Skip to main content
SpringerLink
Log in

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

  • Published:
Ecotoxicology Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Babica P, Blaha L, Marsalek B (2006) Exploring the natural role of microcystins—a review of effects on photoautotrophic organisms. J Phycol 42:9–20

    Article  Google Scholar 

  • 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):3839–3848

    Article  CAS  Google Scholar 

  • 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):3337–3348

    Article  CAS  Google Scholar 

  • 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):e29981

    Article  CAS  Google Scholar 

  • 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):1394–1407

    Article  CAS  Google Scholar 

  • 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 8:715–725

    Article  CAS  Google Scholar 

  • 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 61:149–162

    Article  Google Scholar 

  • 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):151–163

    Article  Google Scholar 

  • 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):579–587

    Article  Google Scholar 

  • Dziallas C, Grossart H-P (2011) Increasing oxygen radicals and water temperature select for toxic Microcystis sp. PLoS One 6(9):e25569

    Article  CAS  Google Scholar 

  • Figueredo CC, Giani A, Bird DF (2007) Does allelopathy contribute to Cylindrospermopsis raciborskii (cyanobacteria) bloom occurrence and geographic expansion? J Phycol 43:256–265

    Article  Google Scholar 

  • Fujii M, Rose AL, Waite TD (2011) Iron uptake by toxic and nontoxic strains of Microcystis aeruginosa. Appl Environ Microbiol 77(19):7068–7071

    Article  CAS  Google Scholar 

  • 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):15–25

    Article  CAS  Google Scholar 

  • Ishida K, Murakami M (2000) Kasumigamide, an antialgal peptide from the cyanobacterium Microcystis aeruginosa. J Org Chem 65:5898–5900

    Article  CAS  Google Scholar 

  • 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):188–193

    Article  Google Scholar 

  • 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 48:1–12

    Article  Google Scholar 

  • 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):2939–2946

    Article  Google Scholar 

  • 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):6723–6730

    Article  CAS  Google Scholar 

  • Leão PN, Vasconcelos MT, Vasconcelos VM (2009) Allelopathy in freshwater cyanobacteria. Crit Rev Microbiol 35(4):271–282

    Article  Google Scholar 

  • 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):7016–7022

    Article  Google Scholar 

  • 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 14:313–334

    Article  Google Scholar 

  • Ray S, Bagchi SN (2001) Nutrients and pH regulate algicide accumulation in cultures of the cyanobacterium Oscillatoria laetevirens. New Phytol 149(3):455–460

    Article  CAS  Google Scholar 

  • 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):665–673

    Article  CAS  Google Scholar 

  • 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 11:1–61

    Google Scholar 

  • 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):4750–4759

    Article  CAS  Google Scholar 

  • 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):798–805

    Article  CAS  Google Scholar 

  • Sedmak B, Elersek T (2005) Microcystins induce morphological and physiological changes in selected representative phytoplanktons. Microb Ecol 50(2):298–305

    Article  CAS  Google Scholar 

  • 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):753–764

    Article  CAS  Google Scholar 

  • 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):1438–1450

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Watanabe MF, Harada K-I, Carmichael WW, Fujiki H (eds) (1996) Toxic Microcystis. CRC Press, Boca Raton

    Google Scholar 

  • 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 150:1785–1796

    Article  CAS  Google Scholar 

  • 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):609–619

    Article  CAS  Google Scholar 

  • 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):400–406

    Article  CAS  Google Scholar 

  • 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):7386–7389

    Article  CAS  Google Scholar 

  • Wilson AE, Kaul RB, Sarnelle O (2010) Growth rate consequences of coloniality in a harmful phytoplankter. PLoS One 5(1):e8679

    Article  Google Scholar 

  • 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 266:49–53

    Article  CAS  Google Scholar 

  • 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):407–415

    Article  CAS  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

  1. Department of Ecology and Key Laboratory of Eutrophication and Red Tide Prevention of Guangdong Higher Education Institutes, Jinan University, Guangzhou, 510632, China

    Lamei Lei, Chunlian Li, Liang Peng & Bo-Ping Han

Authors
  1. Lamei Lei
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chunlian Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Liang Peng
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Bo-Ping Han
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Lamei Lei or Bo-Ping Han.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lei, L., Li, C., Peng, L. et al. Competition between toxic and non-toxic Microcystis aeruginosa and its ecological implication. Ecotoxicology 24, 1411–1418 (2015). https://doi.org/10.1007/s10646-015-1456-2

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-015-1456-2

Keywords

Search

Navigation