Advertisement

Ecotoxicology

, Volume 24, Issue 7–8, pp 1411–1418 | Cite as

Competition between toxic and non-toxic Microcystis aeruginosa and its ecological implication

  • Lamei LeiEmail author
  • Chunlian Li
  • Liang Peng
  • Bo-Ping HanEmail author
Article

Abstract

The frequency of toxic cyanobacterial blooms has increased in recent decades, but the factors that regulate the dominance of toxin-producing cyanobacteria over non-toxin-producing strains of one species are still obscure. This study examined the effects of temperature, light intensity, nitrate and phosphate on the dominance of MC-producing and non-MC-producing strains of Microcystis aeruginosa in monoculture and co-culture experiments. In the monoculture experiments, growth rates of the non-MC-producing strain were higher than those of the MC-producing strain under the same growth conditions. However, at the end of the co-culture experiments, the MC-producing strain became surprisingly dominant in all treatments except when treated with extreme low phosphate concentrations. Higher temperatures and nutrient levels can shift the dominance more quickly towards the toxic strain. The dominance may be explained by allelopathic interactions through allelochemicals and other secondary metabolites, but not MC. Environmental factors such as extremely low phosphate content may exert an indirect effect on strain dominance by changing the production of allelochemicals. Our findings highlight the complications in predicting competitive outcome for cyanobacterial strains in natural environments.

Keywords

Microcystis Microcystin Competition Dominance Environmental factors 

Notes

Acknowledgments

This research was supported by the Grant (No. 31070416) from National Science Foundation of China (NSFC), and the Grant from Guangdong Province for leading talent scientists to Dr Henri Dumont. We thank Leanne A Pearson and other colleagues in University of New South Wales, Australia for commenting and correcting the manuscript.

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Babica P, Blaha L, Marsalek B (2006) Exploring the natural role of microcystins—a review of effects on photoautotrophic organisms. J Phycol 42:9–20CrossRefGoogle Scholar
  2. Briand E, Gugger M, François JC, Bernard C, Humbert JF, Quiblier C (2008a) Temporal variations in the dynamics of potentially microcystin-producing strains in a bloom-forming Planktothrix agardhii (cyanobacterium) population. Appl Environ Microbiol 74(12):3839–3848CrossRefGoogle Scholar
  3. Briand E, Yéprémian C, Humbert JF, Quiblier C (2008b) Competition between microcystin- and non-microcystin-producing Planktothrix agardhii (cyanobacteria) strains under different environmental conditions. Environ Microbiol 10(12):3337–3348CrossRefGoogle Scholar
  4. Briand E, Bormans M, Quiblier C, Salençon MJ, Humbert JF (2012) Evidence of the cost of the production of microcystins by Microcystis aeruginosa under differing light and nitrate environmental conditions. PLoS One 7(1):e29981CrossRefGoogle Scholar
  5. Carey CC, Ibelings BW, Hoffmann EP, Hamilton DP, Brookes JD (2012) Eco-physiological adaptations that favour freshwater cyanobacteria in a changing climate. Water Res 46(5):1394–1407CrossRefGoogle Scholar
  6. Davis TW, Berry DL, Boyer GL, Gobler CJ (2009) The effects of temperature and nutrients on the growth and dynamics of toxic and non-toxic strains of Microcystis during cyanobacteria blooms. Harmful Algae 8:715–725CrossRefGoogle Scholar
  7. Davis TW, Harke MJ, Marcoval MA, Goleski J, Orano-Dawson C, Berry DL, Gobler CJ (2010) Effects of nitrogenous compounds and phosphorus on the growth of toxic and non-toxic strains of Microcystis during cyanobacterial blooms. Aquat Microb Ecol 61:149–162CrossRefGoogle Scholar
  8. de Figueiredo DR, Azeiteiro UM, Esteves SM, Gonçalves FJ, Pereira MJ (2004) Microcystin-producing blooms—a serious global public health issue. Ecotoxicol Environ Saf 59(2):151–163CrossRefGoogle Scholar
  9. De Nobel WT, Matthijs H, Von Elert E, Mur LR (1998) Comparison of the light-limited growth of the nitrogen-fixing cyanobacteria Anabaena and Aphanizomenon. New Phytol 138(4):579–587CrossRefGoogle Scholar
  10. Dziallas C, Grossart H-P (2011) Increasing oxygen radicals and water temperature select for toxic Microcystis sp. PLoS One 6(9):e25569CrossRefGoogle Scholar
  11. Figueredo CC, Giani A, Bird DF (2007) Does allelopathy contribute to Cylindrospermopsis raciborskii (cyanobacteria) bloom occurrence and geographic expansion? J Phycol 43:256–265CrossRefGoogle Scholar
  12. Fujii M, Rose AL, Waite TD (2011) Iron uptake by toxic and nontoxic strains of Microcystis aeruginosa. Appl Environ Microbiol 77(19):7068–7071CrossRefGoogle Scholar
  13. Haande S, Ballot A, Rohrlack T, Fastner J, Wiedner C, Edvardsen B (2007) Diversity of Microcystis aeruginosa isolates (Chroococcales, Cyanobacteria) from East-African water bodies. Arch Microbiol 188(1):15–25CrossRefGoogle Scholar
  14. Ishida K, Murakami M (2000) Kasumigamide, an antialgal peptide from the cyanobacterium Microcystis aeruginosa. J Org Chem 65:5898–5900CrossRefGoogle Scholar
  15. Joung SH, Oh HM, Ko SR, Ahn CY (2011) Correlations between environmental factors and toxic and non-toxic Microcystis dynamics during bloom in Daechung Reservoir, Korea. Harmful Algae 10(2):188–193CrossRefGoogle Scholar
  16. Kardinaal WEA, Janse I, Kamst-van Agterveld MP, Meima M, Snoek J, Mur LR, Huisman J, Zwart G, Visser PM (2007a) Microcystis genotype succession in relation to microcystin concentrations in freshwater lakes. Aquat Microb Ecol 48:1–12CrossRefGoogle Scholar
  17. Kardinaal WEA, Tonk L, Janse I, Hol S, Slot P, Huisman J, Visser PM (2007b) Competition for light between toxic and nontoxic strains of the harmful cyanobacterium Microcystis. Appl Environ Microbiol 73(9):2939–2946CrossRefGoogle Scholar
  18. Kurmayer R, Kutzenberger T (2003) Application of real-time PCR for quantification of microcystin genotypes in a population of the toxic cyanobacterium Microcystis sp. Appl Environ Microbiol 69(11):6723–6730CrossRefGoogle Scholar
  19. Leão PN, Vasconcelos MT, Vasconcelos VM (2009) Allelopathy in freshwater cyanobacteria. Crit Rev Microbiol 35(4):271–282CrossRefGoogle Scholar
  20. Leblanc Renaud S, Pick FR, Fortin N (2011) Effect of light intensity on the relative dominance of toxigenic and non toxigenic strains of Microcystis aeruginosa. Appl Environ Microbiol 77(19):7016–7022CrossRefGoogle Scholar
  21. O’Neil JM, Davis TW, Burford MA, Gobler CJ (2012) The rise of harmful cyanobacteria blooms: the potential roles of eutrophication and climate change. Harmful Algae 14:313–334CrossRefGoogle Scholar
  22. Ray S, Bagchi SN (2001) Nutrients and pH regulate algicide accumulation in cultures of the cyanobacterium Oscillatoria laetevirens. New Phytol 149(3):455–460CrossRefGoogle Scholar
  23. Rinta-Kanto JM, Konopko EA, DeBruyn JM, Bourbonniere RA, Boyer GL, Wilhelm SW (2009) Lake Erie Microcystis: relationship between microcystin production, dynamics of genotypes and environmental parameters in a large lake. Harmful Algae 8(5):665–673CrossRefGoogle Scholar
  24. Rippka R, Deruelles JB, Waterbury M, Herdman M, Stanier RY (1979) Genetics assignments, strain stories and properties of pure cultures of cyanobacteria. J Gen Appl Microbiol 11:1–61Google Scholar
  25. Sabart M, Pobel D, Briand E, Combourieu B, Salençon MJ, Humbert JF, Latour D (2010) Spatiotemporal variations in microcystin concentrations and in the proportions of microcystin-producing cells in several Microcystis aeruginosa populations. Appl Environ Microbiol 76(14):4750–4759CrossRefGoogle Scholar
  26. Schatz D, Keren Y, Hadas O, Carmeli S, Sukenik A, Kaplan A (2005) Ecological implications of the emergence of non-toxic subcultures from toxic Microcystis strains. Environ Microbiol 7(6):798–805CrossRefGoogle Scholar
  27. Sedmak B, Elersek T (2005) Microcystins induce morphological and physiological changes in selected representative phytoplanktons. Microb Ecol 50(2):298–305CrossRefGoogle Scholar
  28. Tillett D, Dittmann E, Erhard M, von Döhren H, Börner T, Neilan BA (2000) Structural organization of microcystin biosynthesis in Microcystis aeruginosa PCC7806: an integrated peptide-polyketide synthetase system. Chem Biol 7(10):753–764CrossRefGoogle Scholar
  29. Van de Waal DB, Verspagen JM, Finke JF, Vournazou V, Immers AK, Kardinaal WE, Tonk L, Becker S, Van Donk E, Visser PM, Huisman J (2011) Reversal in competitive dominance of a toxic versus non-toxic cyanobacterium in response to rising CO2. ISME J 5(9):1438–1450CrossRefGoogle Scholar
  30. 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 43:443–454CrossRefGoogle Scholar
  31. Watanabe MF, Harada K-I, Carmichael WW, Fujiki H (eds) (1996) Toxic Microcystis. CRC Press, Boca RatonGoogle Scholar
  32. Welker M, Brunke M, Preussel K, Lippert I, von Döhren H (2004) Diversity and distribution of Microcystis (cyanobacteria) oligopeptide chemotypes from natural communities studied by single-colony mass spectrometry. Microbiology 150:1785–1796CrossRefGoogle Scholar
  33. Welker M, Šejnohová L, Némethová D, von Döhren H, Jarkovský J, Maršálek B (2007) Seasonal shifts in chemotype composition of Microcystis sp. communities in the pelagial and the sediment of a shallow reservoir. Limnol Oceanogr 52(2):609–619CrossRefGoogle Scholar
  34. Wiegand C, Peuthert A, Pflugmacher S, Carmeli S (2002) Effects of microcin SF608 and microcystin-LR two cyanobacterial compounds produced by Microcystis sp., on aquatic organisms. Environ Toxicol 17(4):400–406CrossRefGoogle Scholar
  35. Wilson AE, Wilson WA, Hay ME (2006) Intraspecific variation in growth and morphology of the bloom-forming cyanobacterium Microcystis aeruginosa. Appl Environ Microbiol 72(11):7386–7389CrossRefGoogle Scholar
  36. Wilson AE, Kaul RB, Sarnelle O (2010) Growth rate consequences of coloniality in a harmful phytoplankter. PLoS One 5(1):e8679CrossRefGoogle Scholar
  37. Yoshida M, Yoshida T, Takashima Y, Hosoda N, Hiroishi S (2007) Dynamics of microcystin-producing and non-microcystin producing Microcystis populations is correlated with nitrate concentration in a Japanese lake. FEMS Microbiol Lett 266:49–53CrossRefGoogle Scholar
  38. Yoshida M, Yoshida T, Satomi M, Takashima Y, Hosoda N, Hiroishi S (2008) Intra-specific phenotypic and genotypic variation in toxic cyanobacterial Microcystis strains. J Appl Microbiol 105(2):407–415CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  1. 1.Department of Ecology and Key Laboratory of Eutrophication and Red Tide Prevention of Guangdong Higher Education InstitutesJinan UniversityGuangzhouChina

Personalised recommendations