Skip to main content

Effects of purified microcystin-LR and cell extracts of Microcystis strains PCC 7813 and CYA 43 on cardiac function in brown trout (Salmo trutta) alevins

Abstract

Sub-lethal cardiac responses of brown trout alevins (Salmo trutta L.) were determined in response to aqueous extracts of the cyanobacterium Microcystis strains PCC 7813 (microcystins detectable by HPLC) and CYA 43 (no microcystins detectable by HPLC) and to the purified cyanobacterial hepatotoxin, microcystin-LR (MC-LR) at concentrations of 5, 50 and 500 μg microcystin-LR equivalents l−1. Responses were determined using a flow chamber and video camera attached to a low power microscope. Heart rate in brown trout alevins was acutely sensitive to cyanobacterial extracts and significant increases were observed within 15–60 sec of exposure to aqueous extracts, although no change was observed on exposure to purified MC-LR. Stroke volume increased in all treatments at 50 and 500 μg MC-LR equivalents l−1, which may, at least in part, have been due to vasodilation of the yolk-sac blood vessels. Cardiac output increased significantly at all three concentrations of cyanobacterial cell extracts but not at the lowest concentration of MC-LR, although the rate increased at levels at/or above 50 μg l−1. Increased heart rate, stroke volume and cardiac output occurred at environmentally relevant microcystin concentrations of Microcystis PCC 7813 and CYA 43 aqueous extracts.

This is a preview of subscription content, access via your institution.

References

  • Adams, W.H., Stoner, R.D., Adams, D.G., Slatkin, D.N. and Siegelman, H.W. 1985. Pathophysiologic effects of a toxic peptide from Microcystis aeruginosa. Toxicon 23: 441–447.

    Google Scholar 

  • Altimiras, J., Aissaoui, A. and Tort, L. 1995. Is the short-term modulation of heart rate in teleost fish physiologically significant? Assessment by spectral analysis techniques. Brazilian J. Med. Biol. Res. 28: 1197–1206.

    Google Scholar 

  • Barton, B.A. and Iwama, G.K. 1991. Physiological changes in fish from stress in aquaculture with emphasis on the response and effects of corticosteroids. Ann. Rev. Fish Dis. 1: 3–26.

    Google Scholar 

  • Bury, N.R., Eddy, F.B. and Codd, G.A. 1995. The effects of the cyanobacterium Microcystis aeruginosa, the cyanobacterial hepatotoxin microcystin-LR and ammonia on growth rate and ionic regulation of brown trout. J. Fish Biol. 46: 1042–1054.

    Google Scholar 

  • Bury, N.R., Flik, G., Eddy, F.B. and Codd, G.A. 1996a. The effects of cyanobacteria and the cyanobacterial toxin microcystin-LR on Ca2+ transport and Na+/K+-ATPase in Tilapia gills. J. Exp. Biol. 1499: 1319–1326.

    Google Scholar 

  • Bury, N.R., Eddy, F.B. and Codd, G.A. 1996b. Stress responses of brown trout, Salmo trutta L., to the cyanobacterium, Microcystis aeruginosa. Environ. Toxicol. Wat. Qual. 11: 187–193.

    Google Scholar 

  • Bury, N.R., McGeer, J.C., Eddy, F.B. and Codd, G.A. 1997. Liver damage in brown trout, Salmo trutta L. and rainbow trout, Oncorhynchus mykiss (Walbaum), following administration of the cyanobacterial hepatotoxin microcystin-LR via the dorsal aorta. J. Fish Dis. 20: 209–215.

    Google Scholar 

  • Bury, N.R., Codd, G.A., Wendelaar Bonga, S.E. and Flik, G. 1998a. Fatty acids from the cyanobacterium Microcystis aeruginosa with the effects on fish gill Na+/K+-ATPase activity. J. Exp. Biol. 201: 81–89.

    Google Scholar 

  • Bury, N.R., Newlands, A.D., Eddy, F.B. and Codd, G.A. 1998b. In vivo and in vitro intestinal transport of 3H-microcystin-LR, a cyanobacterial toxin, in rainbow trout (Oncorhynchus mykiss). Aquat. Toxicol. 42: 139–148.

    Google Scholar 

  • Carbis, C.R., Mitchell, G.F., Anderson, J.W. and McCauley, I. 1996. The effects of microcystins on the serum biochemistry of carp, Cyprinus carpio L., when the toxins are administered by gavage, immersion and intraperitoneal routes. J. Fish Dis. 19: 151–159.

    Google Scholar 

  • Dahlem, A.M., Hassan, A.S., Swanson, S.P., Carmichael, W.W. and Beasley, V.R. 1989. A model system for studying the bioavailablity of intestinally administered microcystin-LR, a hepatotoxic peptide from the cyanobacterium Microcystis aeruginosa. Pharmacol. Toxicol. 64: 177–181.

    Google Scholar 

  • Dalmo. R.A., Kjerstad, A.A., Arnesen, S.M., Tobias, P.S. and Bogwald, J. 2000. Bath exposure of Atlantic halibut (Hippoglossus hippoglossus L.) yolk sac larvae to bacterial lipopolysaccharide (LPS): absorption and distribution of the LPS and effect on fish survival. Fish Shellfish Immunol. 10: 107–128.

    Google Scholar 

  • de Oliveira Azevedo, S.M.F. and Carmouze, J-P. 1994. Une mortalité de poisson dans une lagune tropicale (Brésil) durant une période de dominance de Cyanophyceae. Coincidence ou conséquence ? Rev. Hydrobiol. Trop. 27: 265–272.

    Google Scholar 

  • Eckert, R., Randall, D. and Augustine, G. 1988. Animal Physiology 3ed. W.H. Freeman & Co., New York.

    Google Scholar 

  • Eddy, F.B., McGovern, L. and McGeer, J.C. 1999. Effect of a nitric oxide-releasing compound isosorbide dinitrate on development and cardiovascular physiology of rainbow trout (Oncorhynchus mykiss). Fish Physiol. Biochem. 21: 167–171.

    Google Scholar 

  • Eddy, F.B., McGovern, L., Acock, N. and McGeer, J.C. 2000. Cardiovascular responses of eggs, embryos and alevins of Atlantic salmon and rainbow trout to nitric oxide donors, sodium nitroprusside and isorbide dinitrate, and inhibitors of nitric oxide synthase, N-nitro-L-arginine methyl ester and aminoguanidine, following short-and long-term exposure. J. Fish Biol. 55A: 119–127.

    Google Scholar 

  • Eriksson, J.E., Hägerstrand, H. and Isomaa, B. 1987. Cell selective cytotoxicity of a peptide toxin from the cyanobacterium Microcystis aeruginosa. Biochim. Biophys. Acta. 930: 304–310.

    Google Scholar 

  • Falconer, I.R., Dornbusch, M., Moran, G. and Yeung, S.K. 1992. Effect of the cyanobacterial (blue-green algal) toxins from Microcystis aeruginosa on the isolated enterocytes from the chicken small intestine. Toxicon. 30: 790–793.

    Google Scholar 

  • Falconer, I., Bartram, J., Chorus, I., Kuiper-Goodman, T., Utkilen, H., Burch, M. and Codd, G.A. 1999. Safe Levels and Safe Practices. In: Toxic Cyanobacteria in Water: a Guide to their Public Health Consequences, Monitoring and Management. pp. 155–178. Edited by I. Chorus and J. Bartram. E & F NSpon. London and New York.

    Google Scholar 

  • Fuentes, J. and Eddy, F.B. 1996. Drinking rate in juvenile Atlantic salmon, Salmo salar L. fry in response to a nitric oxide donor, sodium nitroprusside and an inhibitor of angiotensin converting enzyme, enalapril. Fish Physiol. Biochem. 15: 65–69.

    Google Scholar 

  • Fuentes, J. and Eddy, F.B. 1998. Cardiovascular responses in vivo to angiotensin II and the peptide antagonist saralasin in rainbow trout Oncorhynchus mykiss. J. Exp. Biol. 201: 267–272.

    Google Scholar 

  • Gaete, V., Canelo, E., Lagos, N. and Zambrano, F. 1994. Inhibitory effects of Microcystis aeruginosa toxin on the ion pumps of the gill of freshwater fish. Toxicon 32: 121–127.

    Google Scholar 

  • Guyton, K., Bond, R., Romeo, C., Southern, R., Cochran, J., Teti, G. and Cook, J.A. 1999. Endotoxin-induced cross-tolerance to Gram-positive sepsis. J. Endotoxin Res. 5: 119–126.

    Google Scholar 

  • Johnston, N.A.L., Campagna, V.S., Hawkins, P.R. and Banens, R.J. 1994. Response of the eastern rainbowfish (Melanotaenia duboulayi) to toxic Microcystis aeruginosa. Aust. J. Mar. Freshwater. Res. 45: 917–923.

    Google Scholar 

  • Jones, G.J. and Orr, P.T. 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. Water Res. 28: 871–876.

    Google Scholar 

  • Jungi, T.W., Valentin-Wiegand, P. and Brcic, M. 1999. Differential induction of NO synthesis by Gram-positive and Gram-negative bacteria and their components in bovine monocyte derived macrophages. Microbial Pathogenesis 27: 43–55.

    Google Scholar 

  • Kotak, B.G., Semalulu, S., Fritz, D.L., Prepas, E.E., Hrudey, S.E. and Coppock, R.W. 1996. Hepatic and renal pathology of intraperitoneally administered microcystin-LR in rainbow trout (Oncorhynchus mykiss). Toxicon 34: 517–525.

    Google Scholar 

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

    Google Scholar 

  • Lehtimaki, J., Moisander, P., Sivonen, K. and Kononen, K. 1997. Growth, nitrogen fixation and nodularin production by two Baltic Sea cyanobacteria. Appl. Environ. Microbiol.63: 1647–1656.

    Google Scholar 

  • Mackenthun, K.M. and Herman, E.F. 1945. A heavy mortality of fishes resulting from the decomposition of algae in the Yahara River, Wisconsin. Trans. Am. Fish. Soc. 75: 175–180.

    Google Scholar 

  • Mailman, D., Self, A. and Henry, M. 1999. Time-and surgerydependent effects of lipopolysaccharide on gut, cardiovascular and nitric oxide functions. Shock 12: 208–214.

    Google Scholar 

  • McGeer, J.C. and Eddy, F.B. 1996. Effects of sodium nitroprusside on blood circulation, acid-base balance and ionic balance in rainbow trout: indications for nitric oxide induced vasodilation. Can. J. Zool. 74: 1211–1219.

    Google Scholar 

  • Noga, E.J. 1998. Toxic algae, fish kills and fish disease. Fish Pathol. 33: 337–342.

    Google Scholar 

  • O'Donnell, G.B., Smith, P.R., Kilmartin, J.J. and Moran, A.P. 1994. Uptake and fate of orally administered bacterial lipopolysaccharide in brown trout (Salmo trutta). Fish Shellfish Immunol. 4: 285–299.

    Google Scholar 

  • Oishi, S., Watanabe, M.F. and Hiraga, K. 1985. Acute toxicity of Microcystis aeruginosa and its cardiovascular effects. Japanese J. Pharmacol. 39: 315.

    Google Scholar 

  • Palikova, M., Kovaru, F., Navaritil, S., Kubala, L., Pesak, S. and Vajcova, V. 1998. The effects of pure microcystin-LR and biomass of blue-green algae on selected immunological indices of carp (Cyprinus carpio L.) and silver carp (Hypophthalmichthys molitrix Val.). Acta Vet. Brno 67: 265–272.

    Google Scholar 

  • Papendorf, O., Konig, G.M., Wright, A.D., Chorus, I. and Oberemm, A. 1997. Mueggelone a novel fish embryo-larval development inhibitor from the freshwater cyanobacterium Aphanizomenon flos-aquae. J. Nat. Prod. 60: 1298–1300.

    Google Scholar 

  • Pelluet, D. 1944. Criteria for the recognition of developmental stages in the salmon (Salmo salar). J. Morphol. 74: 395–407. Pickering, A.D. 1989. Environmental stress and the survival of brown trout, Salmo trutta. Freshwater Biol. 21: 47–55.

    Google Scholar 

  • Raziuddin, S., Siegelman, H.W. and Tornabene, T.G. 1983. Lipopolysaccharides of the cyanobacterium Microcystis aeruginosa. Eur. J. Biochem. 137: 333–336.

    Google Scholar 

  • Rodger, H.D., Turnbull, T., Edwards, C. and Codd, G.A. 1994. Cyanobacterial (blue-green algal) bloom associated pathology in brown trout, Salmo trutta L., in Loch Leven, Scotland. J. Fish Dis. 17: 177–181.

    Google Scholar 

  • Ruiter, D.J., van der Meulen, J., Brouwer, A., Hummel, M.J.R., Mauw, B.J., van der Ploeg, J.C.M. and Wisse, E. 1981. Uptake by liver cells of endotoxin following intravenous injection. Lab. Invest. 45: 38–45.

    Google Scholar 

  • Sivonen, K. 1990b. Effects of light, temperature, nitrate, orthophosphate and bacteria on growth of and hepatotoxin production by Oscillatoria aghardii strains. Appl. Environ. Microbiol. 56: 2658–2666.

    Google Scholar 

  • Sivonen, K. and Jones, G. 1999. Cyanobacterial Toxins. In: Toxic Cyanobacteria in Water: a Guide to their Public Health Consequences, Monitoring and Management. pp. 41–111. Edited by I. Chorus and J. Bartram. E & F.N. Spon. London and New York.

  • Takemura, S., Minamiyama, Y., Imaoka, S., Funae, Y., Hirohashi, K., Inoue, M. and Kinoshita, H. 1999. Hepatic cytochrome P450 is directly inactivated by nitric oxide, not by inflammatory cytokines, in the early phase of endotoxemia. J. Hepatol. 30: 1035–1044.

    Google Scholar 

  • Tencalla, F. and Dietrich, D. 1997. Biochemical characterization of microcystin toxicity in rainbow trout (Oncorhynchus mykiss). Toxicon 35: 583–595.

    Google Scholar 

  • Theiss, W.C., Carmichael, W.W., Wyman, J. and Bruner, R. 1988. Blood pressure and hepatocellular effects of the cyclic heptapeptide toxin produced by the freshwater cyanobacterium (bluegreen alga) Microcystis aeruginosa strain PCC 7820. Toxicon 26: 603–613.

    Google Scholar 

  • Toivola, D.M. and Eriksson, J.E. 1999. Toxins affecting cell signalling and alteration of cytoskeletal structure. Toxicology in vitro 13: 521–530.

    Google Scholar 

  • Toranzo, A.E., Nieto, F. and Barja, J.L. 1990. Mortality associated with a cyanobacterial bloom in farmed rainbow trout in Galicia (northwestern Spain). Bull. Eur. Assoc. Fish Pathol. 10: 106–107.

    Google Scholar 

  • Traylor, L.A. and Mayeux, P.R. 1997. Superoxide generation by renal proximal tubule nitric oxide synthase. Nitric Oxide: Biol. Chem. 1: 432–438.

    Google Scholar 

  • Weckesser, J. and Drews, G. 1979. Lipopolysaccharides of the photosynthetic prokaryotes. Ann. Rev. Microbiol. 33: 215–239.

    Google Scholar 

  • Weckesser, J. and Jurgens, U.J. 1988. Cell walls and external cell layers. Methods Enzymol. 167: 173–188.

    Google Scholar 

  • Whitelam, G.C. and Codd, G.A. 1983. Photoinhibition of photosynthesis in the cyanobacterium Microcystis aeruginosa. Planta 157: 561–566.

    Google Scholar 

Download references

Authors

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Best, J., Eddy, F. & Codd, G. Effects of purified microcystin-LR and cell extracts of Microcystis strains PCC 7813 and CYA 43 on cardiac function in brown trout (Salmo trutta) alevins. Fish Physiology and Biochemistry 24, 171–178 (2001). https://doi.org/10.1023/A:1014081827372

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1014081827372

  • bioassay
  • cardiac output
  • cyanobacteria
  • heart rate
  • stroke volume