Microbial Ecology

, Volume 66, Issue 3, pp 479–488 | Cite as

Light and Phosphate Competition Between Cylindrospermopsis raciborskii and Microcystis aeruginosa is Strain Dependent

  • Marcelo Manzi Marinho
  • Maria Betânia Gonçalves Souza
  • Miquel Lürling
Microbiology of Aquatic Systems


The hypothesis that outcomes of phosphorus and light competition between Cylindrospermopsis raciborskii and Microcystis aeruginosa are strain dependent was tested experimentally. Critical requirements of phosphorus (P*) and of light (I*) of two strains of each species were determined through monoculture experiments, which indicated a trade-off between species and also between Microcystis strains. Competition experiments between species were performed using the weakest predicted competitors (with the highest values of P* and of I*) and with the strongest predicted competitors (with the lowest values of P* and of I*). Under light limitation, competition between the weakest competitors led C. raciborskii to dominate. Between the strongest competitors, the opposite was observed, M. aeruginosa displaced C. raciborskii, but both strains co-existed in equilibrium. Under phosphate limitation, competition between the weakest competitors led C. raciborskii to exclude M. aeruginosa, and between the strongest competitors, the opposite was observed, M. aeruginosa displaced C. raciborskii, but the system did not reach an equilibrium and both strains were washed out. Hence, outcomes of the competition depended on the pair of competing strains and not only on species or on type of limitation. We concluded that existence of different trade-offs among strains and between species underlie our results showing that C. raciborskii can either dominate or be displaced by M. aeruginosa when exposed to different conditions of light or phosphate limitation.



We thank W. Beekman-Lukassen, F. Gillissen, I. Paredes, N. Noyma, and J. Beijer for assistance with the experiments. M.B.G.S. PhD scholarship (BEX2834/04-9) and M.M.M. Post-Doc fellowship (BEX1988/08-5) were funded by the Federal Government of Brazil, Ministry of Education, through CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior, Ministério da Educação). This study was conducted under the flag of the CAPES (Brazil)/Wageningen University (The Netherlands) CAPES-WUR project 004/2008.


  1. 1.
    Ahn C, Chung A (2002) Diel rhythm of algal phosphate uptake rates in P–limited cyclostats and simulation of its effect on growth and competition. J Phycol 704:695–704CrossRefGoogle Scholar
  2. 2.
    Armstrong RA, McGehee R (1980) Competitive exclusion. Am Nat 115(2):151–170CrossRefGoogle Scholar
  3. 3.
    Bittencourt-Oliveira MC, Oliveira MC, Bolch CJS (2001) Genetic variability of Brazilian strains of the Microcystis aeruginosa complex (Cyanobacteria /Cyanophyceae) using the phycocyanin intergenic spacer and flanking regions (cpcBA). J Phycol 37:810–818CrossRefGoogle Scholar
  4. 4.
    Bolch CJ, Blackburn SI, Jones GJ, Orr PT, Grewe PM (1997) Plasmid content and distribution in Australian isolates of Microcystis Kützing ex Lemmermann (Cyanobacteria: Chroococcales). Phycologia 36:6–11CrossRefGoogle Scholar
  5. 5.
    Bonilla S, Aubriot L, Soares MCS et al (2011) What drives the distribution of the bloom forming cyanobacteria Planktothrix agardhii and Cylindrospermopsis raciborskii? FEMS Microbiol Ecol 79:594–607. doi:10.1111/j.1574-6941.2011.01242.x CrossRefPubMedGoogle Scholar
  6. 6.
    Bouvy M, Falcão D, Marinho M, Pagano M, Moura A (2000) Occurrence of Cylindrospermopsis (Cyanobacteria) in 39 Brazilian tropical reservoirs during the 1998 drought. Aquat Microb Ecol 23:13–27CrossRefGoogle Scholar
  7. 7.
    Briand E, Yéprémian C, Humbert J-F, Quiblier C (2008) Competition between microcystin- and non-microcystin-producing Planktothrix agardhii (Cyanobacteria) strains under different environmental conditions. Environ Microbiol 10(12):3337–3348. doi:10.1111/j.1462-2920.2008.01730.x CrossRefPubMedGoogle Scholar
  8. 8.
    Briand J-F, Leboulanger C, Humbert J-F et al (2004) Cylindrospermopsis raciborskii (Cyanobacteria) invasion at mid-latitudes: selection, wide physiological tolerance, or global warming? J Phycol 40(2):231–238. doi:10.1111/j.1529-8817.2004.03118.x CrossRefGoogle Scholar
  9. 9.
    Butler GJ, Wolkowicz GSK (1987) Exploitative competition in a chemostat for two complementary, and possibly inhibitory, resources. Math Biosci 48:1–48CrossRefGoogle Scholar
  10. 10.
    Chonudomkul D, Yongmanitchai W, Theeragool G et al (2004) Morphology, genetic diversity, temperature tolerance and toxicity of Cylindrospermopsis raciborskii (Nostocales, Cyanobacteria) strains from Thailand and Japan. FEMS Microbiol Ecol 48(3):345–355. doi:10.1016/j.femsec.2004.02.014 CrossRefPubMedGoogle Scholar
  11. 11.
    Coles JF, Jones R (2000) Effect of temperature on photosynthesis-light response and growth of four phytoplankton species isolated from a tidal freshwater river. J Phycol 16:7–16. doi:10.1046/j.1529-8817.2000.98219.x CrossRefGoogle Scholar
  12. 12.
    Ducobu H (1998) The ecophysiology of a prochlorophyte and a cyanobacterium with emphasis on phosphorus metabolism. Dissertation, University of Amsterdam. http://dare.uva.nl/pt/record/156924
  13. 13.
    Ducobu H, Huisman J, Jonker R (1998) Competition between a prochlorophyte and a cyanobacterium under various phosphorus regimes: comparison with the Droop model. J Phycol 34:467–476. doi:10.1046/j.1529-8817.1998.340467.x CrossRefGoogle Scholar
  14. 14.
    Everson S, Fabbro L, Kinnear S, Wright P (2011) Extreme differences in akinete, heterocyte and cylindrospermopsin concentrations with depth in a successive bloom involving Aphanizomenon ovalisporum (Forti) and Cylindrospermopsis raciborskii (Woloszynska) Seenaya and Subba Raju. Harmful Algae 10(3):265–276. doi:10.1016/j.hal.2010.10.006 CrossRefGoogle Scholar
  15. 15.
    Falkner G, Wagner F, Falkner R (1996) The bioenergetic coordination of a complex biological system is revealed by its adaptation to changing environmental conditions. Acta Biotheor 44:283–299CrossRefGoogle Scholar
  16. 16.
    Figueredo CC, Giani A (2009) Phytoplankton community in the tropical lake of Lagoa Santa (Brazil): conditions favoring a persistent bloom of Cylindrospermopsis raciborskii. Limnologica 39(4):264–272. doi:10.1016/j.limno.2009.06.009 CrossRefGoogle Scholar
  17. 17.
    Figueredo CC, Giani A, Bird DF (2007) Does allelopathy contribute to Cylindrospermopsis raciborskii (Cyanobacteria) bloom occurrence and geographic expansion? J Phycol 43(2):256–265. doi:10.1111/j.1529-8817.2007.00333.x CrossRefGoogle Scholar
  18. 18.
    Flöder S, Jaschinski S, Wells G, Burns CW (2010) Dominance and compensatory growth in phytoplankton communities under salinity stress. J Exp Mar Biol Ecol 395:223–231. doi:10.1016/j.jembe.2010.09.006 CrossRefGoogle Scholar
  19. 19.
    Gantar M, Berry JP, Thomas S et al (2008) Allelopathic activity among Cyanobacteria and microalgae isolated from Florida freshwater habitats. FEMS Microbiol Ecol 64(1):55–64. doi:10.1111/j.1574-6941.2008.00439.x PubMedCentralCrossRefPubMedGoogle Scholar
  20. 20.
    Grossman A, Schaefer M, Chiang G (1994) The responses of cyanobacteria to environmental conditions: light and nutrients. In: Bryant D (ed) The Molecular Biology of Cyanobacteria. Kluwer Acad Publ, Amsterdam, pp 641–675CrossRefGoogle Scholar
  21. 21.
    Gugger M, Molica R, Berre BL (2005) Genetic diversity of Cylindrospermopsis strains (Cyanobacteria) isolated from four continents. Appl Environ Microbiol. doi:10.1128/AEM.71.2.1097-1100.2005 PubMedGoogle Scholar
  22. 22.
    Hamilton PB, Ley LM, Dean S, Pick FR (2005) The occurrence of the cyanobacterium Cylindrospermopsis raciborskii in Constance Lake: an exotic cyanoprokaryote new to Canada. Phycologia 44:17–25CrossRefGoogle Scholar
  23. 23.
    Hoeger SJ, Shaw G, Hitzfeld BC, Dietrich DR (2004) Occurrence and elimination of cyanobacterial toxins in two Australian drinking water treatment plants. Toxicon 43(6):639–649. doi:10.1016/j.toxicon.2004.02.019 CrossRefPubMedGoogle Scholar
  24. 24.
    Huisman J, Oostveen PV, Weissing FJ (1999) Species dynamics in phytoplankton blooms: incomplete mixing and competition for light. Am Nat 154(1):46–48CrossRefGoogle Scholar
  25. 25.
    Huisman J, Weissing FJ (1994) Light-limited growth and competition for light in well-mixed aquatic environments: an elementary model. Ecology 75:507–520CrossRefGoogle Scholar
  26. 26.
    Huszar VLM, Silva LHS (1999) Cinco décadas de estudos sobre a ecologia do fitoplâncton no Brasil. Limnotemas 2:1–22Google Scholar
  27. 27.
    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 43:257–275. doi:10.1046/j.1365-2427.2000.00549.x CrossRefGoogle Scholar
  28. 28.
    Janse I, Kardinaal WEA, Meima M et al (2004) Toxic and nontoxic Microcystis colonies in natural populations can be differentiated on the basis of rRNA gene internal transcribed spacer diversity. Appl Environ Microbiol 70:3979–3987PubMedCentralCrossRefPubMedGoogle Scholar
  29. 29.
    Kardinaal WEA, Janse I, Agterveld MK et al (2007) Microcystis genotype succession in relation to microcystin concentrations in freshwater lakes. Aquat Microb Ecol 48:1–12. doi:10.3354/ame048001 CrossRefGoogle Scholar
  30. 30.
    Kato T, Watanabe MF, Watanabe M (1991) Allozyme divergence in Microcystis (Cyanophyceae) and its taxonomic inference. Algol Stud 64:129–140Google Scholar
  31. 31.
    Kenesi G, Shafik HM, Kovács AW, Herodek S, Présing M (2009) Effect of nitrogen forms on growth, cell composition and N2 fixation of Cylindrospermopsis raciborskii in phosphorus-limited chemostat cultures. Hydrobiology 623(1):191–202. doi:10.1007/s10750-008-9657-9 CrossRefGoogle Scholar
  32. 32.
    Klausmeier CA (2001) Algal games: the vertical distribution of phytoplankton in poorly mixed water columns. Limnol Oceanogr 46(8):1998–2007CrossRefGoogle Scholar
  33. 33.
    Leibold MA (1997) Do nutrient-competition models predict nutrient availabilities in limnetic ecosystems? Oecologia 110(1):132–142CrossRefGoogle Scholar
  34. 34.
    Litchman E (2003) Competition and coexistence of phytoplankton under fluctuating light: experiments with two cyanobacteria. Aquat Microb Ecol 31:241–248CrossRefGoogle Scholar
  35. 35.
    Litchman E, Klausmeier CA, Schofield OM, Falkowski PG (2007) The role of functional traits and trade-offs in structuring phytoplankton communities: scaling from cellular to ecosystem level. Ecol Lett 10(12):1170–1181. doi:10.1111/j.1461-0248.2007.01117.x CrossRefPubMedGoogle Scholar
  36. 36.
    Lund JWH, Kipling C, Lecren ED (1958) The inverted microscope method of estimating algal number and statistical basis of estimating by counting. Hydrobiology 11:143–170CrossRefGoogle Scholar
  37. 37.
    Lürling M, Beekman W (2006) Palmelloids formation in Chlamydomonas reinhardtii: defence against rotifer predators? Ann Limnol- Int J Lim 42:65–72. doi:10.1051/limn/2006010 CrossRefGoogle Scholar
  38. 38.
    Lürling M, Faassen EJ (2012) Controlling toxic cyanobacteria: effects of dredging and phosphorus-binding clay on cyanobacteria and microcystins. Water Res 46(5):1447–1459. doi:10.1016/j.watres.2011.11.008 CrossRefPubMedGoogle Scholar
  39. 39.
    Lyck S, Christoffersen K (2003) Microcystin quota, cell division and microcystin net production of precultured Microcystis aeruginosa CYA 228 (Chroococcales, Cyanophyceae) under field conditions. Phycologia 42:667–674CrossRefGoogle Scholar
  40. 40.
    Marinho MM, Azevedo SMF (2007) Influence of N/P ratio on competitive abilities for nitrogen and phosphorus by Microcystis aeruginosa and Aulacoseira distans. Aquat Ecol 41(4):525–533. doi:10.1007/s10452-007-9118-y CrossRefGoogle Scholar
  41. 41.
    Marinho MM, Huszar VL (2002) Nutrient availability and physical conditions as controlling factors of phytoplankton composition and biomass in a tropical reservoir (Southeastern Brazil). Arch Hydrobiol 153(3):443–468Google Scholar
  42. 42.
    Moisander PH, Ochiai M, Lincoff A (2009) Nutrient limitation of Microcystis aeruginosa in northern California Klamath River reservoirs. Harmful Algae 8(6):889–897. doi:10.1016/j.hal.2009.04.005 CrossRefGoogle Scholar
  43. 43.
    Molica RJR, Oliveira EJA, Carvalho PVVC et al (2005) Occurrence of saxitoxins and an anatoxin-a(s)-like anticholinesterase in a Brazilian drinking water supply. Harmful Algae 4(4):743–753. doi:10.1016/j.hal.2004.11.001 CrossRefGoogle Scholar
  44. 44.
    Nixdorf B, Mischke U, Rücker J (2003) Phytoplankton assemblages and steady state in deep and shallow eutrophic lakes—an approach to differentiate the habitat properties of Oscillatoriales. Hydrobiology 502(172):111–121CrossRefGoogle Scholar
  45. 45.
    Oberhaus L, Briand J-F, Humbert J-F (2008) Allelopathic growth inhibition by the toxic, bloom-forming cyanobacterium Planktothrix rubescens. FEMS Microbiol Ecol 66(2):243–249. doi:10.1111/j.1574-6941.2008.00567.x CrossRefPubMedGoogle Scholar
  46. 46.
    Padisák J, Reynolds CS (1998) Selection of phytoplankton associations in Lake Balaton, Hungary, in response to eutrophication and restoration measures, with special reference to the cyanoprokaryotes. Hydrobiology 384:41–53CrossRefGoogle Scholar
  47. 47.
    Padisák J (1997) Cylindrospermopsis raciborskii (Woloszynska) Seenayya et Subba Raju, an expanding, highly adaptive cyanobacterium: worldwide distribution and review of its ecology. Arch Hydrobiol/Supplement 107:563–593Google Scholar
  48. 48.
    Paerl HW, Hall NS, Calandrino ES (2011) Controlling harmful cyanobacterial blooms in a world experiencing anthropogenic and climatic-induced change. Sci Total Environ 409(10):1739–1745. doi:10.1016/j.scitotenv.2011.02.001 CrossRefPubMedGoogle Scholar
  49. 49.
    Paerl HW, Tucker J, Bland PT (1983) Carotenoid enhancement and its role in maintaining blue-green algal (Microcystis aeruginosa) surface blooms. Limnol Oceanogr 28:847–857CrossRefGoogle Scholar
  50. 50.
    Passarge J, Hol S, Escher M, Huisman J (2006) Competition for nutrients and light: stable coexistence, alternative stable states, or competitive exclusion? Ecol Monogr 76(1):57–72CrossRefGoogle Scholar
  51. 51.
    Piccini C, Aubriot L, Fabre A et al (2011) Genetic and eco-physiological differences of South American Cylindrospermopsis raciborskii isolates support the hypothesis of multiple ecotypes. Harmful Algae 10:644–653. doi:10.1016/j.hal.2011.04.016 CrossRefGoogle Scholar
  52. 52.
    Raps S, Wyman K, Siegelman HW, Falkowski PG (1983) Adaptation of the Cyanobacterium Microcystis aeruginosa to light intensity. Plant Physiol 72(3):829–832PubMedCentralCrossRefPubMedGoogle Scholar
  53. 53.
    Repka S, Mehtonen J, Vaitomaa J, Saari L, Sivonen K (2001) Effects of nutrients on growth and nodularin production of Nodularia strain GR8b. Microbial Ecol 42(4):606–613. doi:10.1007/s00248-001-0026-8 CrossRefGoogle Scholar
  54. 54.
    Reynolds CS (2006) Ecology of phytoplankton. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  55. 55.
    Rhee GY (1973) A continuous culture study of phosphate uptake, growth rate and polyphosphate in Scenedesmus sp. J Phycol 9:495–506Google Scholar
  56. 56.
    Rivkin RB, Swift E (1982) Phosphate uptake by the oceanic dinoflagellate Pyrocystis noctiluca. J Phycol 18:113–120. doi:10.1111/j.1529-8817.1982.tb03164.x CrossRefGoogle Scholar
  57. 57.
    Robarts RB, Zohary T (1992) The influence of temperature and light on the upper limit of Microcystis aeruginosa production in a hypertrophic reservoir. J Plankton Res 14(2):235–247CrossRefGoogle Scholar
  58. 58.
    Schwarz R, Forchhammer K (2005) Acclimation of unicellular cyanobacteria to macronutrient deficiency: emergence of a complex network of cellular responses. Microbiology 151:2503–2514. doi:10.1099/mic.0.27883-0 CrossRefPubMedGoogle Scholar
  59. 59.
    Shen H, Song L (2007) Comparative studies on physiological responses to phosphorus in two phenotypes of bloom-forming Microcystis. Hydrobiology 592(1):475–486. doi:10.1007/s10750-007-0794-3 CrossRefGoogle Scholar
  60. 60.
    Smayda T (1997) Harmful algal blooms: their ecophysiology and general relevance to phytoplankton blooms in the sea. Limnol Oceanogr 42(5):1137–1153CrossRefGoogle Scholar
  61. 61.
    Soares MC, Rocha MIA, Marinho MM, Azevedo SMFO, Branco CWC, Huszar VLM (2009) Changes in species composition during annual cyanobacterial dominance in a tropical reservoir: physical factors, nutrients and grazing effects. Aquat Microb Ecol 57:137–149. doi:10.3354/ame01336 CrossRefGoogle Scholar
  62. 62.
    Sommer U (1989) The role of competition for resources in phytoplankton succession. In: Sommer U (ed) Plankton ecology: succession in plankton communities. Springer-Verlag, Berlin, pp 57–106CrossRefGoogle Scholar
  63. 63.
    Stewart FM, Levin BR (1973) Partitioning of resources and the outcome of interspecific competition: a model and some general considerations. Am Nat 107:171–198CrossRefGoogle Scholar
  64. 64.
    Stüken A, Rücker J, Endrulat T et al (2006) Distribution of three alien cyanobacterial species (Nostocales) in northeast Germany: Cylindrospermopsis raciborskii, Anabaena bergii and Aphanizomenon aphanizomenoides. Phycologia 45(6):696–703. doi:10.2216/05-58.1 CrossRefGoogle Scholar
  65. 65.
    Tilman D (1982) Resource competition and community structure. Princeton University Press Princeton, NJGoogle Scholar
  66. 66.
    Tomioka N, Imai A, Komatsu K (2011) Effect of light availability on Microcystis aeruginosa blooms in shallow hypereutrophic Lake Kasumigaura. J Plankton Res 33(8):1263–1273. doi:10.1093/plankt/fbr020 CrossRefGoogle Scholar
  67. 67.
    Tucci A, Sant’Anna CL (2003) Cylindrospermopsis raciborskii ( Woloszynska ) Seenayya &Subba Raju (Cyanobacteria): variação semanal e relações com fatores ambientais em um reservatório eutrófico, São Paulo, SP, Brasil. Rev Bras Bot 2:97–112Google Scholar
  68. 68.
    Van de Waal DB, Verspagen JM, Finke JF et al (2011) Reversal in competitive dominance of a toxic versus non-toxic cyanobacterium in response to rising CO2. ISME J 5(9):1438–1450. doi:10.1038/ismej.2011.28 PubMedCentralCrossRefPubMedGoogle Scholar
  69. 69.
    Vézie C, Rapala J, Vaitomaa J, Seitsonen J, Sivonen K (2002) Effect of nitrogen and phosphorus on growth of toxic and nontoxic Microcystis strains and on intracellular microcystin concentrations. Microb Ecol 43:443–454. doi:10.1007/s00248-001-0041-9 CrossRefPubMedGoogle Scholar
  70. 70.
    Via-Ordorika L, Fastner J, Kurmayer R et al (2004) Distribution of microcystin producing and non-microcystin-producing Microcystis sp. in European freshwater bodies: detection of microcystins and microcystin genes in individual colonies. Syst Appl Microbiol 27:592–602CrossRefPubMedGoogle Scholar
  71. 71.
    Vidal L, Kruk C (2008) Cylindrospermopsis raciborskii (Cyanobacteria) extends its distribution to Latitude 34°53′S: taxonomical and ecological features in Uruguayan eutrophic lakes. Panama J Aquat Sci 3(2):142–151Google Scholar
  72. 72.
    Wilson AE, Sarnelle O, Neilan BA, Tim P, Gehringer MM, Hay ME (2005) Genetic variation of the bloom-forming cyanobacterium Microcystis aeruginosa within and among Lakes: implications for Harmful Algal Blooms. App Environ Microbiol 71:6126–6133. doi:10.1128/AEM.71.10.6126 CrossRefGoogle Scholar
  73. 73.
    Wilson AE, Wilson WA, Hay ME (2006) Intraspecific variation in growth and morphology of the bloom-forming cyanobacterium Microcystis aeruginosa. App Environ Microbiol 72(11):7386–7389. doi:10.1128/AEM.00834-06 CrossRefGoogle Scholar
  74. 74.
    Yoshida M, Yoshida T, Takashima Y, Kondo R, Hiroishi S (2005) Genetic diversity of the toxic cyanobacterium Microcystis in Lake Mikata. Environ Toxicol 20(3):229–234. doi:10.1002/tox.20102 CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Marcelo Manzi Marinho
    • 1
  • Maria Betânia Gonçalves Souza
    • 2
  • Miquel Lürling
    • 2
    • 3
  1. 1.Laboratório de Ecologia e Fisiologia do Fitoplâncton, Departamento de Biologia VegetalUniversidade do Estado do Rio de JaneiroRio de JaneiroBrazil
  2. 2.Aquatic Ecology and Water Quality Management Group, Department of Environmental SciencesWageningen UniversityWageningenThe Netherlands
  3. 3.Department Aquatic EcologyNetherlands Institute for Ecology (NIOO-KNAW)WageningenThe Netherlands

Personalised recommendations