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Initial growth phases of two bloom-forming cyanobacteria (Cylindrospermopsis raciborskii and Planktothrix agardhii) in monocultures and mixed cultures depending on light and nutrient conditions

Published online by Cambridge University Press:  17 July 2014

Myriam Ammar ,
Katia Comte ,
Thi Du Chi Tran  and
Monia El Bour
Myriam Ammar
Affiliation:
Laboratoire de Pathologies des Animaux Aquatiques, Institut National des Sciences et Technologies de la Mer, 2025 Salammbô, Tunisia UMR 7245 CNRS-MNHN Molécules de communication et adaptation des micro-organismes, Muséum national d'Histoire naturelle, Case 39, 12, rue Buffon, F-75231 Paris cedex 05, France
Katia Comte*
Affiliation:
UMR 7245 CNRS-MNHN Molécules de communication et adaptation des micro-organismes, Muséum national d'Histoire naturelle, Case 39, 12, rue Buffon, F-75231 Paris cedex 05, France
Thi Du Chi Tran
Affiliation:
UMR 7245 CNRS-MNHN Molécules de communication et adaptation des micro-organismes, Muséum national d'Histoire naturelle, Case 39, 12, rue Buffon, F-75231 Paris cedex 05, France Faculty of Biology, VNU University of Science, Vietnam National University, Hanoi, Vietnam
Monia El Bour
Affiliation:
Laboratoire de Pathologies des Animaux Aquatiques, Institut National des Sciences et Technologies de la Mer, 2025 Salammbô, Tunisia
*
*Corresponding author: kcomte@mnhn.fr
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Abstract

Proliferations of cyanobacteria have detrimental effects on ecosystem functioning, and on the global freshwater food chain. Many studies have focused on the “in situ” dynamics of bloom-forming cyanobacteria, including Cylindrospermopsis raciborskii and Planktothrix agardhii. Few have used experimental assays to explore the fast-growing ability of naturally co-occurring species. Here we investigated the growth of these species when exposed separately (i.e., in monocultures) to a range of light and nutrient conditions, plus their interactive performances in mixed cultures in a short-time experiment (6 days). The use of microplates made it possible to carry out multiple measurements of in-vivo fluorescence (IVF), and to monitor species-dependent biovolumes. No allelopathic effect was significantly observed for any target species, while significantly lower growth rates were obtained in mixed cultures, which may reflect other interference interactions between the species. We showed that Planktothrix grew faster with low light intensity and high nutrient concentrations, and was drastically inhibited by nitrogen deprivation, in contrast to Cylindrospermopsis. However, Cylindrospermopsis outgrew Planktothrix at high NH4+ concentrations, suggesting that this species may be a serious competitor for the native species in many water systems.

Keywords

Bloom-forming cyanobacteriainteractionsgrowth ratemixed cultures
Type
Research Article
Information
Annales de Limnologie - International Journal of Limnology , Volume 50 , Issue 3 , 2014 , pp. 231 - 240
Copyright
© EDP Sciences, 2014

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References

Anagnostidis, K. and Komárek, J., 1988. Modern approach to the classification system of cyanophytes. 3. Oscillatoriales. Arch. Hydrobiol., 80, 327–472.Google Scholar
Berger, C., Ba, N., Gugger, M., Bouvy, M., Rusconi, F., Couté, A., Troussellier, M. and Bernard, C., 2006. Seasonal dynamics and toxicity of Cylindrospermopsis in Lake Guiers (Senegal, West Africa). FEMS Microbiol. Ecol., 57, 355–366.CrossRefGoogle Scholar
Bonilla, S., Aubriot, L., Soares, M.C.S., Gonzales-Piana, M., Fabre, A., Huszar, V.L.M., Lurning, M., Antoniades, D., Padisák, J. and Kruk, C., 2012. What drives the distribution of the bloom forming cyanobacteria Planktothrix agardhii and Cylindrospermopsis Raciborskii? FEMS Microbiol. Lett., 79, 594–607.CrossRefGoogle ScholarPubMed
Briand, J.-F., Leboulanger, C., Humbert, J.-F., Bernard, C. and Dufour, P., 2004. Cylindrospermopsis raciborskii (Cyanobacteria) invasion at mid-latitudes: selection, wide physiological tolerance, or global warming? J. Phycol., 40, 231–238.CrossRefGoogle Scholar
Bright, D.I. and Walsby, A.E., 2000. The daily integral of growth by Planktothrix rubescens calculated from growth rate in culture and irradiance in Lake Zurich. New Phytol., 146, 301–316.CrossRefGoogle Scholar
Chorus, I. and Bartram, J., 1999. In Toxic Cyanobacteria in Water – A Guide to their Public Health Consequences, Monitoring and Management. E & FN Spon Press, London, 595 p.CrossRefGoogle Scholar
Davis, P.A. and Walsby, A.E., 2002. Comparison of measured growth rates with those calculated from rates of photosynthesis in Planktothrix spp. isolated from Blelham Tarn, English Lake District. New Phytol., 156, 225–239.CrossRefGoogle Scholar
Eisentraeger, A., Dott, W., Klein, J. and Hahn, S., 2003. Comparative studies on algal toxicity testing using fluorometric microplate and Erlenmeyer flask growth-inhibition assays. Ecotox. Environ. Safe., 54, 346–354.CrossRefGoogle Scholar
Graneli, E., Weberg, M. and Salomon, P., 2008. Harmful algal blooms of allelopathic microalgal species: the role of eutrophication. Harmful Algae, 8, 94–102.CrossRefGoogle Scholar
Gregor, J., Jancula, D. and Marsalek, B., 2008. Growth assays with mixed cultures of cyanobacteria and algae assessed by in vivo fluorescence: one step closer to real ecosystems? Chemosphere, 70, 1873–1878.CrossRefGoogle Scholar
Guillard, R.R.L., 1973. Division rates. In: Stein, J.R. (ed.), Phycological Methods, Cambridge Press, New York, 289–311.Google Scholar
Heisler, J., Glibert, P., Burkholder, J., Anderson, D., Cochlan, W., Dennison, W., Gobler, C., Dortch, Q., Heil, C., Humphries, E., Lewitusn, A., Magnien, R., Marshall, H., Sellner, K., Stockwell, D., Stoecker, D. and Suddleson, M., 2008. Eutrophication and harmful algal blooms: a scientific consensus. Harmful Algae, 8, 3–13.CrossRefGoogle ScholarPubMed
Jenhani, A., Fathalli, A. and Romdhane, M.S., 2012. Pytoplankton assemblages in Bir M'Cherga freshwater reservoir (Tunisia). Water Resource and Wetlands. In: Gâştescu, P., Lewis, W. Jr., Breţcan, P. (eds.), Conf. Proceedings, Tulcea – Romania.
Keil, C., Forchert, A., Fastner, J., Szewzyka, U., Rotard, W., Chorus, I. and Kratke, R., 2002. Toxicity and microcystin content of extracts from a Planktothrix bloom and two laboratory strains. Water Res., 36, 2133–2139.CrossRefGoogle ScholarPubMed
Kokocinski, M., Dziga, D., Spoof, L., Stefaniak, K., Jurczak, T., Mankiewicz-Boczek, J. and Meriluoto, J., 2009. First report of the cyanobacterial toxin cylindrospermopsin in the shallow, eutrophic lakes of Western Poland. Chemosphere, 74, 669–675.CrossRefGoogle ScholarPubMed
Kokocinski, M., Stefaniak, K., Mankiewicz-Boczek, J., Izydorczyk, K. and Soininen, J., 2010. The ecology of the invasive cyanobacterium Cylindrospermopsis raciborskii (Nostocales, Cyanophyta) in two hypereutrophic lakes dominated by Planktothrix agardhii (Oscillatoriales, Cyanophyta). Eur. J. Phycol., 45, 365–374.CrossRefGoogle Scholar
Komárek, J. and Anagnostidis, K., 2005. Süsswasserflora von Miteleuropa, Bd 19/2: Cyanoprokaryota. 2. Teil: Oscillatoriales, Elsevier GmbH, Heifelberg, 759 p.Google Scholar
Kotai, J., 1972. Instructions for Preparation of Modified Nutrient Solution Z8 for Algae, Norwegian Institute for Water Research, Oslo, 1–5.Google Scholar
Li, Y. and Li, D., 2012. Competition between toxic Microcystis aeruginosa and nontoxic Microcystis Wesenbergii with Anabaena PCC7120. J. Appl. Phycol., 24, 69–78.CrossRefGoogle Scholar
Løvstad, Ø., 1984. Growth limiting factors for Oscillatoria agardhii and diatoms in eutrophic lakes. OIKOS, 42, 2–12.CrossRefGoogle Scholar
McGregor, G.B. and Fabbro, L.D., 2000. Dominance of Cylindrospermopsis raciborskii (Nostocales, Cyanoprokaryota) in Queensland tropical and subtropical reservoirs: implications for monitoring and management. Lakes  Reservoirs: Res. Manage., 5, 195–205.CrossRefGoogle Scholar
Moisander, P.H., Paerl, H.W. and Zehr, J.P., 2008. Effects of inorganic nitrogen on taxa-specific cyanobacterial growth and nifH expression in a subtropical estuary. J. Limnol. Oceanogr., 53, 2519–2522.CrossRefGoogle Scholar
Mur, L.R. and Beydorff, R.O., 1978. A model of the succession from green to blue-green algae based on light limitation. Ver. Int. Verein. Limnol., 20, 2314–2321.Google Scholar
Nicklisch, A., 1994. Does mortality by nitrogen deficiency influence the succession of Limnothrix redekei and Planktothrix agardhii. Ver. Int. Verein. Limnol., 25, 2214–2217.Google Scholar
Oberhaus, L., Briand, J.-F., Leboulanger, C., Jacquet, S. and Humbert, J.F., 2007. Comparative effects of the quality and quantity of light and temperature on the growth of Planktothrix agardhii and P. rubescens. J. Phycol., 43, 1191–1199.CrossRefGoogle Scholar
O'Neil, J.M., Davis, T.W., Burford, M.A. and Gobler, C.J., 2012. The rise of harmful cyanobacteria blooms: the potential roles of eutrophication and climate change. Harmful Algae, 14, 313–334.CrossRefGoogle Scholar
Padisák, J., 1997. Cylindrospermopsis raciborskii (Woloszynska) Seenayya et Subba Raju, an expanding, highly adaptive cyanobacterium: worldwide distribution and review of its ecology. Arch. Hydrobiol., 107, 563–593.Google Scholar
Paerl, H.W. and Huisman, J., 2009. Climate change: a catalyst for global expansion of harmful cyanobacterial blooms. Environ. Microbiol. Rep., 1, 27–37.CrossRefGoogle ScholarPubMed
Pavlic, Z., Stjepanovic, B., Horvatic, J., Persic, V., Puntaric, D. and Culig, J., 2006. Comparative sensitivity of green algae to herbicides using Erlenmeyer flasks and microplate growth-inhibition assays. Bull. Environ. Contam. Toxicol., 76, 883–890.CrossRefGoogle Scholar
Posselt, A.J., Burford, M.A. and Shaw, G., 2009. Pulses of phosphate promote dominance of the toxic cyanophyte Cylindrospermopsis raciborskii in a subtropical water reservoir. J. Phycol., 45, 540–546.CrossRefGoogle Scholar
Reynolds, C.S., Huszar, V., Kruk, C., Naselli-Flores, L. and Melo, S., 2002. Towards a functional classification of the freshwater phytoplankton . J. Plankton. Res., 24, 417–428.CrossRefGoogle Scholar
Rice, E.L., 1984. Allelopathy (2nd edn,), Academic Press, Orlando, FL.Google Scholar
Rippka, R., 1988. Isolation and purification of cyanobacteria. Method Enzymol., 167, 3–27.CrossRefGoogle ScholarPubMed
Roth, J., Haycock, K., Gagno, J., Soper, C. and Caldarola, J., 1995. L'intégré des analyses de données. Statview Software, Abacus Concepts, California.
Saker, M.L. and Neilan, B.A., 2001. Varied diazotrophies, morphologies and toxicities of genetically similar isolates of Cylindrospermopsis raciborskii (Nostocales, Cyanophyceae) from Northern Australia. Appl. Environ. Microbiol., 67, 1839–1845.CrossRefGoogle ScholarPubMed
Satoh, A., Vudikaria, L.Q., Kurano, N. and Miyachi, S., 2005. Evaluation of the sensitivity of marine microalgal strains to the heavy metals, Cu, As, Pb, and Cd. Environ. Int., 31, 713–722.CrossRefGoogle Scholar
Seenayya, G. and Subba Raju, N., 1972. On the ecology and systematic of the alga known as Anabaenopsis raciborskii (Wolosz.) Elenk. and a critical evaluation of the forms described under the genus Anabaenopsis. In: Desikachary, T.V. (ed.), First International Symposium on Taxonomy and Biology of blue-green algae, Madras.
Shafik, H.M., Herodek, S., Presing, M. and Voros, L., 2001. Factors effecting growth and cell composition of cyanoprokaryote Cylindrospermospis raciborskii (Woloszynska). Algol. Stud., 103, 75–93.Google Scholar
Sinha, R., Leanne, A.P., Timothy, W.D., Burford, M.A., Philip, T.O. and Neilan, B.A., 2012. Increased incidence of Cylindrospermopsis raciborskii in temperate zones – is climate change responsible? Water Res., 46, 1408–1419.CrossRefGoogle ScholarPubMed
Skjelbred, B., Edvardsen, B. and Andersen, T., 2012. A high-throughput method for measuring growth and loss rates in microalgal cultures. J. Appl. Phycol., 24, 1589–1599.CrossRefGoogle Scholar
Stefaniak, K. and Kokocinski, M., 2005. Occurrence of invasive cyanobacteria species in polimictic lakes of the Wielkopolska region (Western Poland). Oceanol. Hydrobiol. St., 34, 137–148.Google Scholar
Sukenik, A., Hadas, O., Kaplan, A. and Quesada, A., 2012. Invasion of Nostocales (cyanobacteria) to subtropical and temperate freshwater lakes – physiological, regional and global driving forces. Front. Microbiol., 3, 86.CrossRefGoogle ScholarPubMed
Sun, J. and Liu, D., 2003. Geometric models for calculating cell biovolume and area for phytoplankton. J. Plankton. Res., 25, 1331–1346.CrossRefGoogle Scholar
Utermöhl, H., 1958. Zur Vervolkommung des quantitativen Phytoplankton, Mrathod. Mitt.  Int. Verein. Limnol., 9, l–38.Google Scholar
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