Advertisement

Hydrobiologia

, Volume 802, Issue 1, pp 97–113 | Cite as

Ecophysiological characterization and toxin profile of two strains of Cylindrospermopsis raciborskii isolated from a subtropical lagoon in Southern Brazil

  • Maria Cecília Miotto
  • Luiza Dy Fonseca Costa
  • Débora Monteiro Brentano
  • Camila Nader
  • Luana dos Santos Souza
  • Pablo Diego Gressler
  • Roselane Laudares-Silva
  • João Sarkis Yunes
  • José Bonomi Barufi
  • Leonardo Rubi Rörig
Primary Research Paper

Abstract

In the present work, we attempted to characterize two isolates of Cylindrospermopsis raciborskii, LP1 and LP2, from Peri Lagoon, for their morphology, ecophysiology, and toxin profiles. The genetic identity of the isolates was confirmed by amplifying and sequencing 16S rRNA. The isolates showed different morphologies and significant differences in the length of trichomes. LP2 showed a trend for higher growth rates than LP1 at the different temperatures and N:P ratios. Both isolates showed low light requirements, but were able to tolerate irradiances of around 200 μmol photons m−2 s−1. LP2 showed higher concentrations of saxitoxin than LP1 and wider range of analogs, therefore being considered more toxic. These results support the hypothesis of ecotype selection for this species, which probably originated in response to environmental fluctuations in Peri Lagoon. Dominance during almost the entire year can be explained by the alternation of these ecotypes in the total biomass contribution according to their physiological advantages, contributing to the ecological success of this species.

Keywords

Cyanobacteria Ecotypes Cyanotoxins Saxitoxin 

Notes

Acknowledgements

We would like to thank the Coordination for the Improvement of Higher Education Personnel (CAPES—Brazil) for providing the scholarship, National Council for Scientific and Technological Development (CNPq) and Fundação de Amparo à Pesquisa e Inovação de Santa Catarina (FAPESC) for research funding, Cecília Barberena de Vinatea for isolating LP1, Mateus Reck and Gustavo Klabunde for their help and support in molecular analyses and Eduardo de Oliveira Bastos for taking and editing the images.

References

  1. Ács, A., A. W. Kovács, J. K. Csepregi, N. Töro, G. Kiss, J. Gyor, A. Vehovszky, N. Kováts & A. Farkas, 2013. The ecotoxicological evaluation of Cylindrospermopsis raciborskii from Lake Balaton (Hungary) employing a battery of bioassays and chemical screening. Toxicon 70: 98–106.CrossRefPubMedGoogle Scholar
  2. Alster, A., R. N. Kaplan-Levy, A. Sukenik & T. Zohary, 2010. Morphology and phylogeny of a non-toxic invasive Cylindrospermopsis raciborskii from a Mediterranean lake. Hydrobiologia 639: 115–138.CrossRefGoogle Scholar
  3. Al-Tebrineh, J., T. K. Mihali, F. Pomati & B. A. Neilan, 2010. Detection of saxitoxin-producing cyanobacteria and Anabaena circinalis in environmental water blooms by quantitative PCR. Applied and Environmental Microbiology 76(23): 7836–7842.CrossRefPubMedPubMedCentralGoogle Scholar
  4. Andersen, R. A., 2005. Algal Culturing Techniques. Elsevier, Academic Press, Amsterdam: 596.Google Scholar
  5. Arar, E.J. & G.B. Collins, 1997. “In vitro” determination of Chlorophyll a and Pheophytina in marine and freshwater phytoplankton by fluorescence. EPA, Cincinnati. (EPA metod 445.0)Google Scholar
  6. Aubriot, L. & S. Bonilla, 2012. Rapid regulation of phosphate uptake in freshwater cyanobacterial blooms. Aquatic Microbial Ecology 67: 251–263.CrossRefGoogle Scholar
  7. Bai, F., R. Liu, Y. Yang, X. Ran, J. Shi & Z. Wu, 2014. Dissolved organic phosphorus use by the invasive freshwater diazotroph cyanobacterium, Cylindrospermopsis raciborskii. Harmful Agae 39: 112–120.CrossRefGoogle Scholar
  8. Bailey, S. & A. Grossman, 2008. Photoprotection in cyanobacteria: regulation of light harvesting. Photochemistry and Photobiology 84: 1410–1420.CrossRefPubMedGoogle Scholar
  9. Baptista, M. G. & B. Nixdorf, 2014. Low disturbances favor steady state: Case of cyanobacterial monodominance in a Brazilian coastal lagoon. Inland Waters 4: 243–254.CrossRefGoogle Scholar
  10. Bernard, C., M. Harvey, J. F. Briand, R. Biré, S. Krys & J. J. Fontaine, 2003. Toxicological comparison of diverse strains: Evidence of liver damage caused by a French strain. Environmental Toxicology 18(3): 176–186.CrossRefPubMedGoogle Scholar
  11. Bilger, W. & O. Björkman, 1990. Role of the xanthophyll cycle in photoprotection elucidated by measurements of light-induced absorbance changes, fluorescence and photosynthesis in leaves of Hedera canariensis. Photosynthesis Research 25(3): 173–185.CrossRefPubMedGoogle Scholar
  12. Bonilla, S., L. Aubriot, M. C. S. Soares, M. González-Piana, A. Fabre, V. L. M. Huszar, M. Lürling, D. Antoniades, J. Padisák & C. Kruk, 2012. What drives the distribution of the bloom-forming cyanobacteria Planktothrix agardhii and Cylindrospermopsis raciborskii? FEMS Microbiology Ecology 79(3): 594–607.CrossRefPubMedGoogle Scholar
  13. Bouvy, M., R. J. R. Molica, S. De Oliveira, M. Marinho & B. Beker, 1999. Dynamics of a toxic cyanobacterial bloom (Cylindrospermopsisraciborskii) in a shallow reservoir in the semi–arid region of Northeast Brazil. Aquatic Microbiology Ecology 20: 285–297.CrossRefGoogle Scholar
  14. Brentano, D. M., E. L. H. Giehl & M. M. Petrucio, 2016. Abiotic variables affect STX concentration in a meso-oligotrophic subtropical coastal lake dominated by Cylindrospermopsis raciborskii (Cyanophyceae). Harmful Algae 56: 22–28.CrossRefPubMedGoogle Scholar
  15. Briand, J. F., C. Leboulanger, J. F. Humbert, C. Bernanrd & P. Dufour, 2004. Cylindrospermopsis raciborskii (Cyanobacteria) invasion at mid latitudes: selection, wide physiological tolerance, or global warming? Journal of Phycology 40: 231–238.CrossRefGoogle Scholar
  16. Briand, J. F., C. Robillot, C. Quiblier-Lloberas, J. F. Humbert & A. Coute, 2002. Environmental context of Cylindrospermopsisraciborskii (cyanobacteria) blooms in a shallow pond in France. Water Research 36: 3183–3192.CrossRefPubMedGoogle Scholar
  17. Chislock, M. F., K. L. Sharp & A. E. Wilson, 2014. Cylindrospermopsis raciborskii dominates under very low and high nitrogen-to-phosphorus ratios. Water Research 49: 207–214.CrossRefPubMedGoogle Scholar
  18. Chonudomkul, D., W. Yongmanitchai, G. Theeragool, M. Kawachi, F. Kasai, K. Kaya & M. M. Watanabe, 2004. Morphology, genetic diversity, temperature tolerance and toxicity of Cylindrospermopsis raciborskii (Nostocales, Cyanobacteria) strains from Thailand and Japan. FEMS Microbiology Ecology 48: 345–355.CrossRefPubMedGoogle Scholar
  19. Detoni, A. M. S., L. D. F. Costa, L. A. Pacheco & J. S. Yunes, 2016. Toxic Trichodesmium bloom occurrence in the southwestern South Atlantic Ocean. Toxicon 110: 51–55.CrossRefGoogle Scholar
  20. Dyble, J., H. W. Paerl & B. A. Neilan, 2002. Genetic characterization of Cylindrospermopsis raciborskii (Cyanobacteria) isolates from diverse geographic origins based on nifh and cpcba-igs nucleotide sequence analysis. Applied and Environmental Microbiology 68: 2567–2571.CrossRefPubMedPubMedCentralGoogle Scholar
  21. Fastner, J., R. Heinze, A. R. Humpage, U. Mischke, G. K. Eaglesham & I. Chorus, 2003. Cylindrospermopsin occurrence in two German lakes and preliminary assessment of toxicity and toxin production of Cylindrospermopsis raciborskii (Cyanobacteria) isolates. Toxicon 42: 3313–3321.CrossRefGoogle Scholar
  22. Ferrão Filho, A. S., S. M. da Costa, M. G. L. Ribeiro & M. F. O. Azevedo, 2008. Effects of a saxitoxin-producer strain of Cylindrospermopsis raciborskii (cyanobacteria) on the swimming movements of cladocerans. Environmental Toxicology 23: 161–168.CrossRefGoogle Scholar
  23. Figueredo, C. C., A. Giani & D. F. Bird, 2007. Does allelopathy contribute to Cylindrospermopsis raciborskii (Cyanobacteria) bloom occurrence and geographic expansion? Journal of Phycology 43: 256–265.CrossRefGoogle Scholar
  24. Givnish, T. J., 1988. Adaptation to sun and shade: A whole-plant perspective. Australian Journal of Plant Physiology 15: 63–92.CrossRefGoogle Scholar
  25. Gomes, A. M. A., M. M. Marinho & S. M. F. O. Azevedo, 2013. Which factors are related to the success of Cylindrospermopsis raciborskii in Brazilian Aquatic Systems? In Ferrão-Filho, A. S. (ed.), Cyanobacteria: ecology, Toxicology and Management. Nova Science Publishers Inc, New York: 73–94.Google Scholar
  26. Gorham, P. R., R. W. McLachlan & U. T. Hammer, 1964. Isolation and culture of toxic strains of Anabaena flos-aquae. Breb. Int. Ver. Theor. Angew. Limnol. Verh. 19: 796–804.Google Scholar
  27. Grellmann, C., 2006. Aspectos da morfologia e da ecologia de Cylindrospermopsis raciborskii (Woloszynska) Seenayya et Subba Raju e da produção de cianotoxinas na Lagoa do Peri, Florianópolis, SC, Brasil. Msc Thesis, Universidade Federal de Santa Catarina, Brazil.Google Scholar
  28. Guildford, S. J. & R. E. Hecky, 2000. Total nitrogen, total phosphorus, and nutrient limitation in lakes and oceans: Is there a common relationship? Limnology and Oceanography 45: 1213–1223.CrossRefGoogle Scholar
  29. Henley, W. J., 1993. On the measurement and interpretation of photosynthetic light-response curves in algae in the context of photoinhibition and diel changes. Journal of Phycology 35: 729–739.CrossRefGoogle Scholar
  30. Hennemann, M. C. & M. M. Petrucio, 2010. Seasonal phytoplankton response to increased temperature and phosphorus inputs in a freshwater coastal lagoon, Southern Brazil: a microcosm bioassay. Acta Limnologica Brasiliensia 22: 295–305.CrossRefGoogle Scholar
  31. Hennemann, M. C. & M. M. Petrucio, 2011. Spatial and temporal dynamic of trophic relevant parameters in a subtropical coastal lagoon in Brazil. Environmental Monitoring and Assessment 181: 347–361.CrossRefPubMedGoogle Scholar
  32. Hillebrand, H., C. D. Dürselen, D. Kirschtel, U. Pollingher & T. Zohary, 1999. Biovolume calculation for pelagic and benthic microalgae. Journal of Phycology 35: 403–424.CrossRefGoogle Scholar
  33. Hoff-Risseti, C., F. A. Dörr, P. D. C. Schaker, E. Pinto, V. R. Werner & M. F. Fiore, 2013. Cylindrospermopsin and saxitoxin synthetase genes in Cylindrospermopsis raciborskii strains from brazilian freshwater. PLoS ONE 8: e74238.CrossRefPubMedPubMedCentralGoogle Scholar
  34. Holland, A. & S. Kinnear, 2013. Interpreting the possible ecological role(s) of cyanotoxins: Compounds for competitive advantage and/or physiological aide? Marine Drugs 11: 2239–2258.CrossRefPubMedPubMedCentralGoogle Scholar
  35. Istvaánovics, V., H. M. Shafik, M. Présing & S. Juhos, 2000. Growth and phosphate uptake kinetics of the cyanobacterium Cylindrospermopsis raciborskii (Cyanophyceae) in through flow cultures. Freshwater Biology 43: 257–275.CrossRefGoogle Scholar
  36. Kana, T. M. & P. M. Glibert, 1987. Effect of irradiances up to 2000 mEm−2 s−1 on marine Synechococcus WH7803-I. Growth, pigmentation, and cell composition. Deep-Sea Research 34: 479–495.CrossRefGoogle Scholar
  37. Komárek, J. & J. Komárková, 2003. Phenotype diversity of the cyanoprokaryotic genus Cylindrospermopsis (Nostocales); review 2002. Czech Phycology 3: 1–30.Google Scholar
  38. Komárková, J., 1998. The tropical planktonic genus Cylindrospermopsis (Cyanophytes, Cyanobacteria). In: Azevedo, T. P. (ed.), Anais dos IV Congresso latino-americano de Ficologia, II Reunião Írbero americana de Ficologia e VII Reunião Brasileira de Ficologia. - Secretaria do Meio Ambiente do Estado de São Paulo, Vol. I: 327–340.Google Scholar
  39. Komárková, J., R. Laudares-Silva & P. A. C. Senna, 1999. Extreme morphology of Cylindrospermopsis raciborskii (Nostocales, Cyanobacteria) in the Lagoa do Peri, a freshwater coastal lagoon, Santa Catarina, Brazil. Algological Studies 94: 207–222.Google Scholar
  40. Lagos, N., H. Onodera, P. A. Zagatto, D. Andrinolo, S. M. F. O. Azevedo & Y. Oshima, 1999. The first evidence of paralytic shelfish toxins in the freshwater cyanobacterium Cylindrospermopsis raciborskii, isolated from Brazil. Toxicon 37: 1359–1373.CrossRefPubMedGoogle Scholar
  41. Laudares-Silva, R., 1999. Aspectos limnológicos, variabilidade espacial e temporal na estrutura da comunidade fitoplanctônica da Lagoa do Peri, Santa Catarina, Brasil. PhD Thesis, Universidade Federal de São Carlos, Brazil.Google Scholar
  42. Molica, R., H. Onodera, C. Garcia, M. Rivas, D. Andrinolo, S. Nascimento, H. Meguro, Y. Oshima, S. Azevedo & N. Lagos, 2002. Toxins in the freshwater cyanobacterium Cylindrospermospsis raciborskii (Cyanophyceae) isolated from Tabocas reservoir in Caruaru, Brazil, including demonstration of a new saxitoxin analogue. Phycology 41: 606–611.CrossRefGoogle Scholar
  43. Neilan, B. A., D. Jacobs, T. D. Dot, L. L. Blackall, P. R. Hawkins, P. T. Cox & A. E. Goodman, 1997. rRNA sequences and evolutionary relationships among toxic and nontoxic cyanobacteria of the Genus Microcystis. International Journal of Systematic Bacteriology. 47: 693–697.CrossRefPubMedGoogle Scholar
  44. Neilan, B. A., M. L. Saker, J. Fastner, A. Torokne & B. P. Burns, 2003. Phylogeography of the invasive cyanobacterium Cylindrospermopsis raciborskii. Molecular Ecology 12: 133–140.CrossRefPubMedGoogle Scholar
  45. O’Brien, K. R., M. A. Burford & J. D. Brookes, 2009. Effects of light history on primary productivity in a phytoplankton community dominated by the toxic cyanobacterium Cylindrospermopsis raciborskii. Freshwater Biology 54: 272–282.CrossRefGoogle Scholar
  46. Ohtani, I., R. E. Moore & M. T. C. Runnegar, 1992. Cylindrospermopsin: a potent hepatotoxin from the blue–green alga Cylindrospermopsis raciborskii. Journal of the American Chemical Society 114: 7941–7942.CrossRefGoogle Scholar
  47. Oshima, Y., 1995. Postcolumn derivatization liquid chromatographic methods for paralytic shellfish toxins. Journal of AOAC International 78: 528–532.Google Scholar
  48. Padisák, J., 1997. Cylindrospermopsis raciborskii (Woloszyska) Seenayya et Subba Raju, an expanding, highly adaptive cyanobacterium: worldwide distribution and review of its ecology. Archives of Hydrobiology Supplement 107: 563–593.Google Scholar
  49. Padisák, J. & C. S. Reynolds, 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.CrossRefGoogle Scholar
  50. Piccini, C., L. Aubriot, A. Fabre, V. Amaral, M. Gonzáles-Piana, A. Giand, C. C. Figueredo, L. Vidal, C. Kruk & S. Bonilla, 2011. Genetic and eco-physiological differences of South American Cylindrospermopsis raciborskii isolates support the hypothesis of multiple ecotypes. Harmful Algae 10: 644–653.CrossRefGoogle Scholar
  51. Pierangelini, M., S. Stojkovic, P. T. Orr & J. Beardall, 2014. Photosynthetic characteristics of two Cylindrospermopsis raciborskii strains differing in their toxicity. Journal of Phycology 50: 292–302.CrossRefPubMedGoogle Scholar
  52. Pierangelini, M., S. Stojkovic, P. T. Orr & J. Beardall, 2015. Photo-acclimation to low light—Changes from growth to antenna size in the cyanobacterium Cylindrospermopsis raciborskii. Harmful Algae 46: 11–17.CrossRefGoogle Scholar
  53. Platt, T., C. L. Gallegos & W. G. Harrison, 1980. Photoinhibition of photosynthesis in natural assemblages of marine phytoplankton. Journal of Marine Research 38: 687–701.Google Scholar
  54. Pomati, F., B. A. Neilan, T. Suzuki, G. Manarolla & C. Rossetti, 2003. Enhancement of intracellular saxitoxin accumulation by lidocaine hydrochloride in the cyanobacterium Cylindrospermopsis raciborskii T3 (Nostocales). Journal of Phycology 39: 535–542.CrossRefGoogle Scholar
  55. Poniedziałek, B., P. Rzymski, M. Kokocinki & J. Karczewski, 2015. Toxic potencies of metabolite(s) of non-cylindrospermopsin producing Cylindrospermopsis raciborskii isolated from temperate zone in human white cells. Chemosphere 120: 608–614.CrossRefPubMedGoogle Scholar
  56. Rangel, L. M., K. A. Ger, L. H. S. Silva, M. C. S. Soares, E. J. Faassen & M. Lürling, 2016. Growth and temperature-related phenotypic plasticity in the cyanobacterium Cylindrospermopsis raciborskii. Microbiology of Aquatic Systems 71: 835–844.Google Scholar
  57. Recknagel, F., P. T. Orr & H. Cao, 2014. Inductive reasoning and forecasting of population dynamics of Cylindrospermopsis raciborskii in three sub-tropical reservoirs by evolutionary computation. Harmful Algae 31: 26–34.CrossRefPubMedGoogle Scholar
  58. Reynolds, C. S., 2006. The Ecology of Phytoplankton. Cambridge University Press, Cambridge: 535.CrossRefGoogle Scholar
  59. Rourke, W. A., C. J. Murphy, G. Pitcher, J. M. Van de Riet, B. G. Burns, K. M. Thomas & M. A. Quilliam, 2008. Rapid postcolumn methodology for determination of paralytic shellfish toxins in shellfish tissue. Journal of AOAC International 91: 589–597.PubMedGoogle Scholar
  60. Rzymski, P., B. Poniedziałek, M. Kokocinski, T. Jurczak, D. Lipski & K. Wiktorowicz, 2014. Interspecific allelopathy in cyanobacteria: Cylindrospermopsin and Cylindrospermopsis raciborskii effect on the growth and metabolism of Microcystis aeruginosa. Harmful Algae 3: 1–8.CrossRefGoogle Scholar
  61. Rzymski, P., B. Poniedziałek, J. Mankiewicz-Boczek, E. J. Faassen, T. Jurczak, I. Gągała-Borowska, A. Ballot, M. Lürling & M. Kokocinski, 2017. Polyphasic toxicological screening of Cylindrospermopsis raciborskii and Aphanizomenon gracile isolated in Poland. Algal Research 24: 72–80.CrossRefGoogle Scholar
  62. Saker, M. L. & B. A. Neilan, 2001. Varied Diazotrophies, Morphologies and Toxicities of genetically similar isolates of Cylindrospermopsis raciborskii (Nostocales, Cyanophyceae) from Northern Australia. Applied Environmental Microbiology 67: 1839–1845.CrossRefPubMedPubMedCentralGoogle Scholar
  63. Saker, M. L. & D. J. Griffiths, 2001. Occurrence of blooms of the cyanobacterium Cylindrospermopsis raciborskii (Woloszynska) Seenayya and Subba Raju from a north Queensland domestic water supply. Marine and Freshwater Research 52: 907–915.CrossRefGoogle Scholar
  64. Saker, M. L., B. A. Neilan & D. J. Griffihs, 1999. Two morphological forms of Cylindrospermopsis raciborskii (cyanobacteria) isolated from Solomon Dam, Palm Island, Queensland. Journal of Phycology 35: 599–606.CrossRefGoogle Scholar
  65. Shafik, H. M., M. Herodek, M. Présing & L. Vörös, 2001. Factors effecting growth and cell composition of cyanoprokaryote Cylindrospermopsis raciborskii (Wolsz) Seenayya et Subba Raju. Archiv fuer Hydrobiologie Supplement band. Algological Studies 103: 75–94.Google Scholar
  66. Shafik, H. M., L. Vörös, P. Spróber, M. Présing & A. Kovács, 2003. Some special morphological features of Cylindrospermopsisraciborskii in batch and continuous cultures. Hydrobiologia 506–509: 163–167.CrossRefGoogle Scholar
  67. Silveira, M.H., 2013. Estrutura e dinâmica do fitoplâncton e fatores direcionadores da dominância anual de cianobactérias em uma lagoa rasa subtropical (lagoa do Peri, SC). Msc Thesis, Universidade Federal de Santa Catarina, Brazil.Google Scholar
  68. Simonassi, J. C., 2001. Caracterização da Lagoa do Peri, através da análise de parâmetros físico-químicos e biológicos, como subsídio ao gerenciamento dos recursos hídricos da Ilha de Santa Catarina, SC, Brasil. Msc Thesis, Universidade Federal de Santa Catarina, Brazil, 72 p.Google Scholar
  69. Sinha, R., L. A. Pearson, T. W. Davis, M. A. Burford, P. T. Orr & B. A. Neilan, 2012. Increased incidence of Cylindrospermopsis raciborskii in temperate zones e is climate change responsible? Water Research 46: 1408–1419.CrossRefPubMedGoogle Scholar
  70. Soares, M. C., M. Lürling, R. Panosso & V. L. M. Huszar, 2009. Effects of the cyanobacterium Cylindrospermopsis raciborskii on feeding and life-history characteristics of the grazer Daphnia magna. Ecotoxicology and Environmental Safety 72: 1183–1189.CrossRefPubMedGoogle Scholar
  71. Soares, M. C. S., M. Lürling & V. L. M. Huszar, 2013a. Growth and temperature-related phenotypic plasticity in the cyanobacterium Cylindrospermopsis raciborskii. Phycological Research 61: 61–67.CrossRefGoogle Scholar
  72. Soares, M. C. S., V. L. M. Huszar, M. N. Miranda, M. M. Mello, F. Roland & M. Lürling, 2013b. Cyanobacterial dominance in Brazil: distribution and environmental preferences. Hydrobiologia 717: 1–12.CrossRefGoogle Scholar
  73. Soto-Liebe, K., A. A. Murillo, B. Krock, K. Stucken, J. J. Fuentes-Valdés, N. Trefault, A. Cembella & M. Vásquez, 2010. Reassessment of the toxin profile of Cylindrospermopsis raciborskii T3 and function of putative sulfotransferases in synthesis of sulfated and sulfonated PSP toxins. Toxicon 56: 1350–1361.CrossRefPubMedGoogle Scholar
  74. Stevens, M., S. Peigneur & J. Tytgat, 2011. Neurotoxins and their binding areas on voltage-gated sodium channels. Frontiers in Pharmacology 2: 1–12.CrossRefGoogle Scholar
  75. Tonetta, D., M. M. Petrucio & R. Laudares-Silva, 2013. Temporal variation in phytoplankton community in a freshwater coastal lake of southern Brazil. Acta Limnologica Brasiliensia 25: 99–110.CrossRefGoogle Scholar
  76. Tonetta, D., M. C. Hennemann, D. M. Brentano & M. M. Petrucio, 2015. Considerations regarding the dominance of Cylindrospermopsis raciborskii under low light availability in a low phosphorus lake. Acta Botanica Brasilica 29: 448–451.CrossRefGoogle Scholar
  77. Tucci, A. & C. Sant’anna, 2003. Cylindrospermopsis raciborskii (Woloszynska) Seenayya & Subba Raju (Cyanobacteria): variação semanal e relações com fatores ambientais em um reservatório eutrófico, São Paulo, SP, Brasil. Revista Brasileira Botanica 26: 97–112.Google Scholar
  78. UNESCO, 1973. A guide to the measurement of marine primary production under some special conditions. Monogr. Oceanogr. Method. 3. UNESCO, Paris. 73 p.Google Scholar
  79. Vico, P., L. Aubriot, F. Martigani, N. Rigamonti, S. Bonilla & C. Piccini, 2016. Influence of nitrogen availability on the expression of genes involved in the biosynthesis of saxitoxin and analogs in Cylindrospermopsis raciborskii. Harmful Algae 56: 37–43.CrossRefPubMedGoogle Scholar
  80. Vidal, L. & C. Kruk, 2008. Cylindrospermopsis raciborskii (Cyanobacteria) extends its distribution to Latitude 34 53′S: taxonomical and ecological features in Uruguayan eutrophic lakes. Pan-American Journal of Aquatic Sciences 3: 142–151.Google Scholar
  81. Wiese, M., P. M. D’Agostino, T. K. Mihali, M. Moffitt & B. A. Neilan, 2010. Neurotoxic Alkaloids: Saxitoxin and Its Analogs. Marine Drugs 8: 2185–2211.CrossRefPubMedPubMedCentralGoogle Scholar
  82. Willis, A., A. W. Chuang, J. N. Woodhouse, B. A. Neilan & M. A. Burford, 2016. Intraspecific variation in growth, morphology and toxin quotas for the cyanobacterium, Cylindrospermopsis raciborskii. Toxicon 119: 307–310.CrossRefPubMedGoogle Scholar
  83. Wojciechowski, J., L. F. Fernandes & F. V. B. Fonseca, 2016. Morpho-physiological responses of a subtropical strain of Cylindrospermopsis raciborskii (Cyanobacteria) to different light intensities. Acta Botanica Brasilica 30: 232–233.CrossRefGoogle Scholar
  84. Wu, Z., J. Shi & R. Li, 2009. Comparative studies on photosynthesis and phosphate metabolism of Cylindrospermopsis raciborskii with Microcystis aeruginosa and Aphanizomenonflos-aquae. Harmful Algae 8: 910–915.CrossRefGoogle Scholar
  85. Yunes, J. S., N. T. Cunha, L. P. Barros, L. A. O. Proença & J. M. Monserrat, 2003. Cyanobacterial Neurotoxins from Southern Brazilian freshwaters. Comments on Toxicology 9: 103–115.CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2017

Authors and Affiliations

  • Maria Cecília Miotto
    • 1
  • Luiza Dy Fonseca Costa
    • 2
  • Débora Monteiro Brentano
    • 3
  • Camila Nader
    • 1
  • Luana dos Santos Souza
    • 1
  • Pablo Diego Gressler
    • 1
  • Roselane Laudares-Silva
    • 1
  • João Sarkis Yunes
    • 2
  • José Bonomi Barufi
    • 1
  • Leonardo Rubi Rörig
    • 1
  1. 1.Laboratory of Phycology, Department of BotanyFederal University of Santa Catarina (UFSC)FlorianópolisBrazil
  2. 2.Laboratory of Cyanobacteria and Phycotoxins, Institute of OceanographyFederal University of Rio Grande (FURG)Rio GrandeBrazil
  3. 3.Laboratory of Ecotoxicology, Federal Institute of EducationScience and Technology of Santa Catarina (IFSC)FlorianópolisBrazil

Personalised recommendations