Environmental Science and Pollution Research

, Volume 24, Issue 5, pp 4666–4675 | Cite as

Allelopathic effect boosts Chrysosporum ovalisporum dominance in summer at the expense of Microcystis panniformis in a shallow coastal water body

  • Wei Zhang
  • Erik Jeppesen
  • Mengmeng Wang
  • Xiaoying Xu
  • Liqing Wang
Research Article


The increased occurrence of harmful cyanobacterial species and, with this, higher frequency of cyanobacteria blooms, closely associated with eutrophication and climate change, have attracted increasing attention worldwide. However, competition mechanisms between the different bloom-forming cyanobacteria species remain to be elucidated. In this paper, for the first time, the allelopathic effect of the cyanobacterium Chrysosporum ovalisporum on the cyanobacterium Microcystis panniformis is reported. The results of our study conducted in a Chinese shallow coastal water body demonstrated that the biomass of M. panniformis was relatively low during the C. ovalisporum blooming period. Co-cultivation of a C. ovalisporum strain with a M. panniformis strain showed strong inhibition of the growth of M. panniformis but stimulation of C. ovalisporum. Thus, filtrate of C. ovalisporum culture had a strong inhibitory effect on the performance of M. panniformis by decreasing the maximum optical quantum yield (F v/F m), the electron transport rate (ETR) of PS II and the onset of light saturation (I k) and by increasing the alkaline phosphatase (ALP) activity and superoxide dismutase (SOD) activity of M. panniformis. Our results suggest that the inter-specific allelopathic effect plays an important role in the competition between different cyanobacteria species. We foresee the importance of C. ovalisporum to intensify in a future warmer world, not least in small- to medium-sized, warm and high conductivity coastal water bodies.


Allelopathy Chrysosporum ovalisporum Microcystis panniformis Competition Cylindrospermopsin Bloom 



This work was supported by the “Shanghai outstanding technical leaders plan” (No. 15XD1522900) and Major Projects on Control and Rectification of Water Body Pollution of China (No. 2012ZX07101-007). EJ was supported by managing aquatic ecosystems and water resources under multiple stress (MARS; Contract No. 603378; We would like to thank Dr. Jianming Deng from Nanjing Institute of Geography and Limnology, Chinese Academy of Sciences, for his positive comments. We would also like to express our deep thanks to Anne Mette Poulsen from Aarhus University for her English assistance. The authors are grateful to the two anonymous reviewers for their constructive comments and suggestions.

Supplementary material

11356_2016_8149_MOESM1_ESM.doc (68 kb)
ESM 1 (DOC 67 kb)


  1. Antal O, Karisztl-Gácsi M, Farkas A, Kovács A, Ács A, Törő N, Kiss G, Saker ML, Győri J, Bánfalvi G (2011) Screening the toxic potential of Cylindrospermopsis raciborskii strains isolated from Lake Balaton, Hungary. Toxicon 57(6):831–840CrossRefGoogle Scholar
  2. Banker R, Carmeli S, Hadas O, Teltsch B, Porat R, Sukenik A (1997) Identification of cylindrospermopsin in Aphanizomenon ovalisporum (Cyanophyceae) isolated from Lake Kinneret, Israel. J Phycol 33(4):613–616Google Scholar
  3. 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(17):1557–1561CrossRefGoogle Scholar
  4. Campos A, Araújo P, Pinheiro C, Azevedo J, Osório H, Vasconcelos V (2013) Effects on growth, antioxidant enzyme activity and levels of extracellular proteins in the green alga Chlorella vulgaris exposed to crude cyanobacterial extracts and pure microcystin and cylindrospermopsin. Ecotoxicol Environ Saf 94(5):45–53CrossRefGoogle Scholar
  5. Carey CC, Rengefors K (2010) The cyanobacterium Gloeotrichia echinulata stimulates the growth of other phytoplankton. J Plankton Res 32(9):1349–1354CrossRefGoogle Scholar
  6. Cirés S, Wörmer L, Wiedner C, Quesada A (2013) Temperature-dependent dispersal strategies of Aphanizomenon ovalisporum (Nostocales, Cyanobacteria): implications for the annual life cycle. Microb Ecol 65(1):12–21CrossRefGoogle Scholar
  7. Duval E, Coffinet S, Bernard C, Briand J (2005) Effects of two cyanotoxins, microcystin-LR and cylindrospermopsin, on Euglena gracilis, Environmental Chemistry. Springer, pp. 659–671Google Scholar
  8. Ebina J, Tsutsui T, Shirai T (1983) Simultaneous determination of total nitrogen and total phosphorus in water using peroxodisulfate oxidation. Water Res 17(12):1721–1726CrossRefGoogle Scholar
  9. Fadel A, Atoui A, Lemaire BJ, Vinçon-Leite B, Slim K (2014) Dynamics of the toxin cylindrospermopsin and the cyanobacterium Chrysosporum (Aphanizomenon) ovalisporum in a Mediterranean eutrophic reservoir. Toxins 6(11):3041–3057CrossRefGoogle Scholar
  10. Figueredo CC, Giani A, Bird DF (2007) Does allelopathy contribute to Cylindrospermopsis raciborskii (cyanobacteria) bloom occurrence and geographic expansion ? J Phycol 43(2):256–265CrossRefGoogle Scholar
  11. Harada K-i, Ohtani I, Iwamoto K, Suzuki M, Watanabe MF, Watanabe M, Terao K (1994) Isolation of cylindrospermopsin from a cyanobacterium Umezakia natans and its screening method. Toxicon 32(1):73–84CrossRefGoogle Scholar
  12. Hu H (2006) The freshwater algae of China: systematics, taxonomy and ecology. Science Press, BeijingGoogle Scholar
  13. Huang H, Xiao X, Ghadouani A, Wu J, Nie Z, Peng C, Xu X, Shi J (2015) Effects of natural flavonoids on photosynthetic activity and cell integrity in Microcystis aeruginosa. Toxins 7(1):66–80CrossRefGoogle Scholar
  14. Huang H, Xiao X, Lin F, Grossart H-P, Nie Z, Sun L, Xu C, Shi J (2016) Continuous-release beads of natural allelochemicals for the long-term control of cyanobacterial growth: preparation, release dynamics and inhibitory effects. Water Res 95:113–123CrossRefGoogle Scholar
  15. Huisman J, Sharples J, Stroom JM, Visser PM, Kardinaal WEA, Verspagen JM, Sommeijer B (2004) Changes in turbulent mixing shift competition for light between phytoplankton species. Ecology 85(11):2960–2970CrossRefGoogle Scholar
  16. Jančula D, Maršálek B (2011) Critical review of actually available chemical compounds for prevention and management of cyanobacterial blooms. Chemosphere 85(9):1415–1422CrossRefGoogle Scholar
  17. Juneau P, Harrison P (2005) Comparison by PAM fluorometry of photosynthetic activity of nine marine phytoplankton grown under identical conditions. Photochem Photobiol 81(3):649–653CrossRefGoogle Scholar
  18. Kobayashi K (2004) Factors affecting phytotoxic activity of allelochemicals in soil. Weed Biology and Management 4(1):1–7CrossRefGoogle Scholar
  19. Komárek J, Kováčik L (1989) Trichome structure of four Aphanizomenon taxa (Cyanophyceae) from Czechoslovakia, with notes on the taxonomy and delimitation of the genus. Plant Syst Evol 164(1–4):47–64CrossRefGoogle Scholar
  20. Kosten S, Huszar VL, Bécares E, Costa LS, Donk E, Hansson LA, Jeppesen E, Kruk C, Lacerot G, Mazzeo N (2012) Warmer climates boost cyanobacterial dominance in shallow lakes. Glob Chang Biol 18(1):118–126CrossRefGoogle Scholar
  21. Leflaive J, Ten-Hage L (2007) Algal and cyanobacterial secondary metabolites in freshwaters: a comparison of allelopathic compounds and toxins. Freshw Biol 52(2):199–214CrossRefGoogle Scholar
  22. Legrand C, Rengefors K, Fistarol GO, Graneli E (2003) Allelopathy in phytoplankton-biochemical, ecological and evolutionary aspects. Phycologia 42(4):406–419CrossRefGoogle Scholar
  23. McMinn A, Hegseth E (2004) Quantum yield and photosynthetic parameters of marine microalgae from the southern Arctic Ocean, Svalbard. J Mar Biol Assoc UK 84(05):865–871CrossRefGoogle Scholar
  24. Mello MM, Soares MCS, Roland F, Lürling M (2012) Growth inhibition and colony formation in the cyanobacterium Microcystis aeruginosa induced by the cyanobacterium Cylindrospermopsis raciborskii. Journal of plankton research: 1–8Google Scholar
  25. Paerl HW, Huisman J (2008) Blooms like it hot. Science 320(5872):57–58CrossRefGoogle Scholar
  26. Pinheiro C, Azevedo J, Campos A, Loureiro S, Vasconcelos V (2013) Absence of negative allelopathic effects of cylindrospermopsin and microcystin-LR on selected marine and freshwater phytoplankton species. Hydrobiologia 705(1):27–42CrossRefGoogle Scholar
  27. Pollingher U, Hadas O, Yacobi Y, Zohary T, Berman T (1998) Aphanizomenon ovalisporum (Forti) in Lake Kinneret, Israel. J Plankton Res 20(7):1321–1339CrossRefGoogle Scholar
  28. Prince EK, Myers TL, Kubanek J (2008) Effects of harmful algal blooms on competitors: allelopathic mechanisms of the red tide dinoflagellate Karenia brevis. Limnol Oceanogr 53(2):531–541CrossRefGoogle Scholar
  29. Rengefors K, Pettersson K, Blenckner T, Anderson DM (2001) Species-specific alkaline phosphatase activity in freshwater spring phytoplankton: application of a novel method. J Plankton Res 23(4):435–443CrossRefGoogle Scholar
  30. Rzymski P, Poniedziałek B (2014) In search of environmental role of cylindrospermopsin: a review on global distribution and ecology of its producers. Water Res 66:320–337CrossRefGoogle Scholar
  31. Rzymski P, Poniedziałek B, Kokociński M, Jurczak T, Lipski D, Wiktorowicz K (2014) Interspecific allelopathy in cyanobacteria: cylindrospermopsin and Cylindrospermopsis raciborskii effect on the growth and metabolism of Microcystis aeruginosa. Harmful Algae 35:1–8CrossRefGoogle Scholar
  32. Shao J, Peng L, Luo S, Yu G, Gu J-d, Lin S, Li R (2013) First report on the allelopathic effect of Tychonema bourrellyi (cyanobacteria) against Microcystis aeruginosa (cyanobacteria). J Appl Phycol 25(5):1567–1573CrossRefGoogle Scholar
  33. Shaw GR, Sukenik A, Livne A, Chiswell RK, Smith MJ, Seawright AA, Norris RL, Eaglesham GK, Moore MR (1999) Blooms of the cylindrospermopsin containing cyanobacterium, Aphanizomenon ovalisporum (Forti), in newly constructed lakes, Queensland, Australia. Environ Toxicol 14(1):167–177CrossRefGoogle Scholar
  34. Sommer U (1989) Nutrient status and nutrient competition of phytoplankton in a shallow, hypertrophic lake. Limnol Oceanogr 34(7):1162–1173CrossRefGoogle Scholar
  35. Stucken K, John U, Cembella A, Soto-Liebe K, Vásquez M (2014) Impact of nitrogen sources on gene expression and toxin production in the diazotroph Cylindrospermopsis raciborskii CS-505 and non-diazotroph Raphidiopsis brookii D9. Toxins 6(6):1896–1915CrossRefGoogle Scholar
  36. Sukenik A, Eshkol R, Livne A, Hadas O, Rom M, Tchernov D, Vardi A, Kaplan A (2002) Inhibition of growth and photosynthesis of the dinoflagellate Peridinium gatunense by Microcystis sp.(cyanobacteria): a novel allelopathic mechanism. Limnol Oceanogr 47(6):1656–1663CrossRefGoogle Scholar
  37. Torres CA, Lürling M, Marinho MM (2015) Assessment of the effects of light availability on growth and competition between strains of Planktothrix agardhii and Microcystis aeruginosa. Microbial ecology: 1–12Google Scholar
  38. Viktória B, Vasas G, Dobronoki D, Gonda S, Nagy S, Bácsi I (2015) Effects of cylindrospermopsin producing cyanobacterium and its crude extracts on a benthic green alga—competition or allelopathy? Marine Drugs 13(11):6703–6722CrossRefGoogle Scholar
  39. Wacker A, Marzetz V, Spijkerman E (2015) Interspecific competition in phytoplankton drives the availability of essential mineral and biochemical nutrients. Ecology 96(9):2467–2477CrossRefGoogle Scholar
  40. Waterbury JB (2006) The cyanobacteria—isolation, purification and identification, The prokaryotes. Springer, pp. 1053–1073Google Scholar
  41. Weckx JE, Clijsters HM (1996) Oxidative damage and defense mechanisms in primary leaves of Phaseolus vulgaris as a result of root assimilation of toxic amounts of copper. Physiol Plant 96(3):506–512CrossRefGoogle Scholar
  42. Zapomělová E, Skácelová O, Pumann P, Kopp R, Janeček E (2012) Biogeographically interesting planktonic Nostocales (Cyanobacteria) in the Czech Republic and their polyphasic evaluation resulting in taxonomic revisions of Anabaena bergii Ostenfeld 1908 (Chrysosporum gen. nov.) and A. tenericaulis Nygaard 1949 (Dolichospermum tenericaule comb. nova). Hydrobiologia 698(1): 353–365Google Scholar
  43. Zhang J, Zhu B, Wu Z, Xu T, Lu Z (2012) Microcystis panniformis—a newly recorded species of Microcystis in China. Journal of Lake Sciences 24(4):647–650CrossRefGoogle Scholar
  44. Zhang M, Shi X, Yu Y, Kong F (2011) The acclimative changes in photochemistry after colony formation of the cyanobacteria Microcystis aeruginosa. J Phycol 47(3):524–532CrossRefGoogle Scholar
  45. Zhang T, Song L (2006) Allelopathic effect between Microcystis aeruginosa and three filamentous cyanobacteria. Journal of lake sciences 18(2):150–156CrossRefGoogle Scholar
  46. Zhu W, Pan Y, Tao J, Li X, Xu X, Wang Y, Wang Q (2013) Phytoplankton community and succession in a newly man-made shallow lake, Shanghai, China. Aquat Ecol 47(2):137–147CrossRefGoogle Scholar
  47. Zonneveld C (1998) Photoinhibition as affected by photoacclimation in phytoplankton: a model approach. J Theor Biol 193(1):115–123CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Wei Zhang
    • 1
  • Erik Jeppesen
    • 2
    • 3
  • Mengmeng Wang
    • 1
  • Xiaoying Xu
    • 1
  • Liqing Wang
    • 1
  1. 1.College of Fisheries and Life ScienceShanghai Ocean UniversityShanghaiChina
  2. 2.Department of BioscienceAarhus UniversitySilkeborgDenmark
  3. 3.Sino-Danish Centre for Education and Research (SDC)BeijingChina

Personalised recommendations