Abstract
A better understanding of the effect of anthropogenic pollution on the formation of toxic Microcystis blooms is particularly important in regions with large urban centres where rivers, lakes, and estuaries receive large quantities of contaminated domestic and industrial wastes. The response of the bloom-forming cyanobacteria Microcystis aeruginosa CALU 972 and CALU 973 from Russian Karelia to pollution was investigated. The contaminants caused compensatory-adaptive changes that led to the retention of cell viability in the cyanobacterial cells. The adaptation to metals and 1,2,4-triazole was realised due to photosystem changes and the enhanced production of organic compounds, such as proteins and exopolysaccharides. Nutrients caused a significant increase in biomass production by M. aeruginosa. The exposure of M. aeruginosa to nutrients and zinc stimulated growth and contributed to enhanced microcystin concentrations. Variants of microcystins responded differently to pollution. Contaminants had pronounced effects on microcystin RR levels but less effects on microcystin LR levels. Heavy metals, 1,2,4-triazole and nitrogen influenced microcystin concentrations by affecting both the growth of Microcystis and hepatotoxin release into the environment.
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Berg, K., Skulberg, O. M., & Skulberg, R. (1987). Effects of decaying toxic blue-green algae on water quality — a laboratory study. Archiv für Hydrobiologie, 108, 549–563.
Bhaya, D., Schwarz, R. & Grossman, A. R. (2000). Molecular responses to environmental stress. In B. A Whitton & M. Potts (Eds.), The Ecology of Cyanobacteria (pp. 397–442). Dordrecht: Kluwer Academic.
Black, I. T. (1974). Principles and techniques of scanning electron microscopy. Biological application. New York: Van Nostrand Reinhold Co.
Böttcher, G., Chorus, I., Ewald, S., Hintze, T., & Walz, N. (2001). Light limited growth and microcystin content of Planktothrix agardhii and Microcystis in turbidostats. In I. Chorus (Ed.), Cyanotoxins: occurrence, causes, consequences (pp. 115–133). Berlin: Springer-Verlag KG.
Brookes, J. D., & Ganf, G. G. (2001). Variations in the buoyancy response of Microcystis aeruginosa to nitrogen, phosphorus and light. Journal of Plankton Research, 23(12), 1399–1411.
Bryant, D. A. (1996). The molecular biology of cyanobacteria (pp. 559–579). Amsterdam: KluwerAcademic publishers.
Chisholm, S. W., & Morel, F. M. M. (1991). What controls phytoplankton production in nutrient-rich areas of the open sea? Limnology & Oceanography, (Special Issue), 36(8), 1507–1511.
Collected sanitary and hygienic standards and methods for control of hazardous substances in the environment. (1991). Moscow: Medicine (in Russian).
De Philippis, R., Sili, C., Tassinato, G., Vincenzini, M., & Materassi, R. (1991). Effects of growth conditions on exopolysaccharide production by Cyanospira capsulata. Bioresource Technology, 38, 101–104.
Dietz, K. J., Heber, U., & Mimura, T. (1998). Modulation of the vacuolar H+-ATPase by adenylates as basis for the transient CO2-dependent acidification of the leaf vacuole upon illumination. Biochimica et Biophysica Acta, 1373, 87–92.
Eullaffroy, P., & Vernet, G. (2003). The F 684/F 735 chlorophyll fluorescence ratio: a potential tool for rapid detection and determination of herbicide phytotoxicity in algae. Water Research, 37(9), 1983–1990.
Falconer, I., Bartram, J., Chorus, I., Kuiper-Goodman, T., Utkilen, H., Burch, M., et al. (1999). Safe levels and safe practices. In I. Chorus & J. Bartram (Eds.), Toxic cyanobacteria in water – a guide to their public health consequences, monitoring and management (pp. 155–178). London: E&FN Spon.
Falconer, I. R. (2005). Cyanobacterial toxins of drinking water supplies: Cylindrospermopsins and microcystin. Florida: CRC Press, Boca Raton.
Fenderson, B. A., Eddy, E. M., & Hakomori, S.-I. (1990). Glycoconjugate expression during embryogenesis and its biological significance. BioEssays, 12(4), 173–179.
Flaibani, A., Olsen, Y., & Painter, T. J. (1989). Polysaccharides in desert reclamation: compositions of exocellular proteoglycan complexes produced by filamentous blue-green and unicellular green edaphic algae. Carbohydrate Research, 190, 235–248.
Fujiki, H., Sueoka, E., & Suganuma, M. (1996). Carcinogenesis of microcystins. In M. F. Watanabe, K. Harada, W. W. Carmichael, H. Fujiki, et al. (Eds.), Toxic Microcystis (pp. 203–233). Florida: CRC Press, Boca Raton.
Giani, A., Bird, D. F., Prairie, Y. T., & Lawrence, J. F. (2005). Empirical study of cyanobacterial toxicity along a trophic gradient of lakes. Canadian Journal of Fisheries and Aquatic Sciences, 62, 2100–2109.
Gouvea, S. P., Boyer, G. L., & Twiss, M. R. (2008). Influence of ultraviolet radiation, copper, and zinc on microcystin content in Microcystis aeruginosa (Cyanobacteria). Harmful Algae, 7, 194–205.
Hayat, M. A. (1986). Basic techniques for transmission electron microscopy (pp. 232–264). London: Acad. Press.
Heipierer, H. J., Keweloh, H., & Rehm, H.-J. (1991). Influence of phenols on growth and membrane permeability of free and immobilized Escherichia coli. Applied and Environmental Microbiology, 57, 1213–1217.
Herbert, D., Phipps, P. J., & Strange, R. E. (1971). Chemical analysis of microbial cells. In J. R. Norris & D. W. Ribbons (Eds.), Methods in Microbiology (pp. 209–374).: Academic Press.
Hesse, K., & Kohl, J.-G. (2001). Effects of light and nutrient supply on growth and microcystin content of different strains of Microcystis aeruginosa. In I. Chorus (Ed.), Cyanotoxins: occurrence, causes, consequences (pp. 152–158). Berlin: Springer-Verlag.
Israel, Y. A. (2003). Review of environmental pollution in Russian Federation in 2002. Moscow: Roshydromet (in Russian).
Jähnichen, S., Petzoldt, T., & Benndorf, J. (2001). Evidence for control of microcystin dynamics in Bautzen Reservoir (Germany) by cyanobacterial population growth rates and dissolved inorganic carbon. Archiv für Hydrobiologie, 150, 177–196.
Jeffrey, S. W., & Humprhråy, G. E. (1975). New spectrophotometric equations for determining chlorophylls a, b, c1 and c2 in higher plants, algae and natural phytoplankton. Biochemie und Physiologie der Pflanzen, 167(2), 191–194.
Jiang, Y., Ji, B., Wong, R. N. S., & Wong, M. H. (2008). Statistical study on the effects of environmental factors on the growth and microcystins production of bloom-forming cyanobacterium — Microcystis aeruginosa. Harmful Algae, 7, 127–136.
Kim, I. S., Beaudette, L. A., Shim, J. H., Trevors, J. T., & Suh, Y. T. (2002). Environmental fate of the triazole fungicide propiconazole in a rice-paddy–soil lysimeter. Plant and Soil, 239, 321–331.
Kiss, T., & Osipenko, O. (1994). Metal ion-induced permeability changes in cell membranes: a minireview. Cellular and Molecular Neurobiology, 14(6), 781–789.
Kotak, B. G., Lam, A. K.-Y., Prepas, E. E., Kenefick, S. L., & Hrudey, S. E. (1995). Variability of the hepatotoxin microcystin-LR in hypereutrophic drinking water lakes. Journal of Phycology, 31, 248–263.
Lawton, L. A., Edwards, C., & Codd, G. A. (1994). Extraction and high-performance liquid chromatographic method for the determination of microcystins in raw and treated waters. Analyst, 119, 1525–1530.
Long, B. M., Jones, G. J., & Orr, P. T. (2001). Cellular microcystin content in N-limited Microcystis aeruginosa can be predicted from growth rate. Applied and Environmental Microbiology, 67, 278–283.
Lowry, O. H., Rosenrough, N. F., Farr, A. L., & Randall, K. J. (1951). Protein measurement with the folin phenol reagent. Journal of Biological Chemistry, 193(1), 265–275.
Lukac, M., & Aegerter, R. (1993). Influence of trace metals on growth and toxin production of Microcystis aeruginosa. Toxicon, 31, 293–305.
Moisander, P. H., Ochiai, M., & Lincoff, A. (2009). Nutrient limitation of Microcystis aeruginosa in northern California Klamath River reservoirs. Harmful Algae, 8, 889–897.
Oh, H.-M., Lee, S. J., Jang, M.-H., & Yoon, B.-D. (2000). Microcystin production by Microcystis aeruginosa in a phosphorous-limited chemostat. Applied and Environmental Microbiology, 66, 176–179.
Paerl, H. W., Tucker, J., & Bland, P. T. (1983). Carotenoid enhancement and its role in maintaining blue-green algal (Microcystis aeruginosa) surface blooms. Limnology and oceanography, 28(5), 847–857.
Parsons, T. R., & Strickland, J. D. H. (1963). Discussion of spectrophotometric determination of marine-plant pigments with revised equations for ascertaining chlorophylls and carotenoids. Journal of Marine Research, 21, 155–163.
Pearson, L. A., Hisbergues, M., Borner, T., Dittman, E., & Neilan, B. A. (2004). Inactivation of an ABC transporter gene, mcyH, results in loss of microcystin production in the cyanobacterium Microcystis aeruginosa PCC 7806. Applied and Environmental Microbiology, 70, 6370–6378.
Poliak, Y. M., Zaytseva, T. B., Petrova, V. N., & Medvedeva, N. G. (2011). Development of mass cyanobacteria species under heavy metals pollution. Hydrobiological Journal, 47(3), 75–90.
Rai, L. C., Raizada, M., Mallick, N., Husaini, Y., Singh, A. K., & Dubey, S. K. (1990). Effect of four heavy metals on the biology of Nostoc muscorum. Biology of Metals, 2, 229–234.
Rapala, J., Sivonen, K., Lyra, C., & Niemela, S. I. (1997). Variation of microcystin, cyanobacterial hepatotoxins, in Anabaena spp as a function of growth stimulation. Applied and Environmental Microbiology, 63, 2206–2212.
Senthilkumar, T., & Jeyachandran, S. (2006). Effect of salinity stress on the marine cyanobacterium Oscillatoria acuminata Gomont with reference to proline accumulation. Seaweed Research and Utilization, 28, 99–104.
Siegelman, H. W., & Kycia, J. H. (1978). Algal biliproteins. In J. A. Hellebust & J. S. Craigie (Eds.), Handbook of phycological methods, physiological and biochemical methods (pp. 72–78). Cambridge: Cambridge University Press.
Sivonen, K. (1990). Effects of light, temperature, nitrate, orthophosphate, and bacteria on growth of and hepatotoxin production by Oscillatoria agardhii strains. Applied and Environmental Microbiology, 56(9), 2658–2666.
Sivonen, K., & Jones, G. (1999). Cyanobacterial toxins. In I. Chorus & J. Bartram (Eds.), Toxic cyanobacteria in water—a guide to their public health consequences, monitoring and management (pp. 41–111). London: E&FN Spon.
Spurr, A. R. (1969). A low viscosity exopy resin embedding medium for electron microscopy. Ultrastructure Research, 26(1), 31–43.
Stanier, R. Y., Kunisawa, R., Mandel, M., & Cohen-Bazire, G. (1971). Purification and properties of unicellular blue-green algae (Order Chroococcales). Bacteriological Reviews, 35, 171–205.
Status of the North West and North Russia environment. (1995). St. Petersburg: Nauka (in Russian).
Sunda, W. G. (1989). Trace metal interactions with marine phytoplankton. Journal of Biological Oceanography, 6, 411–442.
Turpin, D. H. (1991). Effects of inorganic N availability on algal photosynthesis and carbon metabolism. Phycology, 27(1), 14–20.
Utkilen, H., & Gjølme, N. (1995). Iron-stimulated toxin production in Microcystis aeruginosa. Applied and Environmental Microbiology, 61, 797–800.
Vachali, P., Bhosale, P., & Bernstein, P. S. (2012). Microbial carotenoids. In J.-L. Barredo (Ed.), Microbial carotenoids from fungi: methods and protocols (pp. 41–59). New York: Humana Press.
Van der Westhuizen, A. J., & Eloff, J. N. (1985). Effect of temperature and light on the toxicity and growth of the blue-green alga Microcystis aeruginosa (UV-006). Planta, 163, 55–59.
Vezie, C., Rapala, J., Vaitomaa, J., Seitsonen, J., & Sivonen, K. (2002). Effect of nitrogen and phosphorus on growth of toxic and nontoxic Microcystis strains and on intracellular microcystin concentrations. Microbial Ecology, 43, 443–454.
Watanabe, M. F., & Oishi, S. (1985). Effects of environmental factors on toxicity of a cyanobacterium Microcystis aeruginosa under culture conditions. Applied and Environmental Microbiology, 49, 1342.
WHO (2004). Guidelines for drinking water quality. Third edition, Volume 1, Recommendations. World Health Organization, Geneva: Sun Fung.
Wiedner, C., Visser, P. M., Fastner, J., Metcalf, J. S., Codd, G. A., & Mur, L. R. (2003). Effects of light on the microcystin content of Microcystis strain PCC 7806. Applied and Environmental Microbiology, 69, 1475–1481.
Zaccaro, M. C., Salazar, C., Zulpa de Caire, G., Storni de Cano, M., & Stella, A. M. (2000). Lead toxicity in cyanobacterial porphyrin metabolism. Environmental Toxicology, 16, 61–67.
Zhan, L., Sakamoto, H., Sakuraba, M., Wu, D.-S., Zhang, L.-S., Suzuki, T., et al. (2004). Genotoxicity of microcystin-LR in human lymphoblastoid TK6 cells. Mutation Research, 557, 1–6.
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The authors thank Oksana Ribalchenko for the electron microscopic examinations and Evgenii Protasov for the high-performance liquid chromatography analyses.
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Polyak, Y., Zaytseva, T. & Medvedeva, N. Response of Toxic Cyanobacterium Microcystis aeruginosa to Environmental Pollution. Water Air Soil Pollut 224, 1494 (2013). https://doi.org/10.1007/s11270-013-1494-4
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DOI: https://doi.org/10.1007/s11270-013-1494-4