Effects of Cyanobacterial Secondary Metabolites on Phytoplankton Community Succession

  • Ying Pei
  • Runbing Xu
  • Sabine Hilt
  • Xuexiu ChangEmail author
Living reference work entry
Part of the Reference Series in Phytochemistry book series (RSP)


Allelopathic effects are one of the factors potentially influencing the succession of phytoplankton communities; however, their influence has often been neglected. This is especially true for cyanobacteria that often outcompete other phytoplankton species and form blooms causing severe problems. Allelopathic effects of cyanobacteria can play an important role for phytoplankton succession. In this chapter, we introduce the different ways how aquatic organisms are influenced by cyanobacterial allelochemicals; the mechanisms of their interaction from the aspects of chemical intermediates, target reaction, and target signals; and interfering factors and the ecological consequences of this process.

Cyanobacteria produce and excrete a variety of allelopathic compounds that affect other Cyanophyta, eukaryotic algae, bacteria, zooplankton, higher plants, and fish and mammalian cells. These effects are regulated by various abiotic and biotic conditions, such as nutrient availability, temperature, and light intensity but also cell density and growth phase of the source cyanobacterial community. The bioactive metabolites include cyclic peptides, alkaloids, terpenoids, and others which can have a variety of inhibitory effects on the different target organisms. Ecological consequences such as declines in biodiversity and accumulation of toxins in the food chain have been shown. However, most of these compounds have not yet been fully tested regarding their full range of effects on natural phytoplankton communities. A detailed elucidation of the influence of cyanobacterial allelochemicals is of key importance for understanding and managing the succession of natural phytoplankton communities.


Cyanobacteria Allelopathy Secondary metabolites Phytoplankton succession Chemical ecology 



This work was supported by the National Natural Science Foundation of China (No. 31260138) and the Major Research and Development Project of Yunnan Province (2018BC002).


  1. 1.
    Sommer U, Adrian R, De Senerpont Domis L, Elser JJ, Gaedke U, Ibelings B, Jeppesen E, Lürling M, Molinero JC, Mooij WM, van Donk E, Winder M (2012) Beyond the plankton ecology group (PEG) model: mechanisms driving plankton succession. Annu Rev Ecol Evol Syst 43:429–448CrossRefGoogle Scholar
  2. 2.
    Keating KI (1977) Allelopathic influence on blue-green bloom sequence in a eutrophic lake. Science 196:885–887PubMedCrossRefGoogle Scholar
  3. 3.
    Keating KI (1978) Blue-green algal inhibition of diatom growth transition from mesotrophic to eutrophic community structure. Science 199:971–973PubMedCrossRefGoogle Scholar
  4. 4.
    Molisch H (1938) Der Einfluss einer Pflanze auf die Andere, Allelopathie. Nature 141:493CrossRefGoogle Scholar
  5. 5.
    Rice EL (1984) Allelopathy, 2nd edn. Academic, San DiegoGoogle Scholar
  6. 6.
    Whittaker RH, Feeny PP (1971) Allelochemics: chemical interactions between species. Science 171:757–770PubMedCrossRefGoogle Scholar
  7. 7.
    Anaya AL (1999) Allelopathy as a tool in the management of biotic resources in agroecosystems. Crit Rev Plant Sci 18:697–739CrossRefGoogle Scholar
  8. 8.
    Bagnères A-G, Hossaert-Mckey M (2016) Chemical ecology. Wiley-ISTE, Hoboken/LondonCrossRefGoogle Scholar
  9. 9.
    Gross EM (2003) Allelopathy of aquatic autotrophs. Crit Rev Plant Sci 22:313–339CrossRefGoogle Scholar
  10. 10.
    Harke MJ, Steffen MM, Gobler CJ, Otten TG, Wilhelm SW, Wood SA, Paerl HW (2016) A review of the global ecology, genomics, and biogeography of the toxic cyanobacterium, Microcystis spp. Harmful Algae 54:4–20PubMedCrossRefGoogle Scholar
  11. 11.
    Chorus I (2001) Cyanotoxins: occurrence, causes, consequences. Springer, Berlin/HeidelbergCrossRefGoogle Scholar
  12. 12.
    Jochimsen EM, Carmichael WW, An JS, Cardo DM, Cookson ST, Holmes CE, Antunes MB, Da DMF, Lyra TM, Barreto VS (1998) Liver failure and death after exposure to microcystins at a hemodialysis center in Brazil. N Engl J Med 338:873–880PubMedCrossRefGoogle Scholar
  13. 13.
    Paerl HW, Fulton RS, Moisander PH, Dyble J (2001) Harmful freshwater algal blooms, with an emphasis on cyanobacteria. Sci World J 1:76CrossRefGoogle Scholar
  14. 14.
    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
  15. 15.
    Aubriot L, Bonilla S (2018) Regulation of phosphate uptake reveals cyanobacterial bloom resilience to shifting N:P ratios. Freshw Biol 63:318–329CrossRefGoogle Scholar
  16. 16.
    Berry JP, Gantar M, Perez MH, Berry G, Noriega FG (2008) Cyanobacterial toxins as allelochemicals with potential applications as algaecides, herbicides and insecticides. Mar Drugs 6:117–146PubMedPubMedCentralCrossRefGoogle Scholar
  17. 17.
    Shimizu Y (1996) Microalgal metabolites: a new perspective. Annu Rev Microbiol 50:431–465PubMedCrossRefGoogle Scholar
  18. 18.
    Żak A, Kosakowska A (2016) Cyanobacterial and microalgal bioactive compounds – the role of secondary metabolites in allelopathic interactions. Oceanol Hydrobiol Stud 45:131CrossRefGoogle Scholar
  19. 19.
    Tidgewell K, Clark BR, Gerwick WH (2010) 2.06 – The natural products chemistry of cyanobacteria. In: Liu H-W, Mander L (eds) Comprehensive natural products II. Elsevier, OxfordGoogle Scholar
  20. 20.
    Gantar M, Berry JP, Thomas S, Wang M, Perez R, Rein KS (2008) Allelopathic activity among Cyanobacteria and microalgae isolated from Florida freshwater habitats. FEMS Microbiol Ecol 64:55–64PubMedPubMedCentralCrossRefGoogle Scholar
  21. 21.
    Suikkanen S, Fistarol G, Granéli E (2005) Effect of cyanobacterial allelochemicals on a natural plankton community. Mar Ecol Prog Ser 287:1–9CrossRefGoogle Scholar
  22. 22.
    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
  23. 23.
    Leão PN, Vasconcelos MTSD, Vasconcelos VM (2009) Allelopathy in freshwater cyanobacteria. Crit Rev Microbiol 35:271–282PubMedCrossRefGoogle Scholar
  24. 24.
    do Bittencourt-Oliveira MC, Chia MA, de Oliveira HSB, Cordeiro Araújo MK, Molica RJR, Dias CTS (2014) Allelopathic interactions between microcystin-producing and non-microcystin-producing cyanobacteria and green microalgae: implications for microcystins production. J Appl Phycol 27:275–284CrossRefGoogle Scholar
  25. 25.
    Sumper M, Brunner E (2006) Learning from diatoms: nature’s tools for the production of nanostructured silica. Adv Funct Mater 16:17–26CrossRefGoogle Scholar
  26. 26.
    Armbrust EV (2009) The life of diatoms in the world’s oceans. Nature 459:185–185PubMedCrossRefGoogle Scholar
  27. 27.
    Schagerl M, Unterrieder I, Angeler DG (2002) Allelopathy among Cyanoprokaryota and other algae originating from Lake Neusiedlersee (Austria). Int Rev Hydrobiol 87:365–374CrossRefGoogle Scholar
  28. 28.
    Wang LC, Zi JM, Xu RB, Hilt S, Hou XL, Chang XX (2017) Allelopathic effects of Microcystis aeruginosa on green algae and a diatom: evidence from exudates addition and co-culturing. Harmful Algae 61:56–62CrossRefGoogle Scholar
  29. 29.
    Suikkanen S, Fistarol GO, Granéli E (2004) Allelopathic effects of the Baltic cyanobacteria Nodularia spumdigena, Aphanizomenon flos-aquae and Anabaena lemmermannii on algal monocultures. J Exp Mar Biol Ecol 308:85–101CrossRefGoogle Scholar
  30. 30.
    Suikkanen S, Engström-Öst J, Jokela J, Sivonen K, Viitasalo M (2006) Allelopathy of Baltic Sea cyanobacteria: no evidence for the role of nodularin. J Plankton Res 28:543–550CrossRefGoogle Scholar
  31. 31.
    B-Béres V, Grigorszky I, Vasas G, Borics G, Várbíró G, Nagy SA, Borbély G, Bácsi I (2012) The effects of Microcystis aeruginosa (cyanobacterium) on Cryptomonas ovata (Cryptophyta) in laboratory cultures: why these organisms do not coexist in steady-state assemblages? Hydrobiologia 691:97–107CrossRefGoogle Scholar
  32. 32.
    Flores E, Wolk CP (1986) Production, by filamentous, nitrogen-fixing cyanobacteria, of a bacteriocin and of other antibiotics that kill related strains. Arch Microbiol 145:215–219PubMedCrossRefGoogle Scholar
  33. 33.
    Bártová K, Hilscherová K, Babica P, Maršálek B (2011) Extract of Microcystis water bloom affects cellular differentiation in filamentous cyanobacterium Trichormus variabilis (Nostocales, Cyanobacteria). J Appl Phycol 23:967–973CrossRefGoogle Scholar
  34. 34.
    Von Elert E, Jüttner F (1996) Factors influencing the allelopathic activity of the planktonic cyanobacterium Trichormus doliolum. Phycologia 35:68–73CrossRefGoogle Scholar
  35. 35.
    Dodds WK, Gudder DA, Mollenhauer D (1995) The ecology of nostoc. J Phycol 31:2–18CrossRefGoogle Scholar
  36. 36.
    Leao PN, Pereira AR, Liu WT, Ng J, Pevzner PA, Dorrestein PC, Konig GM, Vasconcelos VM, Gerwick WH (2010) Synergistic allelochemicals from a freshwater cyanobacterium. Proc Natl Acad Sci U S A 107:11183–11188PubMedPubMedCentralCrossRefGoogle Scholar
  37. 37.
    Bishop CT, Anet EF, Gorham PR (1959) Isolation and identification of the fast-death factor in Microcystis aeruginosa NRC-1. Can J Biochem Physiol 37:453–453PubMedCrossRefGoogle Scholar
  38. 38.
    WHO (2003) Cyanobacterial toxins: Microcystin-LR in drinking-water. In: World Health Organization (ed) Background document for preparation of WHO Guidelines for drinking-water quality. World Health Organization, GenevaGoogle Scholar
  39. 39.
    Bratbak G, Thingstad T (1985) Phytoplankton-bacteria interactions: an apparent paradox? Analysis of a model system with both competition and commensalism. Mar Ecol Prog Ser 25:23–30CrossRefGoogle Scholar
  40. 40.
    Fish SA, Codd GA (1994) Bioactive compound production by thermophilic and thermotolerant cyanobacteria (blue-green algae). World J Microbiol Biotechnol 10:338–341PubMedCrossRefGoogle Scholar
  41. 41.
    Berry JP, Gantar M, Gawley RE, Wang M, Rein KS (2004) Pharmacology and toxicology of pahayokolide A, a bioactive metabolite from a freshwater species of Lyngbya isolated from the Florida Everglades. Comp Biochem Physiol Part C: Toxicol Pharmacol 139:231–238Google Scholar
  42. 42.
    Volk R-B, Furkert FH (2006) Antialgal, antibacterial and antifungal activity of two metabolites produced and excreted by cyanobacteria during growth. Microbiol Res 161:180–186PubMedCrossRefGoogle Scholar
  43. 43.
    Dias F, Antunes JT, Ribeiro T, Azevedo J, Vasconcelos V, Leão PN (2017) Cyanobacterial allelochemicals but not cyanobacterial cells markedly reduce microbial community diversity. Front Microbiol 8:1495PubMedPubMedCentralCrossRefGoogle Scholar
  44. 44.
    Scheffer M, Hosper SH, Meijer ML, Moss B, Jeppesen E (1993) Alternative equilibria in shallow lakes. Trends Ecol Evol 8:275–279PubMedCrossRefGoogle Scholar
  45. 45.
    Hilt S, Gross EM (2008) Can allelopathically active submerged macrophytes stabilise clear-water states in shallow lakes? Basic Appl Ecol 9:422–432CrossRefGoogle Scholar
  46. 46.
    Hilt S (2015) Regime shifts between macrophytes and phytoplankton–concepts beyond shallow lakes, unravelling stabilizing mechanisms and practical consequences. Limnetica 34:467–480Google Scholar
  47. 47.
    Mohamed ZA (2017) Macrophytes-cyanobacteria allelopathic interactions and their implications for water resources management – a review. Limnologica 63:122–132CrossRefGoogle Scholar
  48. 48.
    Zheng GL, Xu RB, Chang XX, Hilt S, Wu C (2013) Cyanobacteria can allelopathically inhibit submerged macrophytes: effects of Microcystis aeruginosa extracts and exudates on Potamogeton malaianus. Aquat Bot 109:1–7CrossRefGoogle Scholar
  49. 49.
    Xu RB, Wu F, Hilt S, Wu C, Wang XL, Chang XX (2015) Recovery limitation of endangered Ottelia acuminata by allelopathic interaction with cyanobacteria. Aquat Ecol 49:333–342CrossRefGoogle Scholar
  50. 50.
    Chislock MF, Sarnelle O, Jernigan LM, Wilson AE (2013) Do high concentrations of microcystin prevent Daphnia control of phytoplankton? Water Res 47:1961–1970PubMedCrossRefGoogle Scholar
  51. 51.
    Leitão E, Ger KA, Panosso R (2018) Selective grazing by a tropical copepod (Notodiaptomus iheringi) facilitates Microcystis dominance. Front Microbiol 9:301PubMedPubMedCentralCrossRefGoogle Scholar
  52. 52.
    Scotti T, Mimura M, Wakano JY (2015) Avoiding toxic prey may promote harmful algal blooms. Ecol Complex 21:157–165CrossRefGoogle Scholar
  53. 53.
    Jungmann D (1995) Isolation, purification, and characterization of new Daphnia-toxic compound from axenic Microcystis flos-aquae strain PCC7806. J Chem Ecol 21:1665–1676PubMedCrossRefGoogle Scholar
  54. 54.
    Rohrlack T, Christoffersen K, Hansen PE, Zhang W, Czarnecki O, Henning M, Fastner J, Erhard M, Neilan BA, Kaebernick M (2003) Isolation, characterization, and quantitative analysis of microviridin J, a new Microcystis metabolite toxic to Daphnia. J Chem Ecol 29:1757–1770PubMedCrossRefGoogle Scholar
  55. 55.
    Wiegand C, Peuthert A, Pflugmacher S, Carmeli S (2002) Effects of microcin SF608 and microcystin-LR, two cyanotobacterial compounds produced by Microcystis sp., on aquatic organisms. Environ Toxicol 17:400–406PubMedCrossRefGoogle Scholar
  56. 56.
    Gustafsson S, Hansson L-A (2004) Development of tolerance against toxic cyanobacteria in Daphnia. Aquat Ecol 38:37–44CrossRefGoogle Scholar
  57. 57.
    Smutná M, Priebojová J, Večerková J, Hilscherová K (2017) Retinoid-like compounds produced by phytoplankton affect embryonic development of Xenopus laevis. Ecotoxicol Environ Saf 138:32–38PubMedCrossRefGoogle Scholar
  58. 58.
    Zi J, Pan X, MacIsaac HJ, Yang J, Xu R, Chen S, Chang X (2018) Cyanobacteria blooms induce embryonic heart failure in an endangered fish species. Aquat Toxicol 194:78–85PubMedCrossRefGoogle Scholar
  59. 59.
    El-Sheekh MM, Dawah AM, Abd El-Rahman AM, El-Adel HM, Abd El-Hay RA (2008) Antimicrobial activity of the cyanobacteria Anabaena wisconsinense and Oscillatoria curviceps against pathogens of fish in aquaculture. Ann Microbiol 58:527–534CrossRefGoogle Scholar
  60. 60.
    Jonas A, Buranova V, Scholz S, Fetter E, Novakova K, Kohoutek J, Hilscherova K (2014) Retinoid-like activity and teratogenic effects of cyanobacterial exudates. Aquat Toxicol 155:283–290PubMedCrossRefGoogle Scholar
  61. 61.
    Jonas A, Scholz S, Fetter E, Sychrova E, Novakova K, Ortmann J, Benisek M, Adamovsky O, Giesy JP, Hilscherova K (2015) Endocrine, teratogenic and neurotoxic effects of cyanobacteria detected by cellular in vitro and zebrafish embryos assays. Chemosphere 120:321–327PubMedCrossRefGoogle Scholar
  62. 62.
    Zagatto PA, Buratini S, Aragão MA, Ferrão-Filho AS (2012) Neurotoxicity of two Cylindrospermopsis raciborskii (cyanobacteria) strains to mice, Daphnia, and fish. Environ Toxicol Chem 31:857–862PubMedCrossRefGoogle Scholar
  63. 63.
    Otten TG, Paerl HW (2015) Health effects of toxic cyanobacteria in U.S. drinking and recreational waters: our current understanding and proposed direction. Curr Environ Health Rep 2:75–84PubMedCrossRefGoogle Scholar
  64. 64.
    Carmichael WW (1992) Cyanobacteria secondary metabolites – the cyanotoxins. J Appl Bacteriol 72:445–459PubMedCrossRefGoogle Scholar
  65. 65.
    Pearson L, Mihali T, Moffitt M, Kellmann R, Neilan B (2010) On the chemistry, toxicology and genetics of the cyanobacterial toxins, microcystin, nodularin, saxitoxin and cylindrospermopsin. Mar Drugs 8:1650–1680PubMedPubMedCentralCrossRefGoogle Scholar
  66. 66.
    Babica P, Bláha L, Maršálek B (2006) Exploring the natural role of microcystins – a review of effects on photoautotrophic organisms. J Phycol 42:9–20CrossRefGoogle Scholar
  67. 67.
    Leflaive JP, Ten-Hage L (2007) Algal and cyanobacterial secondary metabolites in freshwaters: a comparison of allelopathic compounds and toxins. Freshw Biol 52:199–214CrossRefGoogle Scholar
  68. 68.
    Li Y, Li D (2012) Competition between toxic Microcystis aeruginosa and nontoxic Microcystis wesenbergii with Anabaena PCC7120. J Appl Phycol 24:69–78CrossRefGoogle Scholar
  69. 69.
    Mazmouz R, Chapuis-Hugon F, Pichon V, Méjean A, Ploux O (2011) The last step of the biosynthesis of the cyanotoxins cylindrospermopsin and 7-epi-cylindrospermopsin is catalysed by CyrI, a 2-Oxoglutarate-dependent iron oxygenase. Chembiochem 12:858–862PubMedCrossRefGoogle Scholar
  70. 70.
    Burford MA, Beardall J, Willis A, Orr PT, Magalhaes VF, Rangel LM, Azevedo SMFOE, Neilan BA (2016) Understanding the winning strategies used by the bloom-forming cyanobacterium Cylindrospermopsis raciborskii. Harmful Algae 54:44–53PubMedCrossRefGoogle Scholar
  71. 71.
    Preussel K, Wessel G, Fastner J, Chorus I (2009) Response of cylindrospermopsin production and release in Aphanizomenon flos-aquae (Cyanobacteria) to varying light and temperature conditions. Harmful Algae 8:645–650CrossRefGoogle Scholar
  72. 72.
    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
  73. 73.
    Sant’Anna CL, de Carvalho LR, Fiore MF, Silva-Stenico ME, Lorenzi AS, Rios FR, Konno K, Garcia C, Lagos N (2011) Highly toxic Microcystis aeruginosa strain, isolated from São Paulo – Brazil, produce hepatotoxins and paralytic shellfish poison neurotoxins. Neurotox Res 19:389–402PubMedCrossRefGoogle Scholar
  74. 74.
    Legrand C, Rengefkors K, Fistarol G, Granéli E (2003) Allelopathy in phytoplankton – biochemical, ecological and evolutionary aspects. Phycologia 42:406–419CrossRefGoogle Scholar
  75. 75.
    Matsuura HN, Fett-Neto AG (2017) Plant alkaloids: main features, toxicity, and mechanisms of action. In: Carlini CR, Ligabue-Braun R (eds) Plant toxins. Springer Netherlands, DordrechtGoogle Scholar
  76. 76.
    Wink M, Twardowski T (1992) Allelochemical properties of alkaloids. Effects on plants, bacteria and protein biosynthesis. In: Rizvi SJH, Rizvi V (eds) Allelopathy: basic and applied aspects. Springer Netherlands, DordrechtGoogle Scholar
  77. 77.
    Pattanaik B, Lindberg P (2015) Terpenoids and their biosynthesis in cyanobacteria. Life 5:269–293PubMedPubMedCentralCrossRefGoogle Scholar
  78. 78.
    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 25:1567–1573CrossRefGoogle Scholar
  79. 79.
    Volk R-B (2005) Screening of microalgal culture media for the presence of algicidal compounds and isolation and identification of two bioactive metabolites, excreted by the cyanobacteria Nostoc insulare and Nodularia harveyana. J Appl Phycol 17:339–347CrossRefGoogle Scholar
  80. 80.
    Gromov BV, Vepritskiy AA, Titova NN, Mamkayeva KA, Alexandrova OV (1991) Production of the antibiotic cyanobacterin LU-1 by Nostoc linckia CALU 892 (cyanobacterium). J Appl Phycol 3:55–59CrossRefGoogle Scholar
  81. 81.
    Song H, Lavoie M, Fan XJ, Tan HN, Liu GF, Xu PF, Fu ZW, Paerl HW, Qian HF (2017) Allelopathic interactions of linoleic acid and nitric oxide increase the competitive ability of Microcystis aeruginosa. ISME J 11:1865–1876PubMedPubMedCentralCrossRefGoogle Scholar
  82. 82.
    Jaja-Chimedza A, Gantar M, Mayer GD, Gibbs PDL, Berry JP (2012) Effects of cyanobacterial lipopolysaccharides from microcystis on glutathione-based detoxification pathways in the zebrafish (Danio rerio) embryo. Toxins 4:390–404PubMedPubMedCentralCrossRefGoogle Scholar
  83. 83.
    Jaja-Chimedza A, Saez C, Sanchez K, Gantar M, Berry JP (2015) Identification of teratogenic polymethoxy-1-alkenes from Cylindrospermopsis raciborskii, and taxonomically diverse freshwater cyanobacteria and green algae. Harmful Algae 49:156–161PubMedPubMedCentralCrossRefGoogle Scholar
  84. 84.
    Gross EM, Wolk CP, Jüttner F (1991) Fischerellin, a new allelochemical from the freshwater cyanobacterium Fischerella muscicola. J Phycol 27:686–692CrossRefGoogle Scholar
  85. 85.
    Ishida K, Murakami M (2000) Kasumigamide, an antialgal peptide from the cyanobacterium Microcystis aeruginosa. J Org Chem 65:5898–5900PubMedCrossRefGoogle Scholar
  86. 86.
    An T, Kumar TKS, Wang M, Liu L, Lay JO Jr, Liyanage R, Berry J, Gantar M, Marks V, Gawley RE, Rein KS (2007) Structures of pahayokolides A and B, cyclic peptides from a Lyngbya sp. J Nat Prod 70:730–735PubMedPubMedCentralCrossRefGoogle Scholar
  87. 87.
    Vestola J, Shishido TK, Jokela J, Fewer DP, Aitio O, Permi P, Wahlsten M, Wang H, Rouhiainen L, Sivonen K (2014) Hassallidins, antifungal glycolipopeptides, are widespread among cyanobacteria and are the end-product of a nonribosomal pathway. Proc Natl Acad Sci 111:E1909–E1917PubMedCrossRefGoogle Scholar
  88. 88.
    Adiv S, Ahronov-Nadborny R, Carmeli S (2012) New aeruginazoles, a group of thiazole-containing cyclic peptides from Microcystis aeruginosa blooms. Tetrahedron 68:1376–1383CrossRefGoogle Scholar
  89. 89.
    Leikoski N, Fewer DP, Jokela J, Alakoski P, Wahlsten M, Sivonen K (2012) Analysis of an inactive cyanobactin biosynthetic gene cluster leads to discovery of new natural products from strains of the genus Microcystis. PLoS One 7:e43002PubMedPubMedCentralCrossRefGoogle Scholar
  90. 90.
    Banker R, Carmeli S (1999) Inhibitors of serine proteases from a waterbloom of the cyanobacterium Microcystis sp. Tetrahedron 55:10835–10844CrossRefGoogle Scholar
  91. 91.
    Jüttner F, Todorova AK, Walch N, von Philipsborn W (2001) Nostocyclamide M: a cyanobacterial cyclic peptide with allelopathic activity from Nostoc 31. Phytochemistry 57:613–619PubMedCrossRefGoogle Scholar
  92. 92.
    Portmann C, Blom JF, Gademann K, Jüttner F (2008) Aerucyclamides A and B: isolation and synthesis of toxic ribosomal heterocyclic peptides from the cyanobacterium Microcystis aeruginosa PCC 7806. J Nat Prod 71:1193–1196PubMedCrossRefGoogle Scholar
  93. 93.
    Pérez Gutiérrez RM, Martínez Flores A, Vargas Solís R, Carmona Jimenez J (2008) Two new antibacterial norabietane diterpenoids from cyanobacteria, Microcoleous lacustris. J Nat Med 62:328–331PubMedCrossRefGoogle Scholar
  94. 94.
    Höckelmann C, Becher PG, von Reuss SH, Jüttner F (2009) Sesquiterpenes of the geosmin-producing cyanobacterium Calothrix PCC 7507 and their toxicity to invertebrates. Zeitschrift fur Naturforschung. C. J Biosci 64:49–55Google Scholar
  95. 95.
    Zhang K, Lin TF, Zhang T, Li C, Gao N (2013) Characterization of typical taste and odor compounds formed by Microcystis aeruginosa. J Environ Sci 25:1539–1548CrossRefGoogle Scholar
  96. 96.
    Walsh K, Jones GJ, Dunstan RH (1998) Effect of high irradiance and iron on volatile odour compounds in the cyanobacterium Microcystis aeruginosa. Phytochemistry 49:1227–1239PubMedCrossRefGoogle Scholar
  97. 97.
    Beresovsky D, Hadas O, Livne A, Sukenik A, Kaplan A, Carmeli S (2006) Toxins and biologically active secondary metabolites of Microcystis sp. isolated from Lake Kinneret. Isr J Chem 46:79–87CrossRefGoogle Scholar
  98. 98.
    Jaja-Chimedza A, Sanchez K, Gantar M, Gibbs P, Schmale M, Berry JP (2017) Carotenoid glycosides from cyanobacteria are teratogenic in the zebrafish (Danio rerio) embryo model. Chemosphere 174:478–489PubMedPubMedCentralCrossRefGoogle Scholar
  99. 99.
    Micallef ML, Sharma D, Bunn BM, Gerwick L, Viswanathan R, Moffitt MC (2014) Comparative analysis of hapalindole, ambiguine and welwitindolinone gene clusters and reconstitution of indole-isonitrile biosynthesis from cyanobacteria. BMC Microbiol 14:213–213PubMedPubMedCentralCrossRefGoogle Scholar
  100. 100.
    Volk R-B, Mundt S (2007) Cytotoxic and non-cytotoxic exometabolites of the cyanobacterium Nostoc insulare. J Appl Phycol 19:55–62CrossRefGoogle Scholar
  101. 101.
    Volk R-B (2007) Studies on culture age versus exometabolite production in batch cultures of the cyanobacterium Nostoc insulare. J Appl Phycol 19:491–495CrossRefGoogle Scholar
  102. 102.
    Hirata K, Yoshitomi S, Dwi S, Iwabe O, Mahakhant A, Polchai J, Miyamoto K (2003) Bioactivities of nostocine a produced by a freshwater cyanobacterium Nostoc spongiaeforme TISTR 8169. J Biosci Bioeng 95:512–517PubMedCrossRefGoogle Scholar
  103. 103.
    Doan NT, Rickards RW, Rothschild JM, Smith GD, Doan NT, Rickards RW, Rothschild JM, Smith GD (2000) Allelopathic actions of the alkaloid 12-epi-hapalindole E isonitrile and calothrixin A from cyanobacteria of the genera Fischerella and Calothrix. J Appl Phycol 12:409–416CrossRefGoogle Scholar
  104. 104.
    Rickards RW, Rothschild JM, Willis AC, de Chazal NM, Kirk J, Kirk K, Saliba KJ, Smith GD (1999) Calothrixins A and B, novel pentacyclic metabolites from Calothrix cyanobacteria with potent activity against malaria parasites and human cancer cells. Tetrahedron 55:13513–13520CrossRefGoogle Scholar
  105. 105.
    Etchegaray A, Rabello E, Dieckmann R, Moon DH, Fiore MF, von Döhren H, Tsai SM, Neilan BA (2004) Algicide production by the filamentous cyanobacterium Fischerella sp. CENA 19. J Appl Phycol 16:237–243CrossRefGoogle Scholar
  106. 106.
    Walton K, Gantar M, Gibbs PDL, Schmale MC, Berry JP (2014) Indole alkaloids from Fischerella inhibit vertebrate development in the zebrafish (Danio rerio) embryo model. Toxins 6:3568–3581PubMedPubMedCentralCrossRefGoogle Scholar
  107. 107.
    Abarzua S, Jakubowski S, Eckert S, Fuchs P (1999) Biotechnological investigation for the prevention of marine biofouling II. Blue-green algae as potential producers of biogenic agents for the growth inhibition of microfouling organisms. Bot Mar 42:459–465CrossRefGoogle Scholar
  108. 108.
    Gleason FK, Paulson JL (1984) Site of action of the natural algicide, cyanobacterin, in the blue-green alga, Synechococcus sp. Arch Microbiol 138:273–277CrossRefGoogle Scholar
  109. 109.
    Mason CP, Edwards KR, Carlson RE, Pignatello J, Gleason FK, Wood JM (1982) Isolation of chlorine-containing antibiotic from the freshwater cyanobacterium Scytonema hofmanni. Science (New York) 215:400–402CrossRefGoogle Scholar
  110. 110.
    Jaja-Chimedza A, Gantar M, Gibbs PDL, Schmale MC, Berry JP (2012) Polymethoxy-1-alkenes from Aphanizomenon ovalisporum inhibit vertebrate development in the zebrafish (Danio rerio) embryo model. Mar Drugs 10:2322–2336PubMedPubMedCentralCrossRefGoogle Scholar
  111. 111.
    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 47:1656–1663CrossRefGoogle Scholar
  112. 112.
    Pflugmacher S, Aulhorn M, Grimm B (2007) Influence of a cyanobacterial crude extract containing microcystin-LR on the physiology and antioxidative defence systems of different spinach variants. New Phytol 175:482–489PubMedCrossRefGoogle Scholar
  113. 113.
    Ma Z, Fang T, Thring RW, Li Y, Yu H, Zhou Q, Zhao M (2015) Toxic and non-toxic strains of Microcystis aeruginosa induce temperature dependent allelopathy toward growth and photosynthesis of Chlorella vulgaris. Harmful Algae 48:21–29PubMedCrossRefGoogle Scholar
  114. 114.
    Zhang TT, Liu L, Yang XH, Zhang SJ, Xia WT, Li C (2014) Allelopathic control of freshwater phytoplankton by the submerged macrophyte Najas minor All. Acta Ecol Sin 34:351–355CrossRefGoogle Scholar
  115. 115.
    Xu RB, Hilt S, Pei Y, Yin LJ, Wang XL, Chang XX (2016) Growth phase-dependent allelopathic effects of cyanobacterial exudates on Potamogeton crispus L. seedlings. Hydrobiologia 767:137–149CrossRefGoogle Scholar
  116. 116.
    Vanormelingen P, Vyverman W, De Bock D, Van der Gucht K, Meester LD (2009) Local genetic adaptation to grazing pressure of the green alga Desmodesmus armatus in a strongly connected pond system. Limnol Oceanogr 54:503–511CrossRefGoogle Scholar
  117. 117.
    Eigemann F, Vanormelingen P, Hilt S (2013) Sensitivity of the green alga Pediastrum duplex Meyen to allelochemicals is strain-specific and not related to co-occurrence with allelopathic macrophytes. PLoS One 8:e78463PubMedPubMedCentralCrossRefGoogle Scholar
  118. 118.
    Chang XX, Eigemann F, Hilt S (2012) Do macrophytes support harmful cyanobacteria? Interactions with a green alga reverse the inhibiting effects of macrophyte allelochemicals on Microcystis aeruginosa. Harmful Algae 19:76–84CrossRefGoogle Scholar
  119. 119.
    Chia MA, Cordeiro-Araújo MK, Lorenzi AS, do Carmo Bittencourt-Oliveira M (2017) Cylindrospermopsin induced changes in growth, toxin production and antioxidant response of Acutodesmus acuminatus and Microcystis aeruginosa under differing light and nitrogen conditions. Ecotoxicol Environ Saf 142:189–199PubMedCrossRefGoogle Scholar
  120. 120.
    Pei Y, Liu L, Hilt S, Xu R, Wang B, Li C, Chang X (2018) Root exudated algicide of Eichhornia crassipes enhances allelopathic effects of cyanobacteria Microcystis aeruginosa on green algae. Hydrobiologia 823:67–77CrossRefGoogle Scholar
  121. 121.
    Lürling M, Eshetu F, Faassen EJ, Kosten S, Huszar VLM (2013) Comparison of cyanobacterial and green algal growth rates at different temperatures. Freshw Biol 58:552–559Google Scholar
  122. 122.
    Chen Y, Qin B, Teubner K, Dokulil MT (2003) Long-term dynamics of phytoplankton assemblages: Microcystis-domination in Lake Taihu, a large shallow lake in China. J Plankton Res 25:445–453CrossRefGoogle Scholar
  123. 123.
    Imai H, Chang KH, Kusaba M, Nakano S (2009) Temperature-dependent dominance of Microcystis (Cyanophyceae) species: M. aeruginosa and M. wesenbergii. J Plankton Res 31:171–178CrossRefGoogle Scholar
  124. 124.
    Lei L, Li C, Peng L, Han BP (2015) Competition between toxic and non-toxic Microcystis aeruginosa and its ecological implication. Ecotoxicology 24:1411–1418PubMedCrossRefGoogle Scholar
  125. 125.
    Antunes JT, Leao PN, Vasconcelos VM (2012) Influence of biotic and abiotic factors on the allelopathic activity of the cyanobacterium Cylindrospermopsis raciborskii strain LEGE 99043. Microb Ecol 64:584–592PubMedCrossRefGoogle Scholar
  126. 126.
    Nobel W, Matthijs HCP, Elert E, Mur LR (1998) Comparison of the light-limited growth of the nitrogen-fixing cyanobacteria Anabaena and Aphanizomenon. New Phytol 138:579–587CrossRefGoogle Scholar
  127. 127.
    Ray S, Bagchi SN (2001) Nutrients and pH regulate algicide accumulation in cultures of the cyanobacterium Oscillatoria laetevirens. New Phytol 149:455–460CrossRefGoogle Scholar
  128. 128.
    Shimoda Y, Arhonditsis GB (2016) Phytoplankton functional type modelling: running before we can walk? A critical evaluation of the current state of knowledge. Ecol Model 320:29–43CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Ying Pei
    • 1
  • Runbing Xu
    • 1
  • Sabine Hilt
    • 2
  • Xuexiu Chang
    • 1
    Email author
  1. 1.School of Ecology and Environmental ScienceYunnan UniversityKunmingPeople’s Republic of China
  2. 2.Leibniz-Institute of Freshwater Ecology and Inland FisheriesBerlinGermany

Personalised recommendations