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Research Article

Acclimation at high temperatures increases the ability of Raphidiopsis raciborskii (Cyanobacteria) to withstand phosphate deficiency and reveals distinct strain responses

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Pages 359-368 | Received 10 Oct 2017, Accepted 30 Nov 2018, Published online: 25 Apr 2019

References

  • Aguilera, A., Gómez, E.B., Kaštovský, J., Echenique, R.O. & Salerno, G.L. (2018). The polyphasic analysis of two native Raphidiopsis isolates supports the unification of the genera Raphidiopsis and Cylindrospermopsis (Nostocales, Cyanobacteria). Phycologia, 57: 130–146.
  • Ahlgren, G. (1987). Temperature functions in biology and their application to algal growth constants. Oikos, 49: 177–190.
  • Ahlgren, G. (1988). Phosphorus as growth-regulating factor relative to other environmental factors in cultured algae. In Phosphorus in Freshwater Ecosystems (48) (Persson, G. & Jansson, M., editors), 191–210. Hydrobiologia, Dordrecht.
  • Amaral, V., Bonilla, S. & Aubriot, L. (2014). Growth optimization of the invasive cyanobacterium Cylindrospermopsis raciborskii in response to phosphate fluctuations. European Journal of Phycology, 49: 134–141.
  • Andersen, R.A. (2005). Algal Culturing Techniques. 1st Ed. Academic Press, London.
  • Antunes, J.T., Leão, P.N. & Vasconcelos, V.M. (2015). Cylindrospermopsis raciborskii: review of the distribution, phylogeography, and ecophysiology of a global invasive species. Frontiers in Microbiology, 6.
  • Aubriot, L., Bonilla, S. & Falkner, G. (2011). Adaptive phosphate uptake behaviour of phytoplankton to environmental phosphate fluctuations. FEMS Microbiology Ecology, 77: 1–16.
  • Bonilla, S., Aubriot, L., Soares, M.C.S., González-Piana, M., Fabre, A., Huszar, V.L.M., Lürling, M., Antoniades, D., Padisák, J. & Kruk, C. (2012). What drives the distribution of the bloom-forming cyanobacteria Planktothrix agardhii and Cylindrospermopsis raciborskii? FEMS Microbiology Ecology, 79: 594–607.
  • Bonilla, S., González-Piana, M., Soares, M.C.S., Huszar, V.L.M., Becker, V., Somma, A., Marinho, M.M., Kokociński, M., Dokulil, M., Antoniades, D. & Aubriot, L. (2016). The success of the cyanobacterium Cylindrospermopsis raciborskii in freshwaters is enhanced by the combined effects of light intensity and temperature. Journal of Limnology, 75: 606–617.
  • Brentano, D.M., Giehl, E.L.H. & Petrucio, M.M. (2016). Abiotic variables affect STX concentration in a meso-oligotrophic subtropical coastal lake dominated by Cylindrospermopsis raciborskii (Cyanophyceae). Harmful Algae, 56: 22–28.
  • Briand, J.F., Robillot, C., Quiblier-Llobéras, C., Humbert, J.F., Couté, A. & Bernard, C. (2002). Environmental context of Cylindrospermopsis raciborskii (Cyanobacteria) blooms in a shallow pond in France. Water Research, 36: 3183–3192.
  • Briand, J., Leboulanger, C., Humbert, J., Bernard, C. & Dufour, P. (2004). Cylindrospermopsis raciborskii (Cyanobacteria) invasion at mid-latitudes: selection, wide physiological tolerance, or global warming? Journal of Phycology, 40: 231–238.
  • Burford, M.A., Beardall, J., Willis, A., Orr, P.T., Magalhaes, V.F., Rangel, L.M., Azevedo, S.M.F.O.E. & Neilan, B.A. (2016). Understanding the winning strategies used by the bloom-forming cyanobacterium Cylindrospermopsis raciborskii. Harmful Algae, 54: 44–53.
  • Burford, M.A., Willis, A., Chuang, A., Man, X. & Orr, P.T. (2018). Recent insights into physiological responses to nutrients by the cylindrospermopsin producing cyanobacterium, Cylindrospermopsis raciborskii. Journal of Oceanology and Limnology, 36: 1032–1039.
  • Carey, C.C., Ibelings, B.W., Hoffmann, E.P., Hamilton, D.P. & Brookes, J.D. (2012). Eco-physiological adaptations that favour freshwater cyanobacteria in a changing climate. Water Research, 46: 1394–1407.
  • Chase, J.M. (2010). Stochastic community assembly causes higher biodiversity in more productive environments. Science, 328: 1388–1391.
  • Chonudomkul, D., Yongmanitchai, W., Theeragool, G., Kawachi, M., Kasai, F., Kaya, K. & Watanabe, M.M. (2004). Morphology, genetic diversity, temperature tolerance and toxicity of Cylindrospermopsis raciborskii (Nostocales, Cyanobacteria) strains from Thailand and Japan. FEMS Microbiology Ecology, 48: 345–355.
  • Falkner, R., Priewasser, M. & Falkner, G. (2006). Information processing by cyanobacteria during adaptation to environmental phosphate fluctuations. Plant Signaling and Behavior, 1: 212–220.
  • Hennemann, M.C. & Petrucio, M.M. (2011). Spatial and temporal dynamic of trophic relevant parameters in a subtropical coastal lagoon in Brazil. Environmental Monitoring and Assessment, 181: 347–361.
  • Hillebrand, H., Dürselen, C., Kirschtel, D., Zohary, T. & Pollingher, U. (1999). Biovolume calculation for pelagic and benthic microalgae. Journal of Phycology, 35: 403–424.
  • Hunter-Cevera, K.R., Neubert, M.G., Olson, R.J., Solow, A.R., Shalapyonok, A. & Sosik, H.M. (2016). Physiological and ecological drivers of early spring blooms of a coastal phytoplankter. Science, 354: 326–329.
  • Istvánovics, V., Shafik, H.M., Présing, M. & Juhos, S. (2000). Growth and phosphate uptake kinetics of the cyanobacterium Cylindrospermopsis raciborskii (Cyanophyceae) in throughflow cultures. Freshwater Biology, 43: 257–275.
  • Kenesi, G., Shafik, H.M., Kovács, A.W., Herodek, S. & Présing, M. (2009). Effect of nitrogen forms on growth, cell composition and N2 fixation of Cylindrospermopsis raciborskii in phosphorus-limited chemostat cultures. Hydrobiologia, 623: 191–202.
  • Kovács, A.W., Présing, M. & Vörös, L. (2016). Thermal-dependent growth characteristics for Cylindrospermopsis raciborskii (Cyanoprokaryota) at different light availabilities: methodological considerations. Aquatic Ecology, 50: 623–638.
  • Litchman, E. & Klausmeier, C.A. (2008). Trait-based community ecology of phytoplankton. Annual Review of Ecology, Evolution and Systematics, 39: 615–639.
  • Lürling, M., Eshetu, F., Faassen, E.J., Kosten, S. & Huszar, V.L.M. (2013). Comparison of cyanobacterial and green algal growth rates at different temperatures. Freshwater Biology, 58: 552–559.
  • Mehnert, G., Rücker, J., Nicklisch, A., Leunert, F. & Wiedner, C. (2012). Effects of thermal acclimation and photoacclimation on lipophilic pigments in an invasive and a native cyanobacterium of temperate regions. European Journal of Phycology, 47: 182–192.
  • Miotto, M.C., Costa, L.D.F., Brentano, D.M., Nader, C., dos Santos Souza, L., Gressler, P.D., Laudares-Silva, R., Yunes, J.S., Barufi, J.B. & Rörig, L.R. (2017). Ecophysiological characterization and toxin profile of two strains of Cylindrospermopsis raciborskii isolated from a subtropical lagoon in Southern Brazil. Hydrobiologia, 802: 97–113.
  • Moreira, C., Fathalli, A., Vasconcelos, V. & Antunes, A. (2015). Phylogeny and biogeography of the invasive cyanobacterium Cylindrospermopsis raciborskii. Archives of Microbiology, 197: 47–52.
  • Mur, L.R., Skulberg, O.M. & Utkilen, H. (1999). Cyanobacteria in the environment. In Toxic Cyanobacteria in Water: A Guide to their Public Health Consequences, Monitoring and Management (Chorus, I. & Bartram, J.editors,), 25–54. World Health Organization, London.
  • Padisák, J. & Istvánovics, V. (1997). Differential response of blue-green algal groups to phosphorus load reduction in a large shallow lake: Balaton, Hungary. SIL Proceedings, 1922–2010, 26: 574–580.
  • Padisák, J., Soróczki-Pinté, E. & Rezner, Z. (2003). Sinking properties of some phytoplankton shapes and the relation of form resistance to morphological diversity of phytoplankton – an experimental study. Hydrobiologia, 500: 243–257.
  • Piccini, C., Aubriot, L., Fabre, A., Amaral, V., González-Piana, M., Giani, A., Figueredo, C.C., Vidal, L., Kruk, C. & Bonilla, S. (2011). Genetic and eco-physiological differences of South American Cylindrospermopsis raciborskii isolates support the hypothesis of multiple ecotypes. Harmful Algae, 10: 644–653.
  • Pierangelini, M., Stojkovic, S., Orr, P.T. & Beardall, J. (2014). Elevated CO2 causes changes in the photosynthetic apparatus of a toxic cyanobacterium, Cylindrospermopsis raciborskii. Journal of Plant Physiology, 171: 1091–1098.
  • Pierangelini, M., Sinha, R., Willis, A., Burford, M.A., Orr, P.T., Beardall, J. & Neilan, B.A. (2015). Constitutive cylindrospermopsin pool size in Cylindrospermopsis raciborskii under different light and CO2 partial pressure conditions. Applied and Environmental Microbiology, 81: 3069–3076.
  • Posselt, A.J., Burford, M.A. & Shaw, G. (2009). Pulses of phosphate promote dominance of the toxic cyanophyte Cylindrospermopsis raciborskii in a subtropical water reservoir. Journal of Phycology, 45: 540–546.
  • Prentice, M.J., O’Brien, K.R., Hamilton, D.P. & Burford, M.A. (2015). High- and low-affinity phosphate uptake and its effect on phytoplankton dominance in a phosphate-depauperate lake. Aquatic Microbial Ecology, 75: 139–153.
  • Recknagel, F., Orr, P.T. & Cao, H. (2014). Inductive reasoning and forecasting of population dynamics of Cylindrospermopsis raciborskii in three sub-tropical reservoirs by evolutionary computation. Harmful Algae, 31: 26–34.
  • Reynolds, C.S. (2006). The Ecology of Phytoplankton. Cambridge University Press, Cambridge.
  • Reynolds, C.S., Oliver, R.L. & Walsby, A.E. (1987). Cyanobacterial dominance: the role of buoyancy regulation in dynamic lake environments. New Zealand Journal of Marine and Freshwater Research, 21: 379–390.
  • Ryan, C.N., Thomas, M.K. & Litchman, E. (2017). The effects of phosphorus and temperature on the competitive success of an invasive cyanobacterium. Aquatic Ecology, 51: 463–472.
  • Sinha, R., Pearson, L.A., Davis, T.W., Burford, M.A., Orr, P.T. & Neilan, B.A. (2012). Increased incidence of Cylindrospermopsis raciborskii in temperate zones – is climate change responsible? Water Research, 46: 1408–1419.
  • Sinha, R., Pearson, L.A., Davis, T.W., Muenchhoff, J., Pratama, R., Jex, A., Burford, M.A. & Neilan, B.A. (2014). Comparative genomics of Cylindrospermopsis raciborskii strains with differential toxicities. BMC Genomics, 15: 83.
  • Stucken, K., Murillo, A.A., Soto-Liebe, K., Fuentes-Valdés, J.J., Méndez, M.A. & Vásquez, M. (2009). Toxicity phenotype does not correlate with phylogeny of Cylindrospermopsis raciborskii strains. Systematic and Applied Microbiology, 32: 37–48.
  • Thomas, M.K. & Litchman, E. (2016). Effects of temperature and nitrogen availability on the growth of invasive and native cyanobacteria. Hydrobiologia, 763: 357–369.
  • Thrane, J.-E., Hessen, D.O. & Andersen, T. (2017). Plasticity in algal stoichiometry: experimental evidence of a temperature-induced shift in optimal supply N:P ratio. Limnology and Oceanography, 62: 1346–1354.
  • Varkey, D., Mazard, S., Ostrowski, M., Tetu, S.G., Haynes, P. & Paulsen, I.T. (2015). Effects of low temperature on tropical and temperate isolates of marine Synechococcus. ISME Journal, 10: 1252.
  • Várkonyi, Z., Zsiros, O., Farkas, T., Garab, G. & Gombos, Z. (2000). The tolerance of cyanobacterium Cylindrospermopsis raciborskii to low-temperature photo-inhibition affected by the induction of polyunsaturated fatty acid synthesis. Biochemical Society Transactions, 28: 892–894.
  • Willis, A., Adams, M.P., Chuang, A.W., Orr, P.T., O’Brien, K.R. & Burford, M.A. (2015). Constitutive toxin production under various nitrogen and phosphorus regimes of three ecotypes of Cylindrospermopsis raciborskii ((Wołoszyńska) Seenayya et Subba Raju). Harmful Algae, 47: 27–34.
  • Willis, A., Chuang, A.W., Woodhouse, J.N., Neilan, B.A. & Burford, M.A. (2016). Intraspecific variation in growth, morphology and toxin quotas for the cyanobacterium, Cylindrospermopsis raciborskii. Toxicon, 119: 307–310.
  • Willis, A., Woodhouse, J., Ongley, S., Jex, A., Burford, M. & Neilan, B. (2018). Genome variation in nine co-occurring toxic Cylindrospermopsis raciborskii strains. Harmful Algae, 73: 157–166.
  • Wu, Z., Zeng, B., Li, R. & Song, L. (2012). Physiological regulation of Cylindrospermopsis raciborskii (Nostocales, Cyanobacteria) in response to inorganic phosphorus limitation. Harmful Algae, 15: 53–58.
  • Yema, L., Litchman, E. & de Tezanos Pinto, P. (2016). The role of heterocytes in the physiology and ecology of bloom-forming harmful cyanobacteria. Harmful Algae, 60: 131–138.

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