, Livne, A, Hadas, O, Kaplan, A, Tcernov, D, Vardi, A, Rom, M (2002) Inhibition of growth and photosynthesis of the dinoflagellate Peridinium gatunense by Microcystis sp. (cyanobacteria): a novel allelopathic mechanism. Limnol Oceanogr 47: 1656–1663

    Article  Google Scholar 

  34. Thompson, AS, Rhodes, JC, Pettman, I (1988) Culture Collection of Algae and Protozoa—Catalogue of Strains, 5th Ed. Natural Environment Research Council, Titus Wilson and Son Ltd., Kendal, Ambleside, UK, p 22

  35. Tsuchiya, Y, Watanabe, M (1997) Disk type solid-phase extraction of microcystin in environmental water. Jpn J Toxicol Environ Health 43: 190–196

    CAS  Google Scholar 

  36. Vardi, A, Schatz, D, Beeri, K, Motro, U, Sukenik, A, Levine, A, Kaplan, A (2002) Dinoflagellate–cyanobacterium communication may determine the composition of phytoplankton assemblage in a mesotrophic lake. Curr Biol 12: 1767–1772

    Article  PubMed  CAS  Google Scholar 

  37. Vollenweider, RA (1969) Primary Production in Aquatic Environments. Internal Biology Program Handbook 12. Blackwell Scientific Publications, Oxford, p 213

    Google Scholar 

  38. Walsby, AE (1994) Gas vesicles. Microbiol Rev 58: 94–144

    PubMed  CAS  Google Scholar 

  39. Watanabe, MF, Watanabe, M, Kato, T, Harada, KI, Suzuki, M (1991) Composition of cyclic peptide toxins among strains of Microcystis aeruginosa (blue-green algae, cyanobacteria). Bot Mag Tokyo 104: 49–57

    Article  CAS  Google Scholar 

  40. Wetzel, RG, Likens, GE (1995) Composition and biomass of phytoplankton. In: Limnological Analyses, 2nd edn. Springer-Verlag, New York, pp 139–165

Download references

Acknowledgment

The authors are thankful to Professor Roger Pain for reading the revised manuscript, to Dr. Andrej Blejec for helping us with statistical analyses, and to Karmen Staniè for technical support. The work was supported by grant P-508 (“Ecotoxinology and Ecotoxicology”) from the Ministry of Education, Science and Sport of Slovenia.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Bojan Sedmak.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sedmak, B., Eleršek, T. Microcystins Induce Morphological and Physiological Changes in Selected Representative Phytoplanktons. Microb Ecol 51, 508–515 (2006). https://doi.org/10.1007/s00248-006-9045-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-006-9045-9

Keywords

Navigation