Skip to main content
Log in

Homoserine-lactones and microcystin in cyanobacterial assemblages in Swiss lakes

  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

To learn more whether toxin formation by cyanobacteria is controlled by quorum sensing, the concentrations of microcystins and of homoserine lactones have been followed during a summer period in the deep mesotrophic Lake Zürich and in the shallow eutrophic Lake Muzzano. Specific cyanobacterial populations are present in both lakes, Planktothrix rubescens dominates in Lake Zürich, Microcystis wesenbergii in Lake Muzzano. Both organisms produced microcystins, and homoserine-lactones were detected as well in most of the samples. However, no clear relation between the concentrations of the two compounds was observed with sampling intervals of 2 weeks.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Bachofen, R. & A. Schenk, 1998. Quorum sensing autoinducers: Do they play a role in natural microbial habitats?. Microbiol. Res. 153: 61–63.

    CAS  Google Scholar 

  • Beattie, K. A. & G. A. Codd, 1995. Action of ultraviolet irradiation on microcystin-LR. In: Kaas, H. (ed.), 1st Int. Congr. Toxic Cyanobacteria. Rönne, Denmark, p. 5.

    Google Scholar 

  • Bell, S. G. & G. A. Codd, 1994. Cyanobacterial toxins and human health. Rev. Med. Microbiol. 5: 256–264.

    Google Scholar 

  • Berg, K., W. W. Carmichael, O. M. Skulberg, C. Benestad & B. Underdal, 1987. Investigation of a toxic water-bloom of Microcystis aeruginosa (Cyanophyceae) in lake Akersvatn, Norway. Hydrobiologia 144: 97–103.

    CAS  Google Scholar 

  • Blom, J. F., J. A. Robinson & F. Jüttner, 2001. High grazer toxicity of [D-Asp3, (E)-Dhb7]microcystin-RR of Planktotrix rubescens as compared to different microcystins. Toxicon 39: 1923–1932.

    Article  CAS  PubMed  Google Scholar 

  • Carmichael, W. W., 1992. Cyanobacteria secondary metabolites-the cyanotoxins. J. Appl. Bacteriol. 72: 445–459.

    CAS  PubMed  Google Scholar 

  • Carmichael, W. W., 1996. Toxic Microcystis and the environment. In Watanabe, M.F., K. I. Harada, W. W. Carmichael & H. Fujiki (eds), Toxic Microcystis. CRC Press, Boca Raton, N.Y.: 1–11.

    Google Scholar 

  • Christoffersen, K., S. Lyck & A. Winding, 2002. Microbial activity and bacterial community structure during degradation of microcystins. Aquat. Microbial. Ecol. 27: 125–136.

    Google Scholar 

  • Dittmann, E., M. Erhard, M. Kaebernick, Ch. Scheler. B. A. Neilan. H. von Döhren & T. Borner, 2001. Altered expression of two light-dependent genes in a microcystin-lacking mutant of Microcystis aeruginosa PCC 7806. Microbiology-SGM 147: 3113–3119.

    CAS  Google Scholar 

  • Dong, Y. H., J. L. Xu, X. Z. Li & L. H. Zhang, 2000. AiiA, an enzyme that inactivates the acylhomoserine lactone quorumsensing signal and attenuates the virulence of Erwinia carotovora. Proc. Natn. Acad. Sci. 97: 3526–3531.

    Article  CAS  Google Scholar 

  • Dong, Y. H., L. H. Wang, J. L. Xu, H. B. Zhang, X. F. Zhang & L. H. Zhang, 2001. Quenching quorum-sensing-dependent bacterial infection by an N-acyl homoserine lactonase. Nature 411: 813–817.

    Article  CAS  PubMed  Google Scholar 

  • Fastner, J., M. Erhard, W.W. Carmichael, F. Sun, K. L. Rinehart, H. Rönicke & I. Chorus, 1999. Characterization and diversity of microcystins in natural blooms and strains of the genera Microcystis and Planktothrix from German freshwaters. Arch. Hydrobiol. 145: 147–163.

    CAS  Google Scholar 

  • Harada K. I., K. Tsuji, M. F. Watanabe & F. Kondo, 1996. Stability of microcystins from cyanobacteria: III. Effect of pH and temperature. Phycologia. 35: 83–88.

    Article  Google Scholar 

  • Isenburg, C., M. Bottinelli, M. Tonolla & R. Peduzzi, 2000. Aspetti limnologici e microbiologici des laghetto di Muzzano (Ti). Bollettino Societa Scienze naturali 88: 41–51.

    Google Scholar 

  • Jones, G. J. & P. T. Orr, 1994. Release and degradation of microcystin following algicide treatment of a Microcystis aeruginosa bloom in a recreational lake, as determined by HPLC and protein phosphatase inhibition assay. Wat. Res. 28: 871–876.

    Article  CAS  Google Scholar 

  • Kaebernick, M., B. A. Neilan, T. Börner & E. Dittmann, 2000. Light and the transcriptional response of the Microcystin biosynthesis gene cluster. Appl. Environ. Microbiol. 66: 3387–3392.

    Article  CAS  PubMed  Google Scholar 

  • Kiviranta, J., K. Sivonen, K. Lahti, R. Luukkainen & S. I. Niemela, 1991. Production and biodegradation of cyanobacterial toxins-a laboratory study. Arch. Hydrobiol. 121: 281–294.

    CAS  Google Scholar 

  • Kotak, B. G, A. K. Lam, E. E. Prepas & S. E. Hrudey, 2000. Role of chemical and physical variables in regulating microcystin-LR concentration in phytoplankton of eutrophic lakes. Can. J. Fish. Aquat. Sci. 57: 1584–1593.

    Article  CAS  Google Scholar 

  • Lahti, K., J. Rapala, M. Färdig, M. Niemelä, & K. Sivonen, 1997. Persistence of cyanobacterial hepatotoxin, microcystin-LR in particulate material and dissolved in lake water. Wat. Res. 31: 1005–1012.

    Article  CAS  Google Scholar 

  • Lam, A. K. Y., E. E. Prepas, D. Spinach, & S. E. Hrudey, 1995. Chemical control of hepatotoxic phytoplankton blooms: implications for human health. Water Res. 29: 1845–1854.

    Article  CAS  Google Scholar 

  • Lawton, L. A., C. Edwards & G. A. Codd, 1994. Extraction and high-performance liquid chromatographic method for the determination of microcystins in raw and treated waters. Analyst 119: 1525–1530.

    Article  CAS  PubMed  Google Scholar 

  • Leadbetter, J. R. & E. P. Greenberg, 2000. Metabolism of acylhomoserine lactone quorum-sensing signals by Variovorax paradoxus. J. Bacteriol. 182: 6921–6926.

    Article  CAS  PubMed  Google Scholar 

  • Long, B. M., G. J. Jones & P. T. Orr, 2001. Cellular microcystin content in N-limited Microcystis aeruginosa can be predicted from growth rate. Appl. Environm. Microbiol. 67: 278–283.

    Article  CAS  Google Scholar 

  • McClean, K. H., M. K. Winson, L. Fish, A. Taylor, S. R. Chhabra, M. Camara, M. Daykin, J. H. Lamb, S. Swift, B. W. Bycroft, G. S. A. Stewart, & P. Williams, 1997. Quorum sensing and Chromobacterium violaceum: exploitation of violacein production and inhibition for the detection of N-acyl homoserine-lactones. Microbiology-SGM 143: 3703–3711.

    Article  CAS  Google Scholar 

  • McLean, R. L. C., M. Whiteley, D. J. Stickler & W. C. Fuqua, 1997. Evidence of autoinducer activity in naturally occurring biofilms. FEMS Microbiol. Letters 154: 259–263.

    Article  CAS  Google Scholar 

  • Micheletti, S., F. Schanz & A. E. Walsby, 1998. The daily integral of photosynthesis by Planktothrix rubescens during summer stratification and autumnal mixing in Lake Zürich. New Phytol. 139: 233–246.

    Article  Google Scholar 

  • Miller, M. B. & B. L. Bassler, 2001. Quorum sensing in bacteria. Annu. Rev. Microbiol. 55: 165–199.

    Article  CAS  PubMed  Google Scholar 

  • Oh, H. M., S. J. Lee, M. H. Jang & B. D. Yoon, 2000. Microcystin production by Microcystis aeruginosa in a phosphorus-limited chemostat. Appl. Environm. Microbiol. 66: 176–179.

    Article  CAS  Google Scholar 

  • Orr, P. T. & G. J. Jones, 1998. Relationship between microcystin production and cell division rates in nitrogen-limited Microcystis aeruginosa cultures. Limnol. & Oceanogr. 43: 1604–1614.

    CAS  Google Scholar 

  • Ostensvik, O., O. M. Skulberg, B. Underdal & V. Hormazabal, 1998. Antibacterial properties of extracts from selected planktonic freshwater cyanobacteria-a comparative study of bacterial bioassays. J. Appl. Microbiol. 84: 1117–1124.

    Article  CAS  PubMed  Google Scholar 

  • Park, H. D., M. F. Watanabe, K. I. Harada, H. Nagai, M. Suzuki, M. Watanabe & H. Hayashi, 1993. Hepatotoxin (microcystin) and neurotoxin (anatoxin-a) contained in natural blooms and strains of cyanobacteria from Japanese freshwaters. Natural Toxins 1: 353–360.

    CAS  PubMed  Google Scholar 

  • Paerl, H. W. & D. F. Millie, 1996. Physiological ecology of toxic aquatic cyanobacteria. Phycologia 35: 160–167.

    Article  Google Scholar 

  • Prepas, E. E. & F. H. Rigler, 1982. Improvements in quantifying the phosphorus concentration in lakes water. Can. J. Aquat. Sci. 39: 822–829.

    CAS  Google Scholar 

  • Schanz, F., 1985. Vertical light attenuation and phytoplankton development in Lake Zürich. Limnol. & Oceanogr. 30: 299–310.

    Article  CAS  Google Scholar 

  • Swift, S., J. A. Downie, N.A. Whitehead, A. M. L. Barnard, G. P. C. Salmond & P. Williams, 2001. Quorum sensing as a population-density-dependent determinant of bacterial physiology. Adv. Microbial Physiol. 45: 199–270.

    Article  CAS  Google Scholar 

  • Tsuji, K., S. Nalto, F. Kondo, N. Ishiwaka, M. F. Watanabe, M. Suzuki & K. I. Harada, 1994. Stability of microcystins from cyanobacteria I: Effect of light on decomposition and isomerization. Environ. Sci. Technol. 28: 173–177.

    Article  CAS  Google Scholar 

  • Tsuji, K., T. Watanuki, F. Kondo, N. Ishiwaka, M. F. Watanabe, S. Suzuki, H. Nakazawa, M. Suzuki, & K. I. Harada, 1995. Stability of microcystins from cyanobacteria II: Effect of UV light on decomposition and isomerization. Toxicon 33: 1619–1631.

    Article  CAS  PubMed  Google Scholar 

  • Utkilen, H. & N. Gjølme, 1992. Toxin production by Microcystis aeruginosa as a function of light in continuous cultures and its ecological significance. Appl. Environ. Microbiol. 58: 1321–1325.

    CAS  PubMed  Google Scholar 

  • Vezie, C., L. Brient, K. Sivonen, G. Bertru. J. C. Lefeuvre & M. Salkinoja-Salonen, 1997. Occurrence of microcystin-containing cyanobacterial blooms in freshwaters of Brittany. Arch. Hydrobiol. 139: 401–413.

    CAS  Google Scholar 

  • Vining, L. C., 1990. Functions of secondary metabolites. Annu. Rev. Microbiol. 44: 395–427.

    CAS  PubMed  Google Scholar 

  • Watanabe, M. F., K. I. Harada, K. Matsuura, M. Watanabe, & M. Suzuki, 1989. Heptapeptide toxin production during the batch culture of two Microcystis species (Cyanobacteria). J. Appl. Phycol. 1: 161–165.

    Google Scholar 

  • Wiedner, C., P. M. Visser, J. Fastner, J. S. Metcalf, G. A. Codd & L. R. Mur, 2003. Effects of light on the microcystin content of Microcystis Strain PCC 7806. Appl. Environm. Microbiol. 69: 1475–1481.

    CAS  Google Scholar 

  • Whitehead, N. A., A. M. L. Barnard, H. Slater, N. J. L. Simpson & G. P. C. Salmond. 2001. Quorum sensing in Gram-negative bacteria. FEMS Microbiology Revs. 25: 365–404.

    CAS  Google Scholar 

  • Williams, P., T. J. Baldwin, & J. A. Downie. 1999. Bacterial crosstalk-communication between bacteria, plant, and animal cell. In England, R., G. Hobbs, N. Baiton & D. Mcl Roberts (eds), Microbial Signaling and Communication. Society for General Microbiology Symp. 57: 1–32.

  • Winson, M. K., S. Swift, L. Fish, J. P. Throup, F. Jørgensen, S. R. Chhabra, B. W. Bycroft, P. Williams & G. S. A. B. Stewart, 1998. Construction and analysis of lux CDABE-based plasmids sensors for investigating N-acyl homoserine lactone-mediated quorum sensing. FEMS Microbiol. Lett. 163: 185–192.

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Braun, E., Bachofen, R. Homoserine-lactones and microcystin in cyanobacterial assemblages in Swiss lakes. Hydrobiologia 522, 271–280 (2004). https://doi.org/10.1023/B:HYDR.0000029968.70297.c3

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/B:HYDR.0000029968.70297.c3

Navigation