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Ecotoxicology

, Volume 25, Issue 4, pp 745–758 | Cite as

The interactive effects of microcystin-LR and cylindrospermopsin on the growth rate of the freshwater algae Chlorella vulgaris

  • Carlos PinheiroEmail author
  • Joana Azevedo
  • Alexandre Campos
  • Vítor Vasconcelos
  • Susana Loureiro
Article

Abstract

Microcystin-LR (MC-LR) and cylindrospermopsin (CYN) are the most representative cyanobacterial cyanotoxins. They have been simultaneously detected in aquatic systems, but their combined ecotoxicological effects to aquatic organisms, especially microalgae, is unknown. In this study, we examined the effects of these cyanotoxins individually and as a binary mixture on the growth rate of the freshwater algae Chlorella vulgaris. Using the MIXTOX tool, the reference model concentration addition (CA) was selected to evaluate the combined effects of MC-LR and CYN on the growth of the freshwater green algae due to its conservative prediction of mixture effect for putative similar or dissimilar acting chemicals. Deviations from the CA model such as synergism/antagonism, dose-ratio and dose-level dependency were also assessed. In single exposures, our results demonstrated that MC-LR and CYN had different impacts on the growth rates of C. vulgaris at the highest tested concentrations, being CYN the most toxic. In the mixture exposure trial, MC-LR and CYN showed a synergistic deviation from the conceptual model CA as the best descriptive model. MC-LR individually was not toxic even at high concentrations (37 mg L−1); however, the presence of MC-LR at much lower concentrations (0.4–16.7 mg L−1) increased the CYN toxicity. From these results, the combined exposure of MC-LR and CYN should be considered for risk assessment of mixtures as the toxicity may be underestimated when looking only at the single cyanotoxins and not their combination. This study also represents an important step to understand the interactions among MC-LR and CYN detected previously in aquatic systems.

Keywords

Cyanotoxins Microcystin-LR Cylindrospermopsin Chlorella vulgaris Synergism Concentration addition 

Notes

Acknowledgments

This work was supported by the Portuguese Science Foundation (FCT) through CESAM: UID/AMB/50017/2013.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Amado LL, Monserrat JM (2010) Oxidative stress generation by microcystins in aquatic animals: why and how. Environ Int 36:226–235. doi: 10.1016/j.envint.2009.10.010 CrossRefGoogle Scholar
  2. Babica P, Bláha L, Maršálek B (2006) Exploring the natural role of microcystins—a review of effects on photoautotrophic organisms. J Phycol 42:9–20. doi: 10.1111/j.1529-8817.2006.00176.x CrossRefGoogle Scholar
  3. Babica P, Hilscherová K, Bártová K, Bláha L, Maršálek B (2007) Effects of dissolved microcystins on growth of planktonic photoautotrophs. Phycologia 46:137–142. doi: 10.2216/06-24.1 CrossRefGoogle Scholar
  4. Backhaus T, Arrhenius A, Blanck H (2004) Toxicity of a mixture of dissimilarly acting substances to natural algal communities: predictive power and limitations of independent action and concentration addition. Environ Sci Technol 38:6363–6370. doi: 10.1021/es0497678 CrossRefGoogle Scholar
  5. Banker R, Teltsch B, Sukenik A, Carmeli S (2000) 7-epicylindrospermopsin, a toxic minor metabolite of the cyanobacterium Aphanizomenon ovalisporum from Lake Kinneret, Israel. J Nat Prod 63:387–389CrossRefGoogle Scholar
  6. Bártová K, Hilscherová K, Babica P, Maršálek B, Bláha L (2011) Effects of microcystin and complex cyanobacterial samples on the growth and oxidative stress parameters in green alga Pseudokirchneriella subcapitata and comparison with the model oxidative stressor-herbicide paraquat. Environ Toxicol 26:641–648. doi: 10.1002/tox.20601 CrossRefGoogle Scholar
  7. B-Béres V et al (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 691:97–107. doi: 10.1007/s10750-012-1061-9 CrossRefGoogle Scholar
  8. Best JH, Pflugmacher S, Wiegand C, Eddy FB, Metcalf JS, Codd GA (2002) Effects of enteric bacterial and cyanobacterial lipopolysaccharides, and of microcystin-LR, on glutathione S-transferase activities in zebra fish (Danio rerio). Aquat Toxicol 60:223–231CrossRefGoogle Scholar
  9. Beyer D et al (2009) Cylindrospermopsin induces alterations of root histology and microtubule organization in common reed (Phragmites australis) plantlets cultured in vitro. Toxicon 54:440–449. doi: 10.1016/j.toxicon.2009.05.008 CrossRefGoogle Scholar
  10. Bláha L, Babica P, Maršálek B (2009) Toxins produced in cyanobacterial water blooms—toxicity and risks. Interdiscip Toxicol 2:36–41CrossRefGoogle Scholar
  11. Bláhová L, Oravec M, Maršálek B, Šejnohová L, Šimek Z, Bláha L (2009) The first occurrence of the cyanobacterial alkaloid toxin cylindrospermopsin in the Czech Republic as determined by immunochemical and LC/MS methods. Toxicon 53:519–524. doi: 10.1016/j.toxicon.2009.01.014 CrossRefGoogle Scholar
  12. Boedeker W, Drescher K, Altenburger R, Faust M, Grimme LH (1993) Combined effects of toxicants: the need and soundness of assessment approaches in ecotoxicology. Sci Total Environ 134(Supplement 2):931–939CrossRefGoogle Scholar
  13. Bogialli S, Bruno M, Curini R, Di Corcia A, Fanali C, Laganà A (2006) Monitoring algal toxins in lake water by liquid chromatography tandem mass spectrometry. Environ Sci Technol 40:2917–2923. doi: 10.1021/es052546x CrossRefGoogle Scholar
  14. Brient L, Lengronne M, Bormans M, Fastner J (2009) First occurrence of cylindrospermopsin in freshwater in France. Environ Toxicol 24:415–420. doi: 10.1002/tox.20439 CrossRefGoogle Scholar
  15. Chiswell RK, Shaw GR, Eaglesham G, Smith MJ, Norris RL, Seawright AA, Moore MR (1999) Stability of cylindrospermopsin, the toxin from the cyanobacterium, Cylindrospermopsis raciborskii: effect of pH, temperature, and sunlight on decomposition. Environ Toxicol 14:155–161CrossRefGoogle Scholar
  16. Codd GA, Bell SG, Kaya K, Ward CJ, Beattie KA, Metcalf JS (1999) Cyanobacterial toxins, exposure routes and human health. Eur J Phycol 34:405–415. doi: 10.1017/s0967026299002255 CrossRefGoogle Scholar
  17. Dittmann E, Wiegand C (2006) Cyanobacterial toxins—occurrence, biosynthesis and impact on human affairs. Mol Nutr Food Res 50:7–17. doi: 10.1002/mnfr.200500162 CrossRefGoogle Scholar
  18. Eaglesham GK et al (1999) Use of HPLC-MS/MS to monitor cylindrospermopsin, a blue-green algal toxin, for public health purposes. Environ Toxicol 14:151–154. doi: 10.1002/(sici)1522-7278(199902)14:1<151:aid-tox19>3.0.co;2-d CrossRefGoogle Scholar
  19. European Food Safety Authority (2015) Harmonisation of human and ecological risk assessment of combined exposure to multiple chemicalsGoogle Scholar
  20. Falconer IR (1999) An overview of problems caused by toxic blue-green algae (cyanobacteria) in drinking and recreational water. Environ Toxicol 14:5–12CrossRefGoogle Scholar
  21. Falconer IR, Humpage AR (2005) Cyanobacterial toxins of drinking water supplies: cylindrospermopsins and microcystins. CRC Press, Boca RatonGoogle Scholar
  22. Falconer IR, Humpage AR (2006) Cyanobacterial (blue-green algal) toxins in water supplies: cylindrospermopsins. Environ Toxicol 21:299–304. doi: 10.1002/tox.20194 CrossRefGoogle Scholar
  23. Fastner J, Neumann U, Wirsing B, Weckesser J, Wiedner C, Nixdorf B, Chorus I (1999) Microcystins (hepatotoxic heptapeptides) in German fresh water bodies. Environ Toxicol 14:13–22. doi: 10.1002/(sici)1522-7278(199902)14:1<13:aid-tox4>3.0.co;2-d CrossRefGoogle Scholar
  24. Fastner J et al (2007) Occurrence of the cyanobacterial toxin cylindrospermopsin in northeast Germany. Environ Toxicol 22:26–32. doi: 10.1002/tox.20230 CrossRefGoogle Scholar
  25. Ferreira ALG, Loureiro S, Soares A (2008) Toxicity prediction of binary combinations of cadmium, carbendazim and low dissolved oxygen on Daphnia magna. Aquat Toxicol 89:28–39. doi: 10.1016/j.aquatox.2008.05.012 CrossRefGoogle Scholar
  26. Freitas M, Azevedo J, Pinto E, Neves J, Campos A, Vasconcelos V (2015) Effects of microcystin-LR, cylindrospermopsin and a microcystin-LR/cylindrospermopsin mixture on growth, oxidative stress and mineral content in lettuce plants (Lactuca sativa L.). Ecotoxicol Environ Safe 116:59–67. doi: 10.1016/j.ecoenv.2015.02.002 CrossRefGoogle Scholar
  27. Froscio SM, Humpage AR, Burcham PC, Falconer IR (2001) Cell-free protein synthesis inhibition assay for the cyanobacterial toxin cylindrospermopsin. Environ Toxicol 16:408–412CrossRefGoogle Scholar
  28. Froscio SM, Humpage AR, Wickramasinghe W, Shaw G, Falconer IR (2008) Interaction of the cyanobacterial toxin cylindrospermopsin with the eukaryotic protein synthesis system. Toxicon 51:191–198. doi: 10.1016/j.toxicon.2007.09.001 CrossRefGoogle Scholar
  29. Gallo P, Fabbrocino S, Cerulo MG, Ferranti P, Bruno M, Serpe L (2009) Determination of cylindrospermopsin in freshwaters and fish tissue by liquid chromatography coupled to electrospray ion trap mass spectrometry. Rapid Commun Mass Spectrom 23:3279–3284. doi: 10.1002/rcm.4243 CrossRefGoogle Scholar
  30. Gantar M, Berry JP, Thomas S, Wang ML, Perez R, Rein KS (2008) Allelopathic activity among Cyanobacteria and microalgae isolated from Florida freshwater habitats. FEMS Microbiol Ecol 64:55–64. doi: 10.1111/j.1574-6941.2008.00439.x CrossRefGoogle Scholar
  31. Gulledge BM, Aggen JB, Huang HB, Nairn AC, Chamberlin AR (2002) The microcystins and nodularins: cyclic polypeptide inhibitors of PP1 and PP2A. Curr Med Chem 9:1991–2003CrossRefGoogle Scholar
  32. Humpage AR, Fontaine F, Froscio S, Burcham P, Falconer IR (2005) Cylindrospermopsin genotoxicity and cytotoxicity: role of cytochrome P-450 and oxidative stress. J Toxicol Environ Health A 68:739–753. doi: 10.1080/15287390590925465 CrossRefGoogle Scholar
  33. Jones GJ, Orr PT (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 28:871–876CrossRefGoogle Scholar
  34. Jonker MJ, Svendsen C, Bedaux JJM, Bongers M, Kammenga JE (2005) Significance testing of synergistic/antagonistic, dose level-dependent, or dose ratio-dependent effects in mixture dose-response analysis. Environ Toxicol Chem 24:2701–2713CrossRefGoogle Scholar
  35. Kearns KD, Hunter MD (2000) Green algal extracellular products regulate antialgal toxin production in a cyanobacterium. Environ Microbiol 2:291–297CrossRefGoogle Scholar
  36. Kearns KD, Hunter MD (2001) Toxin-producing Anabaena flos-aquae induces settling of Chlamydomonas reinhardtii, a competing motile alga. Microb Ecol 42:80–86Google Scholar
  37. Kemp A, John J (2006) Microcystins associated with Microcystis dominated blooms in the southwest wetlands, Western Australia. Environ Toxicol 21:125–130. doi: 10.1002/tox.20164 CrossRefGoogle Scholar
  38. Kinnear S (2010) Cylindrospermopsin: a decade of progress on bioaccumulation research. Mar Drugs 8:542–564. doi: 10.3390/md8030542 CrossRefGoogle Scholar
  39. Kokociński M, Dziga D, Spoof L, Stefaniak K, Jurczak T, Mankiewicz-Boczek J, Meriluoto J (2009) First report of the cyanobacterial toxin cylindrospermopsin in the shallow, eutrophic lakes of western Poland. Chemosphere 74:669–675. doi: 10.1016/j.chemosphere.2008.10.027 CrossRefGoogle Scholar
  40. Kotai J (1972) Instructions for the preparation of modified nutrient solution Z8 for algae. Norwegian Institute for Water Research, BlindernGoogle Scholar
  41. Lahti K, Rapala J, Färdig M, Niemelä M, Sivonen K (1997) Persistence of cyanobacterial hepatotoxin, microcystin-LR in particulate material and dissolved in lake water. Water Res 31:1005–1012CrossRefGoogle Scholar
  42. Lindsay J, Metcalf JS, Codd GA (2006) Protection against the toxicity of microcystin-LR and cylindrospermopsin in Artemia salina and Daphnia spp. by pre-treatment with cyanobacterial lipopolysaccharide (LPS). Toxicon 48:995–1001. doi: 10.1016/j.toxicon.2006.07.036 CrossRefGoogle Scholar
  43. Loureiro S, Svendsen C, Ferreira ALG, Pinheiro C, Ribeiro F, Soares A (2010) Toxicity of three binary mixtures to Daphnia magna: comparing chemical modes of action and deviations from conceptual models. Environ Toxicol Chem 29:1716–1726. doi: 10.1002/etc.198 CrossRefGoogle Scholar
  44. Mackintosh C, Beattie KA, Klumpp S, Cohen P, Codd GA (1990) Cyanobacterial microcystin-LR is a potent and specific inhibitor of protein phosphatases 1 and 2A from both mammals and higher plants. FEBS Lett 264:187–192CrossRefGoogle Scholar
  45. Máthé C et al (2007) Microcystin-LR, a cyanobacterial toxin, induces growth inhibition and histological alterations in common reed (Phragmites australis) plants regenerated from embryogenic calli. New Phytol 176:824–835. doi: 10.1111/j.1469-8137.2007.02230.x CrossRefGoogle Scholar
  46. Máthé C, M-Hamvas M, Vasas G (2013) Microcystin-LR and cylindrospermopsin Induced alterations in chromatin organization of plant cells. Mar Drugs 11:3689–3717. doi: 10.3390/md11103689 CrossRefGoogle Scholar
  47. Messineo V, Melchiorre S, Di Corcia A, Gallo P, Bruno M (2010) Seasonal succession of Cylindrospermopsis raciborskii and Aphanizomenon ovalisporum blooms with cylindrospermopsin occurrence in the volcanic lake Albano, Central Italy. Environ Toxicol 25:18–27. doi: 10.1002/tox.20469 Google Scholar
  48. Metcalf JS, Barakate A, Codd GA (2004) Inhibition of plant protein synthesis by the cyanobacterial hepatotoxin, cylindrospermopsin. FEMS Microbiol Lett 235:125–129. doi: 10.1016/j.femsle.2004.04.025 CrossRefGoogle Scholar
  49. Mohamed ZA (2008) Polysaccharides as a protective response against microcystin-induced oxidative stress in Chlorella vulgaris and Scenedesmus quadricauda and their possible significance in the aquatic ecosystem. Ecotoxicology 17:504–516. doi: 10.1007/s10646-008-0204-2 CrossRefGoogle Scholar
  50. Monserrat JM, Pinho GLL, Yunes JS (2003) Toxicological effects of hepatotoxins (microcystins) on aquatic organisms. Comments on Toxicology 9:89–101CrossRefGoogle Scholar
  51. Munkegaard M, Abbaspoor M, Cedergreen N (2008) Organophosphorous insecticides as herbicide synergists on the green algae Pseudokirchneriella subcapitata and the aquatic plant Lemna minor. Ecotoxicology 17:29–35. doi: 10.1007/s10646-007-0173-x CrossRefGoogle Scholar
  52. Nagata S, Tsutsumi T, Hasegawa A, Yoshida F, Ueno Y, Watanabe MF (1997) Enzyme immunoassay for direct determination of microcystins in environmental water. J AOAC Int 80:408–417Google Scholar
  53. Neumann C, Bain P, Shaw G (2007) Studies of the comparative in vitro toxicology of the cyanobacterial metabolite deoxycylindrospermopsin. J Toxicol Environ Health A 70:1679–1686. doi: 10.1080/15287390701434869 CrossRefGoogle Scholar
  54. Norris RL et al (1999) Deoxycylindrospermopsin, an analog of cylindrospermopsin from Cylindrospermopsis raciborskii. Environ Toxicol 14:163–165CrossRefGoogle Scholar
  55. Norris RLG et al (2002) Hepatic xenobiotic metabolism of cylindrospermopsin in vivo in the mouse. Toxicon 40:471–476CrossRefGoogle Scholar
  56. Nováková K, Bláha L, Babica P (2012) Tumor promoting effects of cyanobacterial extracts are potentiated by anthropogenic contaminants—Evidence from in vitro study. Chemosphere 89:30–37CrossRefGoogle Scholar
  57. OECD (2006) OECD Guidelines for the testing of chemicals 201, freshwater alga and cyanobacteria, growth inhibition test. OECD, ParisCrossRefGoogle Scholar
  58. Oehrle SA, Southwell B, Westrick J (2010) Detection of various freshwater cyanobacterial toxins using ultra-performance liquid chromatography tandem mass spectrometry. Toxicon 55:965–972. doi: 10.1016/j.toxicon.2009.10.001 CrossRefGoogle Scholar
  59. Olmstead AW, LeBlanc GA (2005) Toxicity assessment of environmentally relevant pollutant mixtures using a heuristic model. Integr Environ Assess Manag 1:114–122. doi: 10.1897/ieam_2004-005r.1 CrossRefGoogle Scholar
  60. Ou DY, Song LR, Gan NQ, Chen W (2005) Effects of microcystins on and toxin degradation by Poterioochromonas sp. Environ Toxicol 20:373–380. doi: 10.1002/tox.20114 CrossRefGoogle Scholar
  61. Paerl HW, Huisman J (2008) Climate—blooms like it hot. Science 320:57–58. doi: 10.1126/science.1155398 CrossRefGoogle Scholar
  62. Paerl HW, Huisman J (2009) Climate change: a catalyst for global expansion of harmful cyanobacterial blooms. Environ Microbiol Rep 1:27–37. doi: 10.1111/j.1758-2229.2008.00004.x CrossRefGoogle Scholar
  63. Paerl HW, Paul VJ (2012) Climate change: links to global expansion of harmful cyanobacteria. Water Res 46:1349–1363. doi: 10.1016/j.watres.2011.08.002 CrossRefGoogle Scholar
  64. Pereira S, Saker ML, Vale M, Vasconcelos VM (2009) Comparison of sensitivity of grasses (Lolium perenne L. and Festuca rubra L.) and lettuce (Lactuca sativa L.) exposed to water contaminated with microcystins. Bull Environ Contam Toxicol 83:81–84. doi: 10.1007/s00128-009-9763-z CrossRefGoogle Scholar
  65. Pflugmacher S (2004) Promotion of oxidative stress in the aquatic macrophyte Ceratophyllum demersum during biotransformation of the cyanobacterial toxin microcystin-LR. Aquat Toxicol 70:169–178. doi: 10.1016/j.aquatox.2004.06.010 CrossRefGoogle Scholar
  66. Pflugmacher S, Wiegand C, Oberemm A, Beattie KA, Krause E, Codd GA, Steinberg CEW (1998) Identification of an enzymatically formed glutathione conjugate of the cyanobacterial hepatotoxin microcystin-LR: the first step of detoxication. Biochim Biophys Acta 1425:527–533CrossRefGoogle Scholar
  67. Pflugmacher S, Codd GA, Steinberg CEW (1999) Effects of the cyanobacterial toxin microcystin-LR on detoxication enzymes in aquatic plants. Environ Toxicol 14:111–115CrossRefGoogle Scholar
  68. Pinheiro C, Azevedo J, Campos A, Loureiro S, Vasconcelos V (2013) Absence of negative allelopathic effects of cylindrospermopsin and microcystin-LR on selected marine and freshwater phytoplankton species. Hydrobiologia 705:27–42. doi: 10.1007/s10750-012-1372-x CrossRefGoogle Scholar
  69. Pires LMD, Sarpe D, Brehm M, Ibelings BW (2011) Potential synergistic effects of microcystins and bacterial lipopolysaccharides on life history traits of Daphnia galeata raised on low and high food levels. Aquat toxicol 104:230–242CrossRefGoogle Scholar
  70. Preuβel 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 8:645–650. doi: 10.1016/j.hal.2008.10.009 CrossRefGoogle Scholar
  71. Prieto A, Campos A, Cameán A, Vasconcelos V (2011) Effects on growth and oxidative stress status of rice plants (Oryza sativa) exposed to two extracts of toxin-producing cyanobacteria (Aphanizomenon ovalisporum and Microcystis aeruginosa). Ecotoxicol Environ Saf 74:1973–1980. doi: 10.1016/j.ecoenv.2011.06.009 CrossRefGoogle Scholar
  72. Quesada A, Moreno E, Carrasco D, Paniagua T, Wormer L, De Hoyos C, Sukenik A (2006) Toxicity of Aphanizomenon ovalisporum (Cyanobacteria) in a Spanish water reservoir. Eur J Phycol 41:39–45. doi: 10.1080/09670260500480926 CrossRefGoogle Scholar
  73. Rücker J, Stüken A, Nixdorf B, Fastner J, Chorus I, Wiedner C (2007) Concentrations of particulate and dissolved cylindrospermopsin in 21 Aphanizomenon-dominated temperate lakes. Toxicon 50:800–809. doi: 10.1016/j.toxicon.2007.06.019 CrossRefGoogle Scholar
  74. Runnegar M, Berndt N, Kong SM, Lee EYC, Zhang LF (1995a) In vivo and in vitro binding of microcystin to protein phosphatase 1 and 2A. Biochem Biophys Res Commun 216:162–169CrossRefGoogle Scholar
  75. Runnegar MT, Kong SM, Zhong YZ, Lu SC (1995b) Inhibition of reduced glutathione synthesis by cyanobacterial alkaloid cylindrospermopsin in cultured rat hepatocytes. Biochem Pharmacol 49:219–225CrossRefGoogle Scholar
  76. Sedmak B, Eleršek T (2006) Microcystins induce morphological and physiological changes in selected representative phytoplanktons. Microb Ecol 51:508–515. doi: 10.1007/s00248-006-9045-9 CrossRefGoogle Scholar
  77. Sedmak B, Kosi G (1998) The role of microcystins in heavy cyanobacterial bloom formation. J Plankton Res 20:691–708CrossRefGoogle Scholar
  78. Spoof L et al (2006) First observation of cylindrospermopsin in Anabaena lapponica isolated from the boreal environment (Finland). Environ Toxicol 21:552–560. doi: 10.1002/tox.20216 CrossRefGoogle Scholar
  79. Terao K et al (1994) Electron microscopic studies on experimental poisoning in mice induced by cylindrospermopsin isolated from blue-green alga Umezakia natans. Toxicon 32:833–843CrossRefGoogle Scholar
  80. Tsuji K, Naito S, Kondo F, Ishikawa N, Watanabe MF, Suzuki M, Harada K (1994) Stability of microcystins from cyanobacteria: effect of light on decomposition and isomerization. Environ Sci Technol 28:173–177CrossRefGoogle Scholar
  81. van Apeldoorn ME, van Egmond HP, Speijers GJA, Bakker GJI (2007) Toxins of cyanobacteria. Mol Nutr Food Res 51:7–60. doi: 10.1002/mnfr.200600185 CrossRefGoogle Scholar
  82. Vasas G, Gáspár A, Páger C, Surányi G, Máthé C, Hamvas MM, Borbely G (2004) Analysis of cyanobacterial toxins (anatoxin-a, cylindrospermopsin, microcystin-LR) by capillary electrophoresis. Electrophoresis 25:108–115. doi: 10.1002/elps.200305641 CrossRefGoogle Scholar
  83. Wiegand C, Pflugmacher S (2005) Ecotoxicological effects of selected cyanobacterial secondary metabolites a short review. Toxicol Appl Pharmacol 203:201–218. doi: 10.1016/j.taap.2004.11.002 CrossRefGoogle Scholar
  84. Wormer L, Cirés S, Carrasco D, Quesada A (2008) Cylindrospermopsin is not degraded by co-occurring natural bacterial communities during a 40-day study. Harmful Algae 7:206–213. doi: 10.1016/j.ha1.2007.07.004 CrossRefGoogle Scholar
  85. Wörmer L, Huerta-Fontela M, Cirés S, Carrasco D, Quesada A (2010) Natural photodegradation of the cyanobacterial toxins microcystin and cylindrospermopsin. Environ Sci Technol 44:3002–3007. doi: 10.1021/es9036012 CrossRefGoogle Scholar
  86. Zurawell RW, Chen HR, Burke JM, Prepas EE (2005) Hepatotoxic cyanobacteria: a review of the biological importance of microcystins in freshwater environments. J Toxicol Env Health B Crit Rev 8:1–37. doi: 10.1080/10937400590889412 CrossRefGoogle Scholar

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© Springer Science+Business Media New York 2016

Authors and Affiliations

  1. 1.Departamento de Biologia & CESAMUniversidade de AveiroAveiroPortugal
  2. 2.Centro Interdisciplinar de Investigação Marinha e Ambiental, CIIMAR/CIMARPortoPortugal
  3. 3.Escola Superior de Tecnologia da Saúde do PortoVila Nova de GaiaPortugal
  4. 4.Departamento de BiologiaFaculdade de Ciências da Universidade do PortoPortoPortugal

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