Abstract
Eutrophication and enhanced external nutrient loading of lakes and seas are most clearly reflected by increased cyanobacterial blooms, which are often toxic. Freshwater cyanobacteria produce a number of bioactive secondary metabolites, some of which have allelopathic properties, significantly influencing the biological processes of other algae, thereby affecting species composition and succession of the phytoplankton. The goal of this work was to investigate the influence of bloom-forming cyanobacterial exudates on the photophysiology of the green alga Scenedesmus quadricauda by chlorophyll fluorescence analysis. We were able to prove the effect of algal cell-free fltrates on the performance of S. quadricauda and demonstrate for the first time that the freshwater picocyanobacterium Cyanobium gracile has strong negative impact on the coexisting green alga. Neither the cyanotoxin (MYC, CYN and ATX) producing, nor the non-toxic strains showed any systematic effect on the production of S. quadricauda. Various strains of the cyanobacterium Cylindrospermopsis raciborskii inhibited the performance of the green alga independently of their origin. Our results urge further studies for a better understanding of the factors affecting the release of allelopathic compounds and the mechanisms of their effects on target organisms.
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References
Bláha, L., Maršálek, B. (1999) Microcystin production and toxicity of picocyanobacteria as a risk factor for drinking water treatment plants. Algol. Stud. 92, 95–108.
Bilger, W., Schreiber, U. (1986) Energy dependent quenching of dark-level chlorophyll fuorescence in intact leaves. Photosynth Res. 10(3), 303–308.
Ciscar, J. C., Feyen, L., Soria, A. (2014) Climate impacts in Europe. The JRC PESETA II project. JRC scientifc and politicy reports, EUR 26586EN.
Dyble, J., Tester, P. A., Litaker, R. W. (2006) Effects of light intensity on cylindrospermopsin production in the cyanobacterial HAB species Cylindrospermopsis raciborskii. Afr. J. Mar. Sci. 28, 309–312.
Eilers, P. H. C., Peeters, J. C. H. (1988) A model for the relationship between light intensity and the rate of photosynthesis in phytoplankton. Ecol. Model 42, 199–215.
Falkowski, P. G. (1992) Molecular ecology of phytoplankton photosynthesis. In: Falkowski, P. G., Woodhead, A. D. (eds) Primary Productivity and Biogeochemical Cycles in the Sea. Plenum Press, New York, pp. 47–67.
Figueredo, C. C., Giani, A., Bird, D. F. (2007) Does allelopathy contribute to Cylindro-spermopsis raciborskii (Cyanobacteria) bloom occurrence and geographic expansion? J. Phycol. 43, 256–265.
Gross, E. M. (2003) Allelopathy of aquatic autotrophs. Crit. Rev. Plant Sci. 22, 313–339.
Iwamura, T., Nagai, H., Ichimura, S. (1970) Improved methods for determining contents of chlorophyll, protein, ribonucleic acid, deoxyribonucleic acid in planktonic populations. Int. Rev. ges. Hydrobiol. 55, 131–147.
Jakubowska, N., Szeląg-Wasielewska, E. (2015) Toxic picoplanktonic cyanobacteria-Review. Mar. Drugs 13, 1497–1518.
Jasser, I., Lehtovaara, A., Arvola, L. (2006) Seasonality and coexistence of autotrophic pico- and nanoplankton and zooplankton in three boreal lakes. Verhandlungen des Internationalen Verein Limnologie 29, 1413–1416.
Jöhnk, K. D., Huisman, J., Sharples, J., Sommeijer, B., Visser, P. M., Stroom, J. M. (2008) Summer heatwaves promote blooms of harmful cyanobacteria. Glob. Change Biol. 14, 495–512.
Kearns, K. D., Hunter, M. D. (2001) Toxin-producing Anabaena fos-aquae induces settling of Chlamydomonas reinhardtii, a competing motile alga. Microb. Ecol. 42, 80–86.
Keating, K. I. (1977) Allelopathic infuence on blue-green bloom sequence in a eutrophic lake. Science 196, 885–887.
Keating, K. I. (1978) Blue-green algal inhibition of diatom growth: transition from mesotrophic to eutrophic community structure. Science 199, 971–973.
Leăo, P. N., Vasconcelos, M. T. S. D., Vasconcelos, V. M. (2009) Allelopathy in freshwater cyanobacteria. Crit. Rev. Microbiol. 35, 271–282.
Leăo, P. N., Vasconcelos, T. M. S. D., Vasconcelos, V. M. (2009) Allelopathic activity of cyanobacteria on green microalgae at low cell densities. Eur. J. Phycol. 44, 347–355.
Legrand, C., Rengefors, K., Fistarol, G. O., Granéli, E. (2003) Allelopathy in phytoplankton - biochemical, ecological, and evolutionary aspects. Phycologia 42, 406–419.
Li, W. K. W., Suba Rao, D. V., Harrison, W. G., Smith, J. C., Cullen, B., Irwin, B., Platt, T. (1983) Autotrophic picoplankton in the tropical ocean. Science 219, 292–295.
Maxwell, K., Johnson, G. N. (2000) Chlorophyll fuorescence-a practical guide. J. Exp. Botany 51, 659–668.
Mazmouz, R., Chapuis-Hugon, F., Mann, S., Pichon, V., Mejean, A., Ploux, O. (2010) Biosynthesis of cylindrospermopsin and 7-epicylindrospermopsin in Oscillatoria sp. strain PCC 6506: Identifcation of the cyr gene cluster and toxin analysis. App. Environ. Microb. 76, 4943–4949.
Meriluoto, J., Spoof, L., Codd, G. A. (2017) Handbook of Cyanobacterial Monitoring and Cyanotoxin Analysis. John Wiley & Sons Ltd., United Kingdom.
Oberholster, P. J., Myburgh, J. G., Govender, D., Bengis, R., Botha, A.-M. (2009) Identifcation of toxigenic Microcystis strains after incidents of wild animal mortalities in the Kruger National Park, South Africa. Ecotox. Environ. Safety 72, 1177–1182.
O’Neil, J. M., Davis, T. W., Burford, M. A., Gobler, C. J. (2012) The rise of harmful cyanobacteria blooms: The potential roles of eutrophication and climate change. Harmful Algae 14, 313–334.
Padisák, J., Reynolds, C. S. (1998) Selection of phytoplankton associations in Lake Balaton, Hungary, in response to eutrophication and restoration measures, with special reference to the cyanoprokaryotes. Hydrobiologia 384, 41–53.
Paerl, H. W., Paul, V. J. (2012) Climate change: links to global expansion of harmful cyanobacteria. Water Res. 46, 1349–1363.
Pick, F. R. (2016) Blooming algae: A Canadian perspective on the rise of toxic cyanobacteria. Can. J. Fish. Aquat. Sci. 73, 1149–1158.
Rasconi, S., Gall, A., Winter, K., Kainz, M. J. (2015) Increasing water temperature triggers dominance of small freshwater plankton. PLOS ONE DOI:10.1371/journal.pone.0140449.
Reynolds, C. S. (2006) The Ecology of Phytoplankton. Cambridge University Press, New York.
Rippka, R., Deruelles, J., Waterbury, J. B., Herdman, M., Stainer, R. Y. (1979) The cyanobacteria. J. Gen. Microbiol. 111, 1–61.
Saker, M. L., Neilan, B. A. (2001) Varied diazotrophies, morphologies, and toxicities of genetically similar isolates of Cylindrospermopsis raciborskii (Nostocales, Cyanophyceae) from Northern Australia. App. Environ. Microb. 67, 1839–1845.
Schreiber, U. (1998) Chlorophyll fuorescence: new instruments for special applications. In: Garab, Gy. (ed.) Proceedings of the XIth International Congress on Photosynthesis, Vol. V. Kluwer, Dordrecht, pp. 4253–4258.
Schreiber, U., Hormann, H., Neubauer, C., Klughammer, C. (1995) Assessment of photosystem II photochemical quantum yield by chlorophyll fuorescence quenching analysis. Aust. J. Plant Physiol. 22, 209–220.
Sedmak, B., Eleršek, T. (2005) Microcystins induce morphological and physiological changes in selected representative phytoplankton. Microb. Ecol. 50, 298–305.
Śliwińska-Wilczewska, S., Pniewski, F., Latała, A. (2016) Allelopathic activity of the picocyano-bacterium Synechococcus sp. under varied light, temperature, and salinity conditions. Int. Rev. Hydrobiol. 101), 69–77.
Śliwińska-Wilczewska, S., Pniewski, F., Latała, A. (2016) Allelopathic interactions between Synechococcus sp. and Nodularia spumigena under different light conditions. Allelopathy J. 37, 241–252.
Śliwińska-Wilczewska, S., Maculewicz, J., Barreiro, A. F., Vasconcebos, V., Latała, A. (2017) Allelopathic activity of picocyanobacterium Synechococcus sp. on flamentous cyanobacteria. J. Exp. Mar. Biol. Ecol. 496, 16–21.
Smith, G. D., Doan, N. T. (1999) Cyanobacterial metabolites with bioactivity against photosynthesis in cyanobacteria, algae and higher plants. J. Appl. Phycol. 11, 337–344.
Sommer, U., Gliwicz, Z. M., Lampert, W., Duncan, A. (1986) The PEG-Model of seasonal succession of planktonic events in fresh waters. Arch. Hydrobiol. 106, 433–471.
Stal, L. J., Albertano, P., Bergman, B., Bröckel, K., Gallon, J. R., Hayes, P. K., Sivonen, K., Walsby, A. E. (2003) BASIC: Baltic Sea cyanobacteria. An investigation of the structure and dynamics of water blooms of cyanobacteria in the Baltic Sea - responses to a changing environment. Continental Shelf Research 23, 1695–1714.
Suikkanen, S., Fistarol, G. O., Graneli, E. (2005) Effects of cyanobacterial allelochemicals on a natural plankton community. Mar. Ecol. Prog. Ser. 287, 1–9.
Sukenik, A., Eshkol, R., Livne, A., Hadas, O., Rom, M., Tchernov, D., Vardi, A., Kaplan, A. (2002) Inhibition of growth and photosynthesis of the dinofagellate Peridinium gatunense by Microcystis sp. (cyanobacteria): A novel allelopathic mechanism. Limnol. Oceanogr. 47, 1656–1663.
Swain, S. S., Paidesetty, S. K., Padhya, R. N. (2017) Antibacterial, antifungal and antimycobacterial compounds from cyanobacteria. Biomedicine & Pharmacotherapy 90, 760–776.
Tilman, D. (1977) Resource competition between planktonic algae: An experimental and theoretical approach. Ecology 58, 338–348.
Vörös, L., Nagy Göde, P. (1993) Long term changes of phytoplankton in Lake Balaton (Hungary). Verh. Int. Verein. Limnol. 25, 682–686.
Acknowledgements
The research was supported by the Bolyai Research Fund. We are grateful to Martin L. Saker (Interdisciplinary Centre of Marine and Environmental Research, CIIMAR, University of Porto, Portugal) for the C. raciborskii strain of AQS.
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Kovács, A.W., Tóth, V.R. & Pálffy, K. The Effects of Interspecific Interactions Between Bloom Forming Cyanobacteria and Scenedesmus quadricauda (Chlorophyta) on Their Photophysiology. BIOLOGIA FUTURA 69, 210–223 (2018). https://doi.org/10.1556/018.69.2018.2.9
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DOI: https://doi.org/10.1556/018.69.2018.2.9