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“Non-Toxic” Cyclic Peptides Induce Lysis of Cyanobacteria—An Effective Cell Population Density Control Mechanism in Cyanobacterial Blooms

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Abstract

The presence of planktopeptin BL1125, anabaenopeptin B and anabaenopeptin F, two types of “non-toxic” cyclic peptide produced in bloom forming cyanobacteria, can provoke lysis of different non-axenic Microcystis aeruginosa cell lines via the induction of virus-like particles. The resulting particles are also able to infect the axenic M. aeruginosa cell line without lytic effects. Nevertheless, the presence of “non-toxic” cyclic peptides of cyanobacterial origin can induce lysis of these previously infected cells. This effect implies that a possible role of these peptides in the natural environment is the control of cyanobacterial population density. Lysogenic cyanobacteria can consequently act as hot-spots that, in the presence of cyanobacterial cyclic peptides, release numerous infectious particles. The process can be self-augmented with the simultaneous release of additional cyclic peptides from the producing lysogens, starting a forest fire effect that ends in collapse of cyanobacterial blooms.

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References

  1. Banker R, Carmeli S (1999) Inhibitors of serine proteases from a waterbloom of the cyanobacterium Microcystis sp. Tetrahedron 55:10835–10844

    Article  CAS  Google Scholar 

  2. Barrios-Llerena ME, Burja AM, Wright PC (2007) Genetic analysis of polyketide synthase and peptide synthetase genes in cyanobacteria as a mining tool for secondary metabolites. J Ind Microbiol Biotechnol 34:443–456

    Article  PubMed  CAS  Google Scholar 

  3. Bergh O, Børsheim KY, Bratbak G, Heldal M (1989) High abundance of viruses found in aquatic environments. Nature 340:467–468

    Article  PubMed  CAS  Google Scholar 

  4. Carmichael WW, Tones CLA, Mahmood NA, Theiss WC (1985) Algal toxins and water-based diseases. CPC Crit Rev Environ Contr 15:275–283

    CAS  Google Scholar 

  5. Carmichael WW, Gorham PR (1981) The mosaic nature of toxic blooms of cyanobacteria. In: Carmicheal WW (ed) The Water Environment: Algal Toxins and Health. Plenum, New York, pp 161–172

    Google Scholar 

  6. Christoffersen K (1996) Ecological implications of cyanobacterial toxins in aquatic food webs. Phycologia 35:42–50

    Article  Google Scholar 

  7. Dittmann E, Neilan BA, Börner T (2001) Molecular biology of peptide and polyketide biosynthesis in cyanobacteria. Appl Microbiol Biotechnol 57:467–473

    Article  PubMed  CAS  Google Scholar 

  8. Gons HJ, Ebert J, Hoogveld HL, van den Hove L, Pel R, Takkenberg W, Woldringh CJ (2002) Observations on cyanobacterial population collapse in eutrophic lake water. Anton Leeuv Int J 81:319–326

    Article  CAS  Google Scholar 

  9. Grach-Pogrebinsky O, Sedmak B, Carmeli S (2003) Protease inhibitors from a Slovenian Lake Bled toxic waterbloom of the cyanobacterium Planktothrix rubescens. Tetrahedron 59:8329–8336

    Article  CAS  Google Scholar 

  10. Hammer Ř, Harper DAT, Ryan PD (2001) PAST: Paleontological Statistics Software Package for Education and Data Analysis. Palaeontol Electron 4:9

    Google Scholar 

  11. Harada KI, Fujii K, Shimada T, Suzuki M, Sano H, Adachi K, Carmichael WW (1995) Two cyclic peptides, anabaenopeptins, a third group of bioactive compounds from the cyanobacterium Anabaena flos-aquae NRC 525-17. Tetrahedron Lett 36:1511–1514

    Article  CAS  Google Scholar 

  12. Hughes EO, Gorham PR, Zehnder A (1958) Toxicity of an unialgal culture of Microcystis aeruginosa. Can J Microbiol 4:225–236

    Article  PubMed  CAS  Google Scholar 

  13. Komarek J (1991) A review of water-bloom forming Microcystis species, with regard to populations from Japan. Algol Stud 64:115–127

    Google Scholar 

  14. Komarek J (1958) Die taxonomische revision der planktischen Blaualgen der Tschechoslowakei. In: Komarek J, Ettl H (eds) Algologische Studien. Nakl ČSAV, Praha, pp 10–206

    Google Scholar 

  15. Lee T, Tsuzuki M, Takeuchi T, Yokoyama K, Karube I (1994) In vivo fluorimetric method for early detection of cyanobacterial waterblooms. J Appl Phycol 6:489–495

    Article  Google Scholar 

  16. Lin L, Bitner R, Edlin G (1977) Increased reproductive fitness of Escherichia coli lambda lysogens. J Virol 21:554–559

    PubMed  CAS  Google Scholar 

  17. Manage PM, Kawabata Z, Nakano S (2001) Dynamics of cyanophage-like particles and algicidal bacteria causing Microcystis aeruginosa mortality. Limnology 2:73–78

    Article  Google Scholar 

  18. Manage PM, Kawabata Z, Nakano S (2000) Algicidal effect of the bacterium Alcaligenes denitrificans on Microcystis spp. Aquat Microb Ecol 22:111–117

    Article  Google Scholar 

  19. Manage PM, Kawabata Z, Nakano S (1999) Seasonal changes in densities of cyanophage infectious to Microcystis aeruginosa in a hypereutrophic pond. Hydrobiol 411:211–216

    Article  Google Scholar 

  20. Marahiel MA, Stachelhaus T, Mootz HD (1997) Modular peptide synthetases involved in nonribosomal peptide synthesis. Chem Rev 97:2651–2673

    Article  PubMed  CAS  Google Scholar 

  21. Namikoshi M, Rinehart KL (1996) Bioactive compounds produced by cyanobacteria. J Ind Microbiol 17:373–384

    Article  CAS  Google Scholar 

  22. Okino T, Matsuda H, Murakami M, Yamaguchi K (1993) Microginin, an angiotensin-converting enzyme inhibitor from the blue-green alga Microcystis aeruginosa. Tetrahedron Lett 34:501–504

    Article  CAS  Google Scholar 

  23. Padan E, Shilo M (1973) Cyanophages—viruses attacking blue-green algae. Bacteriol Rev 37:343–370

    PubMed  CAS  Google Scholar 

  24. Reshef V, Carmeli S (2006) New microviridins from a water bloom of the cyanobacterium Microcystis aeruginosa. Tetrahedron 62:7361–7369

    Article  CAS  Google Scholar 

  25. Reynolds CS (1984) The ecology of freshwater phytoplankton. University Press, Cambridge, p 384

    Google Scholar 

  26. Reynolds CS (1975) Interrelations of photosynthetic behaviour and buoyancy regulation in a natural population of a blue-green alga. Freshw Biol 5:323–338

    Article  Google Scholar 

  27. Rouhiainen L, Paulin L, Suomalainen S, Hyytiäinen H, Buikema W, Haselkorn R, Sivonen K (2000) Genes encoding synthetases of cyclic depsipeptides, anabaenopeptilides, in Anabaena strain 90. Mol Microbiol 37:156–157

    Article  PubMed  CAS  Google Scholar 

  28. Sedmak B, Eleršek T (2006) Microcystins induce morphological and physiological changes in selected representative phytoplanktons. Microb Ecol 51:508–515

    Article  PubMed  CAS  Google Scholar 

  29. Sedmak B, Kosi G (2002) Harmful cyanobacterial blooms in Slovenia—bloom types and microcystin producers. ABS (Ljubljana) 45:1–17

    Google Scholar 

  30. Sedmak B, Kosi G (1998) The role of microcystins in heavy cyanobacterial bloom formation. J Plankton Res 20:691–708 [Erratum (1998) 20:1421]

    Article  CAS  Google Scholar 

  31. Sedmak B, Kosi G (1997) Microcystins in Slovene freshwaters (Central Europe)—first report. Nat Toxins 5:64–73

    PubMed  CAS  Google Scholar 

  32. Thompson AS, Rhodes JC, Pettman I (1988) Culture collection of algae and protozoa – catalogue of strains, 5th ed. Natural environment research council. Wilson, Kendal, Ambleside, UK, p 22

    Google Scholar 

  33. Tucker S, Pollard P (2005) Identification of cyanophage Ma-LBP and infection of the cyanobacterium Microcystis aeruginosa from an Australian subtropical lake by the virus. Appl Environ Microbiol 71:629–635

    Article  PubMed  CAS  Google Scholar 

  34. Tuomi P, Fagerbakke KM, Bratbak G, Heldal M (1995) Nutritional enrichment of a microbial community: the effects on activity, elemental composition, community structure and virus production. FEMS Microbiol Ecol 16:123–134

    Article  CAS  Google Scholar 

  35. Wilson WH, Carr NG, Mann NH (1996) The effect of phosphate status on the kinetics of cyanophage infection in the oceanic cyanobacterium Synechococcus sp. WH7803. J Phycol 32:506–516

    Article  CAS  Google Scholar 

  36. Wommack KE, Colwell RR (2000) Virioplankton: viruses in aquatic ecosystems. Microbiol Mol Biol Rev 64:69–114

    Article  PubMed  CAS  Google Scholar 

  37. Yamamoto Y, Nizuma S, Kuroda N, Sakamoto M (1993) Occurrence of heterotrophic bacteria causing lysis in a eutrophic lake. Jpn J Phycol 41:215–220

    CAS  Google Scholar 

  38. Yoshida T, Takashima Y, Tomaru Y, Shirai Y, Takao Y, Hiroshi S, Nagasaki K (2006) Isolation and characterisation of cyanophage infecting the toxic cyanobacterium Microcystis aeruginosa. Appl Env Microbiol 72:1239–1247

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This study was supported by the Ministry of Higher Education, Science and Technology, Slovenian Research Agency by Basic Research grant (J1–7376) “How cyclic cyanobacterial peptides affect biodiversity?”, party by Program P1-0245 and by Ministry of Defence (214-00-167/2003-30). We thank Professor Roger Pain for critical reading of the manuscript.

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Authors and Affiliations

  1. Laboratory of Ecotoxicology and Ecotoxinology, Department of Genetic Toxicology and Cancer Biology, National Institute of Biology Ljubljana, Večna pot 111, 1000, Ljubljana, Slovenia

    B. Sedmak & Tina Eleršek

  2. Raymond and Beverly Sackler Faculty of Exact Sciences, School of Chemistry, Tel Aviv University, Ramat Aviv, Tel Aviv, 69978, Israel

    S. Carmeli

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  1. B. Sedmak
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  2. S. Carmeli
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  3. Tina Eleršek
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Correspondence to B. Sedmak.

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Sedmak, B., Carmeli, S. & Eleršek, T. “Non-Toxic” Cyclic Peptides Induce Lysis of Cyanobacteria—An Effective Cell Population Density Control Mechanism in Cyanobacterial Blooms. Microb Ecol 56, 201–209 (2008). https://doi.org/10.1007/s00248-007-9336-9

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  • DOI: https://doi.org/10.1007/s00248-007-9336-9

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