Microbial Ecology

, Volume 64, Issue 3, pp 584–592 | Cite as

Influence of Biotic and Abiotic Factors on the Allelopathic Activity of the Cyanobacterium Cylindrospermopsis raciborskii Strain LEGE 99043

  • Jorge T. Antunes
  • Pedro N. Leão
  • Vítor M. VasconcelosEmail author
Microbiology of Aquatic Systems


Allelopathy is considered to be one of the factors underlying the global expansion of the toxic cyanobacterium Cylindrospermopsis raciborskii. Although the production and release of allelopathic compounds by cyanobacteria is acknowledged to be influenced by environmental parameters, the response of C. raciborskii remains generally unrecognized. Here, the growth and allelopathic potential of C. raciborskii strain LEGE 99043 towards the ubiquitous microalga Ankistrodesmus falcatus were analyzed under different biotic and abiotic conditions. Filtrates from C. raciborskii cultures growing at different cell densities displayed broad inhibitory activity. Moreover, higher temperature, higher light intensity as well phosphate limitation further enhanced this activity. The distinct and comprehensive patterns of inhibition verified during the growth phase, and under the tested parameters, suggest the action of several, still unidentified allelopathic compounds. It is expectable that the observed increase in allelopathic activity can result in distinct ecological advantages to C. raciborskii.


Cell Density High Light Intensity Lower Cell Density Initial Cell Density Cellular Density 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



The authors thank Lúcia Guilhermino for access to the spectrophotometer and Aldo Barreiro for statistical advice. PNL acknowledges a postdoctoral scholarship from Fundação para a Ciência e a Tecnologia (SFRH/BPD/70233/2010).


  1. 1.
    Arar EJ (1997) In vitro determination of Chlorophyll a, b, c1 and c2, and Pheopigments in marine and freshwater phytoplankton by spectrophotometry. EPA, Cincinnati EPA method 446.0)Google Scholar
  2. 2.
    Bar-Yosef Y, Sukenik A, Hadas O, Viner-Mozzini Y, Kaplan A (2010) Enslavement in the water body by toxic Aphanizomenon ovalisporum, inducing alkaline phosphatase in phytoplanktons. Curr Biol 20:1557–1561PubMedCrossRefGoogle Scholar
  3. 3.
    Berger C, Ba N, Gugger M, Bouvy M, Rusconi F, Couté A, Troussellier M, Bernard C (2006) Seasonal dynamics and toxicity of Cylindrospermopsis raciborskii in Lake Guiers (Senegal, West Africa). FEMS Microbiol Ecol 57:355–366PubMedCrossRefGoogle Scholar
  4. 4.
    Bouvy M, Falcão D, Marinho M, Pagano P, Moura A (2001) Occurrence of Cylindrospermopsis (Cyanobacteria) in 39 Brazilian tropical reservoirs during the 1998 drought. Aquat Microb Ecol 23:13–27CrossRefGoogle Scholar
  5. 5.
    Briand JF, Leboulanger C, Humbert JF, Bernard C, Dufor P (2004) Cylindrospermopsis raciborskii (Cyanobacteria) invasion at mid-latitudes: selection, wide physiological tolerance, or global warming? J Phycol 40:231–238CrossRefGoogle Scholar
  6. 6.
    Carneiro RL, dos Santos MEA, Pacheco ABF, Azevedo SMFO (2009) Effects of light intensity and light quality on growth and circadian rhythm of saxitoxins production in Cylindrospermopsis raciborskii (Cyanobacteria). J Plankton Res 31:481–488CrossRefGoogle Scholar
  7. 7.
    Chauhan VS, Marwah JB, Bagchi SN (1992) Effect of an antibiotic from Oscillatoria sp. on phytoplankters, higher plants and mice. New Phytol 120:251–257CrossRefGoogle Scholar
  8. 8.
    Cirés S, Wörmer L, Timón J, Wiedner C, Quesada A (2011) Cylindrospermopsin production and release by the potentially invasive cyanobacterium Aphanizomenon ovalisporum under temperature and light gradients. Harmful Algae 10:668–675CrossRefGoogle Scholar
  9. 9.
    Dyble J, Tester PA, Litaker RW (2006) Effects of light intensity on cylindrospermopsin production in the cyanobacterial HAB species Cylindrospermopsis raciborskii. Afr J Mar Sci 28:309–312CrossRefGoogle Scholar
  10. 10.
    Fabbro LD, Duivenvoorden LJ (1996) Profile of a bloom of the cyanobacterium Cylindrospermopsis raciborskii (Woloszynska) Seenaya and Subba Raju in the Fitzroy River in tropical central Queensland. Mar Freshw Res 47:685–694CrossRefGoogle Scholar
  11. 11.
    Figueredo CC, Giani A, Bird DF (2007) Does allelopathy contribute to Cylindrospermopsis raciborskii blooms occurrence and geographic expansion? J Phycol 43:256–265CrossRefGoogle Scholar
  12. 12.
    Granéli E, Johansson N (2003) Increase in the production of allelopathic substances by Prymnesium parvum cells grown under N- or P-deficient conditions. Harmful Algae 2:135–45CrossRefGoogle Scholar
  13. 13.
    Granéli E, Weberg M, Salomon PS (2008) Harmful algal blooms of allelopathic species: the role of eutrophication. Harmful Algae 8:94–102CrossRefGoogle Scholar
  14. 14.
    Gross EM (2003) Allelopathy of aquatic autotrophs. Crit Rev Plant Sci 22:313–339CrossRefGoogle Scholar
  15. 15.
    Isvánovics V, Shafik HM, Présing M, Juhos S (2000) Growth and phosphate uptake kinetics of the cyanobacterium, Cylindrospermopsis raciborskii (Cyanophyceae) in throughflow cultures. Freshw Biol 43:257–275CrossRefGoogle Scholar
  16. 16.
    Istvánovics V, Somlyody L (2001) Factors influencing lake recovery from eutrophication: the case of basin 1 of Lake Balaton. Water Res 35:729–735PubMedCrossRefGoogle Scholar
  17. 17.
    Johansson N, Granéli E (1999) Influence of different nutrient conditions on cell density, chemical composition and toxicity of Prymnesium parvum (Haptophyta) in semi-continuous cultures. J Exp Mar Biol Ecol 239:243–258CrossRefGoogle Scholar
  18. 18.
    Jonsson PR, Pavia H, Toth G (2009) Formation of harmful algal blooms cannot be explained by allelopathic interactions. Proc Natl Acad Sci USA 106:11177–11182PubMedCrossRefGoogle Scholar
  19. 19.
    Kaebernick M, Neilan BA, Bürner T, Dittmann E (2000) Light and the transcriptional response of the microcystin biosynthesis gene cluster. Appl Environ Microbiol 66:3387–3392PubMedCrossRefGoogle Scholar
  20. 20.
    Kaebernick M, Neilan BA (2001) Ecological and molecular investigations of cyanotoxin production. FEMS Microbiol Ecol 35:1–9PubMedCrossRefGoogle Scholar
  21. 21.
    Kotai J (1972) Instructions for the preparation of modified nutrient solution Z8 for algae. Oslo: Norwegian Institute for Water Research Blindern NIVA B-11/69Google Scholar
  22. 22.
    Krüger T, Hölzel N, Luckas B (2011) Influence of cultivation parameters on growth and microcystin production of Microcystis aeruginosa (Cyanophyceae) isolated from Lake Chao (China). Micro Ecol. doi: 10.1007/s00248-011-9899-3
  23. 23.
    Kurmayer R (2011) The toxic cyanobacterium Nostoc sp. strain 152 produces highest amounts of microcystin and nostophycin under stress conditions. J Phycol 47:200–207PubMedCrossRefGoogle Scholar
  24. 24.
    Leão PN, Vasconcelos MTSD, Vasconcelos VM (2009) Allelopathy in freshwater cyanobacteria. Crit Rev Microbiol 35:271–282PubMedCrossRefGoogle Scholar
  25. 25.
    Leão PN, Vasconcelos MTSD, Vasconcelos VM (2009) Allelopathic activity of cyanobacteria on green microalgae at low cell densities. Eur J Phycol 44:347–355CrossRefGoogle Scholar
  26. 26.
    Legrand C, Rengefors K, Fistarol GO, Granéli E (2003) Allelopathy in phytoplankton—biochemical, ecological and evolutionary aspects. Phycologia 42:406–419CrossRefGoogle Scholar
  27. 27.
    McGregor GB, Fabbro LD (2000) Dominance of Cylindrospermopsis raciborskii (Nostocales, Cyanoprokaryota) in Queensland tropical and subtropical reservoirs: implications for monitoring and management. Lakes Reserv: Res Mgmt 5:195–205CrossRefGoogle Scholar
  28. 28.
    Mogelhoj MK, Hansen PJ, Henriksen P, Lundholm N (2006) High pH and not allelopathy may be responsible for negative effects of Nodularia spumigena on other algae. Aquat Microb Ecol 43:43–54CrossRefGoogle Scholar
  29. 29.
    Moisander PH, Cheshire LA, Braddy J, Calandrino ES, Hoffman M, Piehler MF, Paerl HW (2012) Facultative diazotrophy increases Cylindrospermopsis raciborskii competitiveness under fluctuating nitrogen availability. FEMS Microbiol Ecol 79:800–811PubMedCrossRefGoogle Scholar
  30. 30.
    Nan C, Zhang H, Lin S, Zhao G, Liu X (2008) Allelopathic effects of Ulva lactuca on selected species of harmful bloom-forming microalgae in laboratory cultures. Aquat Bot 89:9–15CrossRefGoogle Scholar
  31. 31.
    Padisák J (1997) Cylindrospermopsis raciborskii (Woloszynska) Seenayya et Subba Raju, an expanding, highly adaptive cyanobacterium: worldwide distribution and review of its ecology. Arch Hydrobiol Suppl 107:563–593Google Scholar
  32. 32.
    Ray S, Bagchi SN (2001) Nutrients and pH regulate algicide accumulation in cultures of the cyanobacterium Oscillatoria laetevirens. New Phytol 149:455–460CrossRefGoogle Scholar
  33. 33.
    Rengefors K, Legrand C (2007) Broad allelopathic activity in Peridinium aciculiferum. Eur J Phycol 42:341–349CrossRefGoogle Scholar
  34. 34.
    Saker ML, Eaglesham GK (1999) The accumulation of cylindrospermopsin from the cyanobacterium Cylindrospermopsis raciborskii in tissues of the Redclaw crayfish Cherax quadricarinatus. Toxicon 37:1065–1077PubMedCrossRefGoogle Scholar
  35. 35.
    Saker ML, Nogueira ICG, Vasconcelos VM, Neilan BA, Eaglesham GK, Pereira P (2003) First report and toxicological assessment of the cyanobacterium Cylindrospermopsis raciborskii from Portuguese freshwaters. Ecotoxicol Environ Saf 55:243–250PubMedCrossRefGoogle Scholar
  36. 36.
    Schatz D, Keren Y, Vardi A, Sukenik A, Carmeli S, Borner T, Dittmann E, Kaplan A (2007) Towards clarification of the biological role of microcystins, a family of cyanobacterial toxins. Environ Microbiol 9:965–970PubMedCrossRefGoogle Scholar
  37. 37.
    Schindler DW (1977) Evolution of phosphorus limitation in lakes. Science 195:260–262PubMedCrossRefGoogle Scholar
  38. 38.
    Schmidt LE, Hansen PJ (2001) Allelopathy in the prymnesiophyte Chrysochromulina polylepis: effect of cell concentration, growth phase and pH. Mar Ecol Prog Ser 216:67–81CrossRefGoogle Scholar
  39. 39.
    Singh S, Kate BN, Banerjee UC (2005) Bioactive compounds from cyanobacteria and microalgae: an overview. Crit Rev Biotechnol 25:73–95PubMedCrossRefGoogle Scholar
  40. 40.
    Suikkanen S, Fistarol GO, Granéli E (2005) Effects of cyanobacterial allelochemicals on a natural plankton community. Mar Ecol Prog Ser 287:1–9CrossRefGoogle Scholar
  41. 41.
    Utermöhl H (1958) Zur Vervollkommung der quantitativen Phytoplankton-Methodik. Mitt Int Ver Limnol 9:1–38Google Scholar
  42. 42.
    von Elert E, Jüttner F (1997) Phosphorus limitation and not light controls the extracellular release of allelopathic compounds by Trichormus doliolum (cyanobacteria). Limnol Oceanogr 42:1796–180CrossRefGoogle Scholar
  43. 43.
    Vrba J, Komarkova J, Vyhnalek V (1993) Enhanced activity of alkaline phosphatases phytoplankton response to epilimnetic phosphorus depletion. Water Sci Technol 28:15–24Google Scholar
  44. 44.
    Wu Z, Shi J, Li R (2009) Comparative studies on photosynthesis and phosphate metabolism of Cylindrospermopsis raciborskii with Microcystis aeruginosa and Aphanizomenon flos-aquae. Harmful Algae 8:910–915CrossRefGoogle Scholar
  45. 45.
    Wu Z, Zeng B, Li R, Song L (2011) Physiological regulation of Cylindrospermopsis raciborskii (Nostocales, Cyanobacteria) in response to inorganic phosphorus limitation. Harmful Algae 15:53–58CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  • Jorge T. Antunes
    • 1
    • 2
  • Pedro N. Leão
    • 1
  • Vítor M. Vasconcelos
    • 1
    • 2
    Email author
  1. 1.CIIMAR/CIMAR, Centro Interdisciplinar de Investigação Marinha e AmbientalUniversidade do PortoPortoPortugal
  2. 2.Departamento de Biologia, Faculdade de CiênciasUniversidade do PortoPortoPortugal

Personalised recommendations