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We studied the toxicity of a glyphosate formulation and provide evidence of metabolic alterations due to oxidative stress caused in a Chlorella kessleri tolerant strain by exposure to the herbicide. After 96h of exposure to increasing concentrations of the herbicide (0-70mgL-1) with alkylaryl polyglycol ether surfactant, growth was inhibited (EC50-96h 55.62mgL-1). Glyphosate increased protein and malondialdehyde content which was significantly higher than in the control at 50-70mgL-1. Superoxide dismutase and catalase activities and reduced glutathione levels increased in a concentration-dependant manner. Morphological studies showed increases in vacuolisation and in cell and sporangia sizes. The glyphosate formulation studied has a cytotoxic effect on C. kessleri through a mechanism that would involve the induction of oxidative stress. Upon glyphosate exposure, oxidative stress parameters such as SOD and CAT activities and MDA level could be more sensitive biomarkers than usually tested growth parameters in C. kessleri. © 2010 Elsevier Inc.


Documento: Artículo
Título:Oxidative stress induced by a commercial glyphosate formulation in a tolerant strain of Chlorella kessleri
Autor:Romero, D.M.; Ríos de Molina, M.C.; Juárez, Á.B.
Filiación:Laboratorio de Enzimología, Estrés Oxidativo y Metabolismo, Departamento de Química Biológica, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Argentina
Consejo Nacional de Investigaciones Científicas y Técnicas, Buenos Aires, Argentina
Departamento de Biodiversidad y Biología Experimental, Departamento de Química Biológica, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Intendente Güiraldes 2160, C1428EGA Buenos Aires, Argentina
Palabras clave:Antioxidant defences; Chlorella kessleri; Glyphosate; Microalgae; Oxidative stress; algal protein; biological marker; catalase; glutathione; glyphosate; malonaldehyde; superoxide dismutase; surfactant; biomarker; concentration (composition); ecotoxicology; enzyme activity; free radical; glyphosate; green alga; inhibition; microalga; oxidation; pollution exposure; surfactant; algal growth; antioxidant activity; article; biomass; cell size; cell structure; cell vacuole; Chlorella; Chlorella kessleri; chlorophyll content; controlled study; cytotoxicity test; enzyme activity; growth inhibition; growth rate; herbicide tolerance; lipid peroxidation; nonhuman; oxidative stress; plant cell; plant metabolism; protein content; sensitivity analysis; sporangium; Biological Markers; Catalase; Chlorella; Glutathione; Glutathione Peroxidase; Glutathione Reductase; Glycine; Herbicides; Lipid Peroxidation; Malondialdehyde; Oxidative Stress; Superoxide Dismutase; Thiobarbituric Acid Reactive Substances; Water Pollutants, Chemical; Parachlorella kessleri
Página de inicio:741
Página de fin:747
Título revista:Ecotoxicology and Environmental Safety
Título revista abreviado:Ecotoxicol. Environ. Saf.
CAS:catalase, 9001-05-2; glutathione, 70-18-8; glyphosate, 1071-83-6; malonaldehyde, 542-78-9; superoxide dismutase, 37294-21-6, 9016-01-7, 9054-89-1; Biological Markers; Catalase,; Glutathione, 70-18-8; Glutathione Peroxidase,; Glutathione Reductase,; Glycine, 56-40-6; Herbicides; Malondialdehyde, 542-78-9; Superoxide Dismutase,; Thiobarbituric Acid Reactive Substances; Water Pollutants, Chemical; glyphosate, 1071-83-6


  • Aebi, H., Catalase in vitro (1984) Methods Enzymol., 105, pp. 121-126
  • Ahsan, N., Lee, D.G., Lee, K.W., Alam, I., Lee, S.H., Bahk, J.D., Lee, B.H., Glyphosate-induced oxidative stress in rice leaves revealed by proteomic approach (2008) Plant Physiol. Biochem., 46, pp. 1062-1070
  • Amorós, I., Alonso, J.L., Romaguera, S., Carrasco, J.M., Assessment of toxicity of a glyphosate-based formulation using bacterial systems in lake water (2007) Chemosphere, 67, pp. 2221-2228
  • Bagchi, D., Bagchi, M., Hassoun, E.A., Stohs, S.J., In vitro and in vivo generation of reactive oxygen species, DNA damage and lactate dehydrogenase leakage by selected pesticides (1995) Toxicology, 104, pp. 129-140
  • Baker-Austin, C., Dopson, M., Life in acid: pH homeostasis in acidophiles (2007) TRENDS Microbiol., 15, pp. 165-171
  • Beauchamp, C., Fridovich, I., Superoxide dismutase: improved assays and an assay applicable to acrylamide gels (1971) Anal. Biochem., 44, pp. 276-286
  • Bischoff, H.W., Bold, H.C., (1963) Phycological Studies IV. Some Soil Algae from Enchanted Rock and Related Algal Species, , Univ. Texas Publ. 6318, 1-95 p
  • Borggaard, O.K., Gimcing, A.L., Fate of glyphosate in soil and the possibility of leaching to ground and surface water: a review (2008) Pest Manage. Sci., 64, pp. 441-456
  • Bradford, M.M., A rapid and sensitive method for the quantitation of micrograms quantities utilizing the principle of protein dye binding (1976) Anal. Biochem., 72, pp. 248-254
  • Chaufan, G., Juárez, A., Basack, S., Ithuralde, E., Sabatini, S.E., Genovese, G., Oneto, M.L., Ríos de Molina, M.C., Toxicity of hexachlorobenzene and its transference from microalgae (Chlorella kessleri) to crabs (Chasmagnatus granulatus) (2006) Toxicology, 227, pp. 262-270
  • Coleman, F.O.D., Blake-Kalff, M.M.A., Davies, T.E., Detoxification of xenobiotics by plants: chemical modification and vacuolar compartmentation (1997) Trends Plant Sci., 2, pp. 144-151
  • Contardo-Jara, V., Klingelmann, E., Wiegand, C., Bioaccumulation of glyphosate and its formulation Roundup Ultra in Lumbricus variegatus and its effects on biotransformation and antioxidant enzymes (2009) Environ. Pollut., 157, pp. 57-63
  • Costa, M.J., Monteiro, D.A., Oliveira-Neto, A.L., Rantin, F.T., Kalinin, A.L., Oxidative stress biomarkers and heart function in bullfrog tadpoles exposed to Roundup Original® (2008) Ecotoxicology, 17, pp. 153-163
  • De Lorenzo, M.E., Scott, G.I., Ross, P.E., Toxicity of pesticides to aquatic microorganisms: a review (2001) Environ. Toxicol. Chem., 20, pp. 84-98
  • Dixon, D.P., Cummins, I., Cole, D.J., Edwards, R., Glutathione-mediated detoxification systems in plants (1998) Curr. Opin. Plant Biol., 1, pp. 258-266
  • Duke, S.O., Glyphosate (1988) Herbicides: Chemistry, Degradation and Mode of Action, pp. 1-58. , Marcel Dekker, New York, P.C. Kearney, D.D. Kaufman (Eds.)
  • Hodges, D.M., Delong, J.M., Forney, C.F., Prange, R.K., Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and others interfering compounds (1999) Planta, 207, pp. 604-611
  • Jain, M., Bhalla-Sarin, N., Glyphosate-induced increase in glutathione S-transferase activity and glutathione content in groundnut (Arachis hypogea L.) (2001) Pest. Biochem. Physiol., 69, pp. 143-152
  • Jamers, A., De Coen, W., Effect assessment of the herbicide paraquat on a green alga using differential gene expression and biochemical biomarkers (2010) Environ. Toxicol. Chem., 29, pp. 893-901
  • Janero, D.R., Malondialdehyde and thiobarbituric acid-reactivity as diagnostic indices of lipid peroxidation and peroxidative tissue injury (1990) Free Radic. Biol. Med., 9, pp. 515-540
  • Juárez, A.B., Barsanti, L., Passarelli, V., Evangelista, V., Vesentini, N., Conforti, V., Gualtieri, P., In vivo microspectroscopy monitoring of chromium effects on the photosynthetic and photoreceptive apparatus of Eudorina unicocca and Chlorella kessleri (2008) J. Environ. Monit., 10, pp. 1313-1318
  • Juárez, A.B., Vélez, C.G., Sobre la presencia de Chlorella kessleri (Chlorococcales, Chlorophyceae) en el Complejo Termal Copahue (Neuquén, Argentina) (1993) Bol. Soc. Argent. Bot., 29, pp. 105-107
  • Kjaer, J., Olsen, P., Ullum, M., Grant, R., Leaching of glyphosate and aminomethylphosphonic acid from Danish agricultural field sites (2005) J. Environ. Qual., 34, pp. 608-620
  • Kolpin, D.W., Thurman, E.M., Lee, E.A., Meyer, M.T., Furlong, E.T., Glassmeyer, S.T., Urban contribution of glyphosate and its degradate AMPA to streams in the United States (2006) Sci. Total Environ, 354, pp. 191-197
  • Lei, A., Hu, Z., Wong, Y., Tam, N.F., Antioxidant responses of microalgal species to pyrene (2006) J. Appl. Phycol., 18, pp. 67-78
  • Lewis, M.A., Use of freshwater plants for phytotoxicity testing: a review (1995) Environ. Pollut., 87, pp. 319-336
  • Lichtenthaler, H.K., Chlorophylls and Carotenoids: pigments of photosynthetic biomembranes (1987) Methods Enzymol., 148, pp. 349-382
  • Ma, J., Wang, S., Wang, P., Ma, L., Chen, X., Xu, R., Toxicity assessment of 40 herbicides to the green alga Raphidocelis subcapitata (2006) Ecotoxicol. Environ. Saf., 63, pp. 456-462
  • Ma, J., Xu, L., Wang, S., Zheng, R., Jin, S., Huang, S., Huang, Y., Toxicity of 40 herbicides to the green alga Chlorella vulgaris (2002) Ecotoxicol. Environ. Saf., 51, pp. 128-132
  • McCormic, P.V., Cairns, J., Algal indicators of aquatic ecosystem condition and change (1997) Plants for Environmental Studies, pp. 177-208. , Lewish Publishers, W. Wuncheng, J.W. Gorsuch, J.S. Hughes (Eds.)
  • Melis, A., Dynamics of photosynthetic membrane composition and function (1991) Biochim. Biophys. Acta, 1058, pp. 87-106
  • Okamoto, O.K., Pinto, E., Latorre, L.R., Bechara, E.J.H., Colepicolo, P., Antioxidant modulation in response to metal-induced oxidative stress in algal chloroplasts (2001) Arch. Environ. Contam. Toxicol., 40, pp. 18-24
  • Öncel, I., Keles, Y., Ustün, A.S., Interactive effects of temperature and heavy metal stress on the growth and some biochemical compounds in wheat seedlings (2000) Environ. Pollut., 107, pp. 315-320
  • Pätsikkä, E., Aro, E.M., Tyystjarvi, E., Increase in the quantum yield of photoinhibition contributes to copper toxicity in vivo (1998) Plant Physiol., 117, pp. 619-627
  • Peixoto, F., Comparative effects of the Roundup and glyphosate on mitochondrial oxidative phosphorylation (2005) Chemosphere, 61, pp. 115-1122
  • Peruzzo, P.J., Porta, A.A., Ronco, A.E., Levels of glyphosate in surface waters, sediments and soils associated with direct sowing soybean cultivation in north pampasic region of Argentina (2008) Environ. Pollut., 156, pp. 61-66
  • Pettersson, M., Ekelund, N.G., Effects of the herbicides roundup and Avans on Euglena gracilis (2006) Arch. Environ. Contam. Toxicol., 50, pp. 175-181
  • Pintilie, M., Oprica, L., Surleac, M., Dragut Ivan, C., Creanga, D.E., Artenie, V., Enzyme activity in plants treated with magnetic liquid (2006) Rom. J. Phys., 51, pp. 239-244
  • Rai, L.C., Rai, P.K., Mallick, N., Regulation of heavy metal toxicity in acid-tolerant Chlorella: physiological and biochemical approaches (1996) Environ. Exp. Bot., 36, pp. 99-109
  • Relyea, R.A., The impact of insecticides and herbicides on the biodiversity and productivity of aquatic communities (2005) Ecol. Appl., 15, pp. 618-627
  • Sabatini, S.E., Juárez, A.B., Eppis, M.R., Bianchi, L., Luquet, C.M., Ríos de Molina, M.C., Oxidative stress and antioxidant defenses in two green microalgae exposed to copper (2009) Ecotoxicol. Environ. Saf., 72, pp. 1200-1206
  • Sáenz, M., Di Marzio, W., Alberdi, J., Tortorelli, M., Effects of technical grade and a commercial formulation of glyphosate on algal population growth (1997) Bull. Environ. Contam. Toxicol., 59, pp. 638-644
  • Samuel, K., Bose, S., Bleaching of photosyntethic pigments in Chlorella protothecoides grown in the presence of SANDOZ 9785 (4-chloro-5 dimethylamino-2 phenyl-3 (H) pyridazione) (1987) J. Biosci., 12, pp. 399-404
  • Schiariti, A., Juárez, A.B., Rodríguez, M.C., Effects of sublethal concentrations of copper on three strains of green microalgae under autotrophic and mixotrophic culture conditions (2004) Arch. Hydrobiol., "Algol. Stud.", 114, pp. 143-157
  • Sobrero, M.C., Rimoldi, F., Ronco, A.E., Effects of the glyphosate active ingredient and a formulation on Lemna gibba L. at different exposure levels and assessment end-points (2007) Bull. Environ. Contam. Toxicol., 79, pp. 537-543
  • Struger, J., Thompson, D., Staznik, B., Martin, P., McDaniel, T., Marvin, C., Ocurrence of glyphosate in surface waters of Southern Ontario (2008) Bull. Environ. Contam. Toxicol., 80, pp. 378-384
  • Tsui, M.T., Chu, L.M., Aquatic toxicity of glyphosate-based formulations: comparison between different organisms and the effects of environmental factors (2003) Chemosphere, 52, pp. 1189-1197
  • Tukaj, S., Tukaj, Z., Distinct chemical contaminants induce the synthesis of Hsp70 proteins in green microalgae Desmodesmus subspicatus: heat pretreatment increases cadmium resistance (2010) J. Therm. Biol., 35, pp. 239-244
  • Uotila, M., Gullner, G., Komives, T., Induction of glutathione S-transferase activity and glutathione levels in plants exposed to glyphosate (1995) Physiol. Plant., 93, pp. 689-694
  • (2002), USEPA, Short term methods for estimating the chronic toxicity of effluents and receiving waters to freshwater organism, 4th ed. EPA-821-R-02-013. Washington, DC; Vavilin, D.V., Ducruet, J.M., Matorin, D.N., Venediktov, P.S., Rubin, A.B., Membrane lipid peroxidation, cell viability and Photosystem II activity in the green alga Chlorella pyrenoidosa subjected to various stress conditions (1998) J. Photochem. Photobiol., 42, pp. 233-239
  • Vendrell, E., Gómez de Barreda Ferraz, D., Sabater, C., Carrasco, J.M., Effect of glyphosate on growth of four freshwater species of phytoplankton: a microplate bioassay (2009) Bull. Environ. Contam. Toxicol., 82, pp. 538-542
  • Venrick, E.L., How many cells to count? (1978) Phytoplankton Manual, Monographs on oceanographic methodology, pp. 167-180. , UNESCO Press, Paris, A. Sournia (Ed.)
  • Wong, P.K., Effects of 2,4-D, glyphosate and paraquat on growth, photosynthesis and chlorophyll-a synthesis of Scenedesmus quadricauda Berb 614 (2000) Chemosphere, 41, pp. 177-182


---------- APA ----------
Romero, D.M., Ríos de Molina, M.C. & Juárez, Á.B. (2011) . Oxidative stress induced by a commercial glyphosate formulation in a tolerant strain of Chlorella kessleri. Ecotoxicology and Environmental Safety, 74(4), 741-747.
---------- CHICAGO ----------
Romero, D.M., Ríos de Molina, M.C., Juárez, Á.B. "Oxidative stress induced by a commercial glyphosate formulation in a tolerant strain of Chlorella kessleri" . Ecotoxicology and Environmental Safety 74, no. 4 (2011) : 741-747.
---------- MLA ----------
Romero, D.M., Ríos de Molina, M.C., Juárez, Á.B. "Oxidative stress induced by a commercial glyphosate formulation in a tolerant strain of Chlorella kessleri" . Ecotoxicology and Environmental Safety, vol. 74, no. 4, 2011, pp. 741-747.
---------- VANCOUVER ----------
Romero, D.M., Ríos de Molina, M.C., Juárez, Á.B. Oxidative stress induced by a commercial glyphosate formulation in a tolerant strain of Chlorella kessleri. Ecotoxicol. Environ. Saf. 2011;74(4):741-747.