Hostname: page-component-669899f699-2mbcq Total loading time: 0 Render date: 2025-04-27T05:40:12.292Z Has data issue: false hasContentIssue false
  • English
  • Français

Temporal variation in microcystin production by Planktothrix agardhii (Gomont) Anagnostidis and Komárek (Cyanobacteria, Oscillatoriales) in a temperate lake

Published online by Cambridge University Press:  21 December 2011

Mikołaj Kokociński ,
Karolina Stefaniak ,
Katarzyna Izydorczyk ,
Tomasz Jurczak ,
Joanna Mankiewicz-Boczek  and
Janne Soininen
Mikołaj Kokociński*
Affiliation:
Collegium Polonicum, Adam Mickiewicz University, ul. Kościuszki 1, 69-100 Słubice, Poland Department of Hydrobiology, Adam Mickiewicz University, Umultowska 89, 61-614 Poznań, Poland
Karolina Stefaniak
Affiliation:
Faculty of Biology, Adam Mickiewicz University, Umultowska 89, 61-614 Poznań, Poland
Katarzyna Izydorczyk
Affiliation:
International Institute of the Polish Academy of Sciences, European Regional Centre of Ecohydrology u/a UNESCO, Tylna 3, 90-364 Łódź, Poland
Tomasz Jurczak
Affiliation:
Department of Applied Ecology, University of Łódź, 12/16 Banacha Str. - 90-237 Łódź, Poland
Joanna Mankiewicz-Boczek
Affiliation:
International Institute of the Polish Academy of Sciences, European Regional Centre of Ecohydrology u/a UNESCO, Tylna 3, 90-364 Łódź, Poland
Janne Soininen
Affiliation:
Department of Environmental Sciences, University of Helsinki, Niemenkah 73, 15140 Lahti, Finland
*
*Corresponding author: [email protected]
Get access

Abstract

Eutrophication of freshwater lakes has led to blooms formed by cyanobacteria often associated with toxins harmful to livestock and humans. Environmental conditions that favor toxin production during cyanobacterial blooms are, however, not well understood. Moreover, the ability to use cyanobacteria quantity to assess the level of threat associated with toxin production is a topic of discussion. The purpose for this study was to examine Planktothrix agardhii dynamics in a shallow, temperate hypertrophic lake and to determine the factors that affect microcystin production. In addition, the relationship between P. agardhii morphology and microcystin production was examined. The study spanned 2 years, and we documented a perennial P. agardhii bloom that contributed up to 99% of the total biomass. Intracellular microcystins were primarily detected throughout the study, with the highest concentration in October. Microcystin concentrations ranged from 3.4 to 71.2 μg.L−1, and they had a strong, positive correlation with P. agardhii biomass. In contrast, the levels of weight-specific microcystin were relatively stable throughout the entire study, ranging from 0.23 to 1.18 μg.mg−1. We also found that environmental factors, such as water temperature, phosphate level, ammonium nitrogen and transparency, were the most related to microcystin production. Furthermore, a significant relationship between filament morphology and toxin concentration suggested that there were different morphotypes within the toxic and non-toxic populations of P. agardhii. Our study showed that P. agardhii biomass and filament morphology may be useful characteristics for the identification of threats associated with cyanotoxins.

Keywords

Cyanobacteriafilament morphologyhepatotoxinsPlanktothrix agardhiishallow lakes
Type
Research Article
Information
Annales de Limnologie - International Journal of Limnology , Volume 47 , Issue 4 , 2011 , pp. 363 - 371
Copyright
© EDP Sciences, 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

References

Akcaalan, R., Young, F.M., Metcalf, J.S., Morrison, L.F., Albay, M. and Codd, G.A., 2006. Microcystin analysis in single filamentous of Planktothrix spp. in laboratory cultures and environmental blooms. Water Res. , 40, 1583–1590.CrossRefGoogle Scholar
Anderson, R.J., Luu, D.Z.X., Chen, C.F.B., Holmes, M.L., Kent, M., Le Blanc, F.J.R., Taylor, A. and Williams, D.E., 1993. Chemical and biological evidence links microcystins to salmon nepten liver disease. Toxicon , 31, 1315–1323.CrossRefGoogle Scholar
Briand, E., Gugger, M., Francois, J.C., Bernard, C., Humbert, J.F. and Quiblier, C., 2008a. Temporal variations in the dynamics of potentially microcystin-producing strains in a bloom-forming Planktothrix agardhii (Cyanobacterium) population. Appl. Environ. Microb. , 74, 3839–3848.CrossRefGoogle Scholar
Briand, E., Yéprémian, C., Humbert, J.F. and Quiblier, C., 2008b. Competition between microcystin- and non-microcystin-producing Planktothrix agardhii (cyanobacteria) strains under different environmental conditions. Environ. Microbiol. , 10, 3337–3348.CrossRefGoogle Scholar
Briand, J.F., Robillot, C., Quiblier-Lloberas, C. and Bernard, C., 2002. A perennial bloom of Planktothrix agardhii (cyanobacteria) in a shallow eutrophic French lake: limnological and microcystin production studies. Arch. Hydrobiol. , 153, 605–622.CrossRefGoogle Scholar
Burnham, K.M. and Anderson, D.R., 1998. Model selection and inference: a practical information-theoretic approach, Springer, 353 p.CrossRefGoogle Scholar
Carmichael, W.W. and Falconer, I.R., 1993. Diseases related to freshwater blue-green algal toxins, control measures. In: Falconer, I.R. (ed.), Algal toxins in seafood and drinking water, Academic Press, London, 187–209.CrossRefGoogle Scholar
Catherine, A., Quiblier, C., Yéprémian, C., Got, P., Groleau, A., Vincon-Leite, C., Bernard, C. and Troussellier, M., 2008. Collapse of a Planktothrix agardhii perennial bloom and microcystin dynamics in response to reduced phosphate concentrations in a temperate lake. FEMS Microbiol. Ecol. , 65, 61–73.CrossRefGoogle Scholar
Chorus, I., 2001. Cyanotoxins, occurrence, causes, consequences, Springer-Verlag KG, Berlin, 357 p.Google Scholar
Ernst, B., Hitzfeld, B. and Dietrich, D., 2001. Presence of Planktothrix sp. and cyanobacterial toxins in Lake Ammersee, Germany and their impact on whitefish (Coregonus lavaretus L.). Environ. Toxicol. , 16, 483–488.CrossRefGoogle Scholar
Falconer, I.R., 2005. Chemistry of microcystin: Cyanobacterial toxins of drinking water supplies: cylindrospermosins and microcystins, CRC Press, Taylor and Francis Group, 31–34.Google Scholar
Fastner, J., Neumann, U., Wirsing, B., Weckesser, J., Wiedner, C., Nixdorf, B. and Chorus, I., 1999. Microcystins (hepatotoxic heptapeptides) in German fresh water bodies. Environ. Toxicol. , 14, 13–22.3.0.CO;2-D>CrossRefGoogle Scholar
Ghadouani, A., Pinel-Alloul, B. and Prepas, E.E., 2003. Effects of experimentally induced cyanobacterial blooms on crustacean zooplankton communities. Freshw. Biol. , 48, 363–381.CrossRefGoogle Scholar
Gilbert, J.J., 1990. Differential effects of Anabaena affinis on cladocerans and rotifers: mechanisms and implications. Ecology , 71, 1727–1740.CrossRefGoogle Scholar
HACH, 1997. Water analysis handbook, HACH Company, 1309 p.Google Scholar
Halstvedt, C.B., Rohrlack, T., Andersen, T., Skulberg, O. and Edvardsen, B., 2007. Seasonal dynamics and depth distribution of Planktothrix spp. in Lake Steinsfjorden (Norway) related to environmental factors. J. Plankton Res. , 29, 471–482.CrossRefGoogle Scholar
Halstvedt, C.B., Rohrlack, T., Ptacnik, R. and Bente, E., 2008. On the effect of abiotic environmental factors on production of bioactive oligopeptides in field populations of Planktothrix spp. (Cyanobacteria). J. Plankton Res. , 30, 607–617.CrossRefGoogle Scholar
Hašler, P. and Pouličkova, A., 2003. Diurnal changes in vertical distribution and morphology of natural population of Planktothrix agardhii (Gom.) Anagn. et Kom. (Cyanobacteria). Hydrobiol. , 506–509, 195–201.CrossRefGoogle Scholar
Hindak, F., 1978. Freshwater algae. Slovenské Pedagogické Nakladatelstwo, Bratislava, 724 p. (in Slovak).Google Scholar
Humbert, J.F. and Le Berre, B., 2001. Genetic diversity in two species of freshwater cyanobacteria, Planktothrix (Oscillatoria) rubescens and P. agardhii . Arch. Hydrobiol. , 150, 197–206.CrossRefGoogle Scholar
Janse, I., Kardinaal, W.E.A., Kamst-van Agterveld, M., Meima, M., Visser, P.M. and Zwart, G., 2005. Contrasting microcystin production and cyanobacterial population dynamics in two Planktothrix-dominated freshwater lakes. Environ. Microbiol. , 7, 1514–1524.CrossRefGoogle ScholarPubMed
Javornickỳ, P. (ed.), 1958. Revise některỳch method pro zjišt'ovănĭkvantity fitoplantonu (Revision of some methods for the phytoplankton quantity estimation), Scientific Paper 2, Faculty of Technology of Fuel and Water, Institute of Chemical Technology, Prague, 283–267.Google Scholar
Jurczak, T., Tarczyńska, M., Izydorczyk, K., Mankiewicz, J., Zalewski, M. and Meriluoto, J., 2005. Elimination of microcystins by water treatment processes-examples from Sulejów reservoir, Poland. Water Res. , 39, 2394–2406.CrossRefGoogle ScholarPubMed
Kardinaal, W.E.A. and Visser, P.M., 2005. Dynamics of cyanobacterial toxins: sources of variability in microcystin concentrations. In: Huisman, J., Matthijs, H.C.P. and Visser, P.M. (eds), Harmful cyanobacteria, Springer-Verlag, Berlin, Germany, 41–63.Google Scholar
Kardinaal, W.E.A., Tonk, L., Janse, I., Hol, S., Slot, P., Huisman, J. and Visser, P.M., 2007. Competition for light between toxic and nontoxic strains of the harmful cyanobacterium Microcystis . Appl. Environ. Microbiol. , 73, 2939–2946.CrossRefGoogle ScholarPubMed
Keil, C., Forchert, A., Fastner, J., Szewczyk, U., Rotard, W., Chorus, I. and Krätke, R., 2002. Toxicity and microcystin content of extracts from a Planktothrix bloom and two laboratory strains. Water Res. , 36, 2133–2139.CrossRefGoogle ScholarPubMed
Korhonen, J.J., Soininen, J. and Hillebrand, H., 2010. A quantitative analysis of temporal turnover in aquatic species assemblages across ecosystems. Ecology , 91, 508–517.CrossRefGoogle ScholarPubMed
Kurmayer, R., Christiansen, G. and 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. Microb. , 69, 787–795.CrossRefGoogle ScholarPubMed
Kurmayer, R., Christiansen, G., Fastner, J. and Börner, T., 2004. Abundance of active and inactive microcystin ecotypes in populations of the toxic cyanobacterium Planktothrix spp . Environ. Microbiol. , 6, 831–841.CrossRefGoogle Scholar
Laamanen, M.J., Gugger, M.F., Lehtimäki, M.J., Haukka, K. and Sivonen, K., 2001. Diversity of toxic and nontoxic Nodularia isolates (Cyanobacteria) and filaments from Baltic Sea. Appl. Environ. Microb. , 67, 4638–4647.CrossRefGoogle ScholarPubMed
Lehtiniemi, M., Engstrom-Ost, J., Karjalainen, M., Kozlowsky-Suzuki, B. and Viitasalo, M., 2002. Fate of cyanobacterial toxins in the pelagic food web: transfer to copepods or to fecal pellets? Mar. Ecol. Prog. Ser. , 241, 13–21.CrossRefGoogle Scholar
Liras, V., Lindberg, N., Nystom, P., Annadotter, H., Lawton, L.A. and Graf, B., 1998. Can ingested cyanobacteria be harmful to the signal crayfish (Pacifastacus leniusculus)? Freshw. Biol. , 39, 233–242.CrossRefGoogle Scholar
Mankiewicz-Boczek, J., Gągała, I., Kokociński, M., Jurczak, T. and Stefaniak, K., 2011. Perennial toxigenic Planktothrix agardhii bloom in selected lakes of Western Poland. Environ. Toxicol. , 26 (1), 10–20.CrossRefGoogle ScholarPubMed
Mbedi, S., Welker, M., Fastner, J. and Wiedner, C., 2005. Variability of the microcystin synthetase gene cluster in the genus Planktothrix (Oscillatoriales, Cyanobacteria). FEMS Microbiol. Lett. , 245, 299–306.CrossRefGoogle Scholar
Mikalsen, B., Boison, G., Skulberg, O.M., Fastner, J., Davies, W. and Gabrielsen, T.M., 2003. Natural variation in the microcystin synthetase operon mcyABC and impact on microcystin production in Microcystis strains. J. Bacteriol. , 185, 2774–2785.CrossRefGoogle ScholarPubMed
Neilan, B.A., Pearson, L.A., Moffitt, M.C., Mihali, K.T., Kaebernick, M., Kellmann, R. and Pomati, F., 2008. The genetics and genomics of cyanobacetrial toxicity. In: Hudnell, H.K. (ed.), Cyanobacterial Harmful algal blooms. State of science and researches needs. Advances in experimental medicine and biology. Springer, New York, 619, 417–452.Google Scholar
Nixdorf, B., 1994. Polymixis of a shallow lake (Großer Müggelsee, Berlin) and its influence on seasonal phytoplankton dynamics. Hydrobiol. , 275/276, 173–186.CrossRefGoogle Scholar
Nixdorf, B., Mischke, U. and Rücker, J., 2003. Phytoplankton assemblages and steady state in deep and shallow eutrophic lakes – an approach to differentiate the habitat properties of Oscillatoriales. Hydrobiol. , 502, 111–121.CrossRefGoogle Scholar
Pawlik-Skowrońska, B., Pirszel, J. and Kornijów, R., 2008. Spatial and temporal variation in microcystin concentrations during perennial bloom of Planktothrix agardhii in a hypertrophic lake. Ann. Limnol. – Int. J. Lim. , 44, 63–68.CrossRefGoogle Scholar
Pouličkova, A., Hašler, P. and Kitner, M., 2004. Annual Cycle of Planktothrix agardhii (Gom.) Anagn. & Kom. nature population. Int. Rev. Hydrobiol. , 89, 278–288.CrossRefGoogle Scholar
R Development Core Team, 2005. R: a language and environment for statistical computing, R Foundation for Statistical Computing, Vienna, Austria, http://www.R-project.org Google Scholar
Romo, S., 1994. Seasonal variation in size of cyanophytes Planktothrix agardhii, Pseudoanabaena galeata and Geitlerinema sp. Verh. Int. Verein. Limnol. , 25, 2221–2225.Google Scholar
Rücker, J., Wiedner, C. and Zippel, P., 1997. Factors controlling the dominance of Planktothrix agardhii and Limnothrix redekei in eutrophic shallow lakes. Hydrobiol. , 342/343, 107–115.CrossRefGoogle Scholar
Scheffer, M., 1998. Ecology of shallow lakes, Chapman & Hall, London, UK, 1–357.Google Scholar
Scheffer, M., Rinaldi, S., Gragnami, A., Mur, L.R. and van Nes, E.H., 1997. On the dominance of filamentous cyanobacteria in shallow, turbid lakes. Ecology , 78, 272–282.CrossRefGoogle Scholar
Sivonen, K., 1990. Effect of light, temperature, nitrate, orthophosphate and bacteria on growth of hepatotoxin production by Oscillatoria agardhii strains. Appl. Environ. Microbiol. , 56, 2658–2666.CrossRefGoogle ScholarPubMed
Sivonen, K. and Jones, G.J., 1999. Cyanobacterial toxins. In: Chorus, I. and Bartman, J. (eds.), Toxic cyanobacteria in water, E and FN Spon, London, 41–111.Google Scholar
Soininen, J., McDonald, R. and Hillebrand, H., 2007. The distance decay of similarity in ecological communities. Ecography , 30, 3–12.CrossRefGoogle Scholar
SPSS, 1999. SYSTAT 9 Graphics, SPSS, Chicago.Google Scholar
Stefaniak, K., Kokociński, M. and Messyasz, B., 2005. Dynamics of Planktothrix agardhii (Gom.) Anagn. et Kom. blooms inpolimictic Lake Laskownickie and Grylewskie (Wielkopolska region) Poland. Ocean. Hydrobiol. Stud. Suppl. , 3, 125–136.Google Scholar
Suikkanen, S., Fistarol, G.O.I. and Graneli, E., 2004. Allelopathic effects of the Baltic cyanobacteria Nodularia spumigena, Aphanizomenon flos-aquae and Anabaena lammermannii on algal monocultures. J. Exp. Mar. Biol. and Ecol. , 308, 85–101.CrossRefGoogle Scholar
Tonk, L., Visser, P.M., Christiansen, G., Dittmann, E., Snelder, E.O.F.M., Wiedner, C., Mur, L.R. and Huisman, J., 2005. The microcystin composition of the cyanobacterium Planktothrix agardhii changes toward a more toxic variant with increasing light intensity. Appl. Environ. Microbiol. , 71, 5177–5181.CrossRefGoogle Scholar
Van Liere, L. and Mur, L.R., 1980. Occurrence of Oscillatoria agardhii and some related species, a survey. Dev. Hydrobiol. , 2, 67–77.Google Scholar
Wetzel, R.G. and Likens, G.E., 2000. Limnological analyses (Third edn,), Springer-Verlag, New York, 1–429.CrossRefGoogle Scholar
Wiedner, C., Nixdorf, B., Heinze, R., Wirsing, B., Neumann, U. and Weckesser, J., 2002. Regulation of cyanobacteria and microcystin dynamics in polymictic shallow lakes. Arch. Hydrobiol. , 155, 383–400.CrossRefGoogle Scholar
Yéprémian, C., Gugger, M., Briand, E., Catherine, A., Berger, C., Quiblier, C. and Bernard, C., 2007. Microcystin ecotypes in a perennial Planktothrix agardhii bloom. Water Res. , 41, 4446–4456.CrossRefGoogle Scholar