Skip to main content

Advertisement

Log in

Microcystis toxigenic strains in urban lakes: a case of study in Mexico City

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

Microcystis is a bloom-forming, common cyanobacterium in urban lakes of Mexico City. To assess the presence of potentially cyanotoxin-producing Microcystis, molecular techniques were applied and acute toxicity bioassays were performed with Daphnia magna neonates exposed to cyanobacterial crude extracts. Toxigenic potential of isolated strains was inferred by amplifying the mcyA-Cd genes and their identity as Microcystis was confirmed through the 16S rDNA and phycocyanin operon amplification. Microcystins synthesized under culture conditions were quantified through ELISA. The acute toxicity bioassays revealed that mortality was independent from the cyanotoxin concentration in some strains; this suggests the presence of other metabolites (different from microcystins) that also exerted an important biological effect. Isolated strains had the mcyA-Cd gene and most of them produced variable amounts of microcystins in the culture conditions used, confirming their toxigenic potential. Results warn about possible toxic effect risks for aquatic biota, neighboring areas, visitors and users of these sites, due to the constant presence of these blooms in the studied water bodies.

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

  • Allers T, Lichten M (2000) A method for preparing genomic DNA that restrains branch migration of Holiday junctions. Nucleic Acid Res 28(2):e6

    Article  CAS  Google Scholar 

  • Alva-Martínez AF, Sarma SSS, Nandini S (2007) Effect of mixed diets (Cyanobacteria and green algae) on the population growth of the cladocerans Ceriodaphnia dubia and Moina macrocopa. Aquat Ecol 41:579–585

    Article  Google Scholar 

  • Babica P, Blaha L, Marsalek B (2006) Exploring the natural role of microcystins—a review of effects on photoautotrophic organisms. J Phycol 42:9–20

    Article  Google Scholar 

  • Benedetti S, Benvenuti F, Pagliarani S, Francogli S, Scoglio S, Canestrari F (2004) Antioxidant properties of a novel phycocyanin extract from the blue-green alga Aphanizomenon flos-aquae. Life Sci 75(19):2353–2362

    Article  CAS  Google Scholar 

  • Benzie J (2005) Cladocera: the genus Daphnia (including Daphniopsis) (Anomopoda: Daphniidae). Kenobi productions, Ghent. Backhuys Publishers, Leiden

    Google Scholar 

  • Best JH, Eddy FB, Codd GA (2001) 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 Physiol Biochem 24:171–178

    Article  CAS  Google Scholar 

  • Burýšková B, Hilscherová K, Babica P, Vrsková D, Marsálek B, Bláha L (2006) Toxicity of complex cyanobacterial samples and their fractions in Xenopus laevis embryos and the role of microcystins. Aquat Toxicol 80(4):346–354

    Article  CAS  Google Scholar 

  • Carmichael WW (1992) Cyanobacteria secondary metabolites—the cyanotoxins. J Appl Bacteriol 72:445–459

    CAS  Google Scholar 

  • Codd GA, Lindsay J, Young FM, Morrison LF, Metcalf JS (2005) Harmful cyanobacteria: from mass mortalities to management measures. In: Huisman J, Matthijs H, Visser P (eds) Harmful cyanobacteria. Springer, The Netherlands, pp 1–24

    Chapter  Google Scholar 

  • Dai M, Xie P, Liang G, Chen J, Lei H (2008) Simultaneous determination of microcystin-LR and its glutathione conjugate in fish tissues by liquid chromatography–tandem mass spectrometry. J Chromatogr B Analyt Technol Biomed Life Sci 862(1–2):43–50

    CAS  Google Scholar 

  • de Figueiredo DR, Azeiteiro UM, Esteves SM, Gonçalves FJM, Pereira MJ (2004) Microcystin producing blooms—a serious global Public Health issue. Ecotoxicol Environ Saf 59(2):151–163

    Article  CAS  Google Scholar 

  • Dittman E, Börner T (2005) Genetic contributions to the risk assessment of microcystin in the environment. Toxicol Appl Pharmacol 203:192–200

    Article  CAS  Google Scholar 

  • Falconer IR (2007) Cyanobacterial toxins present in Microcystis aeruginosa extracts—more than microcystins!. Toxicon 50(4):585–588

    Article  CAS  Google Scholar 

  • Gómez-Díaz M, Martínez-Jerónimo FF (2009) Modification of the acute toxic response of Daphnia magna Straus 1820 to Cr(VI) by the effect of varying saline concentrations (NaCl). Ecotoxicology 18:81–86

    Article  CAS  Google Scholar 

  • Gonçalves AMM, Castro BB, Pardal MA, Gonçalves F (2007) Salinity effects on survival and life history of two freshwater cladocerans (Daphnia magna and Daphnia longispina). Ann Limnol Int J Lim 43(1):13–20

    Article  Google Scholar 

  • Gustafsson S, Hansson LA (2004) Development of tolerance against toxic cyanobacteria in Daphnia. Aquat Ecol 38:37–44

    Article  Google Scholar 

  • Hisbergues M, Chriastiansen G, Rouhiainen L, Sivonen K, Börner T (2003) PCR-based identification of microcystin-producing genotypes of different cyanobacterial genera. Arch Microbiol 180:402–410

    Article  CAS  Google Scholar 

  • Keil C, Forchert A, Fastner J, Szewzyk U, Rotard W, Chorus I, Krätke R (2002) Toxicity and microcystin content of extracts from a Planktothrix bloom and two laboratory strains. Water Res 36(8):2133–2139

    Article  CAS  Google Scholar 

  • Kim SG, Rhee SK, Ahn CY, Ko SR, Choi GG, Bae JW, Park YH, Oh HM (2006) Determination of cyanobacterial diversity during algal blooms in Daechung Reservoir, Korea, on the basis of cpcBA intergenic spacer region analysis. Appl Environ Microbiol 72(5):3252–3258

    Article  CAS  Google Scholar 

  • Komárek J, Komárková-Legnerová J (2002) Contribution to the knowledge of planktic cyanoprokaryotes from Central Mexico. Preslia Praha 74:207–233

    Google Scholar 

  • Leflaive JP, Ten-Hage LC (2007) Algal and cyanobacterial secondary metabolites in freshwaters: a comparison of allelopathic compounds and toxins. Freshw Biol 52:199–214

    Article  CAS  Google Scholar 

  • Liu G, Qian Y, Dai S, Feng N (2008) Adsorption of microcystin LR and LW on suspended particulate matter (SPM) at different pH. Water Air Soil Pollut 192:67–76

    Article  CAS  Google Scholar 

  • Martínez-Jerónimo FF, Martínez-Jerónimo L (2007) Chronic effect of NaCl salinity on a freshwater strain of Daphnia magna Straus (Crustacea: Cladocera): a demographic study. Ecotoxicol Environ Saf 67:411–416

    Article  CAS  Google Scholar 

  • Martínez-Jerónimo F, Villaseñor R, Rios G, Espinosa-Chávez F (1994) Effect of food type and concentration on the survival, longevity, and reproduction of Daphnia magna. Hydrobiologia 287(2):207–214

    Google Scholar 

  • Mikalsen B, Boison G, Skulberg OM, Fastner J, Davies W, Gabrielsen TM, Rudi K, Jakobsen KS (2003) Natural variation in the microcystin synthetase operon mcyABC and impact on microcystin production in Microcystis strains. J Bacteriol 185(9):2774–2785

    Article  CAS  Google Scholar 

  • Mohamed ZA (2001) Accumulation of cyanobacterial hepatotoxins by Daphnia in some Egyptian irrigation canals. Ecotoxicol Environ Saf 50:4–8

    Article  CAS  Google Scholar 

  • Morris RJ, Williams DE, Luu HA, Holmes CFB, Andersen RJ, Calvert SE (2000) The adsorption of microcystin-LR by natural clay particles. Toxicon 38:303–308

    Article  CAS  Google Scholar 

  • Nandini S (2000) Responses of rotifers and cladocerans to Microcystis aeruginosa (Cyanophyceae): a demographic study. Aquat Ecol 34:227–242

    Article  Google Scholar 

  • Oberholster PJ, Botha AM, Cloete TE (2006) Toxic cyanobacterial blooms in a shallow, artificially mixed urban lake in Colorado, USA. Lakes Reserv Res Manag 11:111–123

    Article  CAS  Google Scholar 

  • OECD (1982) Eutrophication of waters. Monitoring assessment and control. OECD, Paris, France, p 154

    Google Scholar 

  • OECD (2004). Daphnia sp. Acute Immobilization Test, OECD Guideline for Testing of Chemicals No. 202. Organization for the Economical Cooperation and Development

  • Oliva-Martínez MG, Rodríguez-Rocha A, Lugo-Vázquez A, Sánchez-Rodríguez MR (2008) Composición y dinámica del fitoplancton en un lago urbano hipertrófico. Hidrobiológica 18(1):1–13

    Google Scholar 

  • Otsuka S, Suda S, Li R, Watanabe M, Oyaizu H, Matsumoto S, Watanabe MM (1999) Phylogenetic relationships between toxic and non-toxic strains of the genus Microcystis based on 16S to 23S internal transcribed spacer sequence. FEMS Microbiol Lett 172(1):15–21

    Article  CAS  Google Scholar 

  • Ouellette AJ, Handy SM, Wilhelm SW (2006) Toxic Microcystis is widespread in Lake Erie: PCR detection of toxin genes and molecular characterization of associated cyanobacterial communities. Microb Ecol 51(2):154–165

    Article  CAS  Google Scholar 

  • Palíková M, Krejcí R, Hilscherová K, Babica P, Navrátil S, Kopp R, Bláha L (2007) Effect of different cyanobacterial biomasses and their fractions with variable microcystin content on embryonal development of carp (Cyprinus carpio L.). Aquat Toxicol 81(3):312–318

    Article  CAS  Google Scholar 

  • Pietsch C, Wiegand C, Ame MV, Nicklisch A, Wunderlin D, Pflugmacher S (2001) The effects of a cyanobacterial crude extract on different aquatic organisms: evidence for cyanobacterial toxin modulating factors. Environ Toxicol 16:535–542

    Article  CAS  Google Scholar 

  • Prakash S, Lawton LA, Edwards C (2009) Stability of toxigenic Microcystis blooms. Harmful Algae 8(3):377–384

    Article  CAS  Google Scholar 

  • Prieto AI, Jos A, Pichardo S, Moreno I, Cameán AM (2006) Differential oxidative stress responses to microcystins LR and RR in intraperitoneally exposed tilapia fish (Oreochromis sp.). Aquat Toxicol 77:314–321

    Article  CAS  Google Scholar 

  • Rippka R (1988) Isolation and purification of cyanobacteria. Methods Enzymol 167:3–27

    Article  CAS  Google Scholar 

  • Rodríguez-Tovar AV, Ruiz-Medrano R, Herrera-Martínez A, Barrera-Figueroa BE, Hidalgo-Lara ME, Reyes-Márquez BE, Cabrera-Ponce JL, Valdés M, Xoconostle-Cázares B (2005) Stable genetic transformation of the ectomycorrhizal fungus Pisolithus tinctorius. J Microbiol Methods 63(1):45–54

    Article  CAS  Google Scholar 

  • Romay Ch, González R, Ledón N, Remirez D, Rimbau V (2003) C-phycocyanin: a biliprotein with antioxidant, anti-inflammatory and neuroprotective effects. Curr Protein Pept Sci 4(3):207–216

    Article  CAS  Google Scholar 

  • Saker ML, Fastner J, Dittmann E, Christiansen G, Vasconcelos VM (2005) Variation between strains of the cyanobacterium Microcystis aeruginosa isolated from a Portuguese river. J App Microbiol 99:749–757

    Article  CAS  Google Scholar 

  • Saker ML, Welker M, Vasconcelos VM (2007) Multiplex PCR for the detection of toxigenic cyanobacteria in dietary supplements produced for human consumption. Appl Microbiol Biotechnol 73(5):1136–1142

    Article  CAS  Google Scholar 

  • Sheng JW, He M, Shi HC (2007) A highly specific immunoassay for microcystin-LR detection based on a monoclonal antibody. Anal Chem Acta 603(1):111–118

    Article  CAS  Google Scholar 

  • Silva EIL (2003) Emergence of a Microcystis bloom in an urban water body, Kandy Lake, Sri Lanka. Curr Sci 85(6):723–725

    Google Scholar 

  • Sivonen K, Jones G (1999) Cyanobacterial toxins. In: Chorus I, Bartam J (eds) Toxic cyanobacteria in water. A guide to their public health consequences, monitoring and management. E and FN Spon, London, pp 41–111

    Google Scholar 

  • Sotero-Santos RB, Souza e Silva CR, Verani NF, Nonaka KO, Rocha O (2006) Toxicity of a cyanobacteria bloom in Barra Bonita Reservoir (Middle Tiete River, Sao Paulo, Brazil). Ecotoxicol Environ Saf 64:163–170

    Article  CAS  Google Scholar 

  • Stephan CE (1977) Methods for calculating an LC50. In: Mayer FI, Hamelink JL (eds) Aquatic toxicology and hazard evaluation. ASTM STP 634, American Society for Testing and Materials, Philadelphia, pp 65–84

    Chapter  Google Scholar 

  • Tillett D, Parker DL, Neilan BA (2001) Detection of toxigenicity by a probe for the microcystin synthetase A gene (mcyA) of the cyanobacterial genus Microcystis: comparison of toxicities with 16S rRNA and phycocyanin operon (Phycocyanin Intergenic Spacer) phylogenies. Appl Environ Microbiol 67(6):2810–2818

    Article  CAS  Google Scholar 

  • U. S. Environmental Protection Agency (2002) Methods for measuring the acute toxicity of effluents and receiving waters to freshwater and marine organisms. 5th Ed. EPA-821-R-02-012

  • Valdor R, Aboal M (2007) Effects of living cyanobacteria, cyanobacterial extracts and pure microcystins on growth and ultrastructure of microalgae and bacteria. Toxicon 49(6):769–779

    Article  CAS  Google Scholar 

  • Visser P, Ibelings B, Mur LR, Walsby A (2005) The ecophysiology of the harmful cyanobacterium Microcystis: features explaining its success and measures for its control. In: Huisman J, Matthijs HCP, Visser P (eds) Harmful cyanobacteria. Springer, Berlin, Germany, pp 109–142

    Chapter  Google Scholar 

  • Welker M, Maršálek B, Šejnohová L, von Döhren H (2006) Detection and identification of oligopeptides in Microcystis (cyanobacteria) colonies: toward an understanding of metabolic diversity. Peptides 27(9):2090–2103

    Article  CAS  Google Scholar 

  • WHO (1998). Cyanobacterial toxins: microcystin-LR. In: Guidelines for drinking water quality, 2nd edn, Addendum to Vol. 2. Health criteria and other supporting information. World Health Organization, Geneva, Switzerland, pp. 95–110

  • Wiegand C, Pflugmacher S (2005) Ecotoxicological effects of selected cyanobacterial secondary metabolites: a short review. Toxicol Appl Pharmacol 203:201–218

    Article  CAS  Google Scholar 

  • Yoshida M, Yoshida T, Satomi M, Takashima Y, Hosoda N, Hiroishi S (2008) Intra-specific phenotypic and genotypic variation in toxic cyanobacterial Microcystis strains. J Appl Microbiol 105(2):407–415

    Article  CAS  Google Scholar 

Download references

Acknowledgments

M. A. Arzate-Cárdenas thanks Consejo Nacional de Ciencia y Tecnología (CONACYT) for the fellowship to perform graduate studies (No. 205163). Authors thank the Instituto Politécnico Nacional (IPN) and, particularly, the Secretaría de Investigación y Posgrado, the Sistema de Estímulo al Desempeño de los Investigadores and the Comisión de Operación y Fomento de Actividades Académicas del IPN for the support received to perform this study. We also thank Ms. Ingrid Mascher for editorial assistance with the English version of this manuscript. Thanks are due to two anonymous reviewers for their critical observations and comments that improved substantially this paper.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Fernando Martínez-Jerónimo.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Arzate-Cárdenas, M.A., Olvera-Ramírez, R. & Martínez-Jerónimo, F. Microcystis toxigenic strains in urban lakes: a case of study in Mexico City. Ecotoxicology 19, 1157–1165 (2010). https://doi.org/10.1007/s10646-010-0499-7

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-010-0499-7

Keywords

Navigation