Investigation of heavy metal (Pb+) effect in presence of (Ca2+) on photosynthetic pigmentsand antioxidant enzymes activityof Entromorpha sp.
Subject Areas : GeneticBelghais Boyok 1 , Saeid Soltani 2 , Amene sadat Hashemi 3
1 - Department of Biology, Faculty of Science, Qaemshahr Branch, Islamic Azad University, Qaemshahr, Iran.
2 - Department of Biology, Faculty of Science, Qaemshahr Branch, Islamic Azad University, Qaemshahr, Iran.
3 - Departmentof Agriculture, University of Applied Science and Technology, Sari, Mazandaran, Iran
Keywords: Lead, Green algae, Antioxidant enzymes, Heavy metal, Enteromorpha,
Abstract :
Lead as one of the most expanded metals in environment, effects on human health. Besides, the biological absorption by algae leads to the reduction of heavy metal pollutions in aqueoussolutions. In this study, accumulation and bioabsorption of Pb+ on biochemical characteristics of green alga Entromorpha was investigated. For this purpose, effects of different concentrations of Pb2+ (0, 50, 100 and 150 µM Pb(SO4)2) in presence of two concentrations of Ca2+ (0 and 0.5 mM CaCl2) was studied in Entromorpha collected on Caspian Sea in two times of 3 and 8 days in random complete design with 4 replications for photosynthetic pigments content, membrane lipid peroxidation and antioxidant enzymes activity. The results indicated a decreasing rate of chlorophylla and b, total chlorophyll and carotenoid and also activity of polyphenoloxidase enzymewith increase of Pb2+ concentration and stress during. In membrane lipid peroxidation assay, malondialdehyde increased significantly by increase of Pb2+concentration. For these traits including chlorophyll, and carotenoid content and also membrane lipid peroxidation assay, effects of Pb2+ stress decreased by using CaCl2 treatment. The results of antioxidant assay showed that catalase, ascorbate peroxidase and peroxidase activities in both 3 and 8 days stress was high without CaCl2 treatment than using it. In general, the results of this study showed that Pb2+causes oxidative stress and biochemical changes in Enteromorpha green algae. Also, the presence of CaCl2 treatment reduces the effects of stress.
Arunakumara, K. and Zhang, X. (2009). Effects of heavy metals (Pb 2+ and Cd 2+) on the ultrastructure, growth and pigment contents of the unicellular cyanobacterium Synechocystis sp. PCC 6803. Chinese Journal of Oceanology and Limnology.27: 383-388.
Bajguz, A. (2010). An enhancing effect of exogenous brassinolide on the growth and antioxidant activity in Chlorella vulgaris cultures under heavy metals stress. Environmental and Experimental Botany.68: 175-179.
Cao, D.-j., Shi, X.-d., Li, H., Xie, P.-p., Zhang, H.-m., Deng, J.-w. and Liang, Y.-g. (2015). Effects of lead on tolerance, bioaccumulation, and antioxidative defense system of green algae, Cladophora. Ecotoxicology and Environmental Safety.112: 231-237.
Dao, L.H. and Beardall, J. (2016a). Effects of lead on growth, photosynthetic characteristics and production of reactive oxygen species of two freshwater green algae. Chemosphere.147: 420-429.
Dao, L.H. and Beardall, J. (2016b). Effects of lead on two green microalgae Chlorella and Scenedesmus: photosystem II activity and heterogeneity. Algal Research.16: 150-159.
Drazkiewicz, M. (1994). Chlorophyllase: occurrence, functions, mechanism of action, effects of external and internal factors. Photosynthetica. (Czech Republic).
Fodorpataki, L., and Bartha, L. (2008). Differential sensitivity of the photosynthetic apparatus of a freshwater green alga and of duckweed exposed to salinity and heavy metal stress. In Photosynthesis. Energy from the Sun. pp. 1451-1454.Springer.
Foyer, C.H., and Noctor, G. (2000). Tansley Review No. 112 Oxygen processing in photosynthesis: regulation and signalling. The New Phytologist.146: 359-388.
Heath, R.L., and Packer, L. (1968). Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Archives of Biochemistry and Biophysics. 125: 189-198.
Jaishankar, M., Tseten, T., Anbalagan, N., Mathew, B.B., and Beeregowda, K.N. (2014). Toxicity, mechanism and health effects of some heavy metals. Interdisciplinary Toxicology.7: 60-72.
Ji, L., Xie, S., Feng, J., Li, Y., and Chen, L. (2012). Heavy metal uptake capacities by the common freshwater green alga Cladophora fracta. Journal of Applied Phycology.24: 979-983.
Kuo, S., Lai, M.S., and Lin, C.W. (2006). Influence of solution acidity and CaCl2 concentration on the removal of heavy metals from metal-contaminated rice soils. Environmental Pollution.144: 918-925.
Küpper, H., Küpper, F., and Spiller, M. (1996). Environmental relevance of heavy metal-substituted chlorophylls using the example of water plants. Journal of Experimental Botany.47: 259-266.
Lamaia, C., Kruatrachuea, M., Pokethitiyooka, P., Upathamb, E.S., and Soonthornsarathoola, V. (2005). Toxicity and accumulation of lead and cadmium in the filamentous green alga Cladophorafracta (OF Muller ex Vahl) Kutzing: A laboratory study. Science Asia.31: 121-127.
Lichtenthaler, H.K., and Wellburn, A.R. (1983). Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Portland Press Limited.
Maraga, J.O., Kimaiyo, P.K., Kituyi, L., and Lutta, S. (2016). Biosorption of Cu+2 and Zn+2 Heavy Metal Ions from Test Solutions Using Green Algae Biosorbent. Scientific Research Journal. 4:13-19.
Mehta, S., and Gaur, J. (2005). Use of algae for removing heavy metal ions from wastewater: progress and prospects. Critical Reviews in Biotechnology.25: 113-152.
Morcillo, P., Esteban, M.Á., and Cuesta, A. (2016). Heavy metals produce toxicity, oxidative stress and apoptosis in the marine teleost fish SAF-1 cell line. Chemosphere.144: 225-233.
Nakano, Y., and Asada, K. (1981). Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant and Cell Physiology.22: 867-880.
Nicoli, M.C., Elizalde, B.E., Pitotti, A., and Lerici, C.R. (1991). Effect of sugars and maillard reaction products on polyphenol oxidase and peroxidase activity in food. Journal of Food Biochemistry.15: 169-184.
Okamoto, O., Pinto, E., Latorre, L., Bechara, E., and Colepicolo, P. (2001). Antioxidant modulation in response to metal-induced oxidative stress in algal chloroplasts. Archives of Environmental Contamination and Toxicology.40: 18-24.
Ouyang, H., Kong, X., He, W., Qin, N., He, Q., Wang, Y., Wang, R., and Xu, F. (2012). Effects of five heavy metals at sub-lethal concentrations on the growth and photosynthesis of Chlorella vulgaris. Chinese Science Bulletin.57: 3363-3370.
Pinto, E., Sigaud‐kutner, T., Leitao, M.A., Okamoto, O.K., Morse, D., and Colepicolo, P. (2003). Heavy metal–induced oxidative stress in algae. Journal of Phycology.39: 1008-1018.
Piotrowska-Niczyporuk, A., Bajguz, A., Talarek, M., Bralska, M., and Zambrzycka, E. (2015). The effect of lead on the growth, content of primary metabolites, and antioxidant response of green alga Acutodesmus obliquus (Chlorophyceae). Environmental Science and Pollution Research.22: 19112-19123.
Piotrowska-Niczyporuk, A., Bajguz, A., Zambrzycka-Szelewa, E., and Bralska, M. (2018). Exogenously applied auxins and cytokinins ameliorate lead toxicity by inducing antioxidant defence system in green alga Acutodesmus obliquus. Plant Physiology and Biochemistry.132: 535-546.
Posmyk, M., Kontek, R., and Janas, K. (2009). Antioxidant enzymes activity and phenolic compounds content in red cabbage seedlings exposed to copper stress. Ecotoxicology and Environmental Safety.72: 596-602.
Ratkevicius, N., Correa, J., and Moenne, A. (2003). Copper accumulation, synthesis of ascorbate and activation of ascorbate peroxidase in Enteromorpha compressa (L.) Grev.(Chlorophyta) from heavy metal‐enriched environments in northern Chile. Plant, Cell & Environment.26: 1599-1608.
Shaw, B., Sahu, S., and Mishra, R. (2004). Heavy metal induced oxidative damage in terrestrial plants. In: Heavy metal stress in plants. pp. 84-126.Springer.
Sofo, A., Scopa, A., Nuzzaci, M., and Vitti, A. (2015). Ascorbate peroxidase and catalase activities and their genetic regulation in plants subjected to drought and salinity stresses. International Journal of Molecular Sciences.16: 13561-13578.
Soto, P., Gaete, H., and Hidalgo, M.E. (2011). Assessment of catalase activity, lipid peroxidation, chlorophyll-a, and growth rate in the freshwater green algae Pseudokirchneriella subcapitata exposed to copper and zinc. Latin American Journal of Aquatic Research.39: 280-285.
Tabaraki, R., Nateghi, A., and Ahmady-Asbchin, S. (2014). Biosorption of lead (II) ions on Sargassum ilicifolium: Application of response surface methodology. International Biodeterioration & Biodegradation.93: 145-152.
Teoh, M.L., and Wong, S.W. (2018). Influence of lead on growth and physiological characteristics of a freshwater green alga Chlorella sp. Malaysian Journal of Science.37: 82-93.
Vetrivel, S.A., Diptanghu, M., Ebhin, M.R., Sydavalli, S., Gaurav, N., and Tiger, K.P. (2017). Green algae of the genus Spirogyra: A potential absorbent for heavy metal from coal mine water. Remediation Journal.27: 81-90.
Xiong, B., Zhang, W., Chen, L., Lin, K.F., Guo, M.J., Wang, W.L., Cui, X.H., Bi, H.S., and Wang, B. (2014). Effects of Pb (Ⅱ) exposure on Chlorella protothecoides and Chlorella vulgaris growth, malondialdehyde, and photosynthesis‐related gene transcription. Environmental Toxicology.29: 1346-1354.
Yalçın, S. (2014). The mechanism of heavy metal biosorption on green marine macroalga Enteromorpha linza. Clean–Soil, Air, Water.42: 251-259.
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Arunakumara, K. and Zhang, X. (2009). Effects of heavy metals (Pb 2+ and Cd 2+) on the ultrastructure, growth and pigment contents of the unicellular cyanobacterium Synechocystis sp. PCC 6803. Chinese Journal of Oceanology and Limnology.27: 383-388.
Bajguz, A. (2010). An enhancing effect of exogenous brassinolide on the growth and antioxidant activity in Chlorella vulgaris cultures under heavy metals stress. Environmental and Experimental Botany.68: 175-179.
Cao, D.-j., Shi, X.-d., Li, H., Xie, P.-p., Zhang, H.-m., Deng, J.-w. and Liang, Y.-g. (2015). Effects of lead on tolerance, bioaccumulation, and antioxidative defense system of green algae, Cladophora. Ecotoxicology and Environmental Safety.112: 231-237.
Dao, L.H. and Beardall, J. (2016a). Effects of lead on growth, photosynthetic characteristics and production of reactive oxygen species of two freshwater green algae. Chemosphere.147: 420-429.
Dao, L.H. and Beardall, J. (2016b). Effects of lead on two green microalgae Chlorella and Scenedesmus: photosystem II activity and heterogeneity. Algal Research.16: 150-159.
Drazkiewicz, M. (1994). Chlorophyllase: occurrence, functions, mechanism of action, effects of external and internal factors. Photosynthetica. (Czech Republic).
Fodorpataki, L., and Bartha, L. (2008). Differential sensitivity of the photosynthetic apparatus of a freshwater green alga and of duckweed exposed to salinity and heavy metal stress. In Photosynthesis. Energy from the Sun. pp. 1451-1454.Springer.
Foyer, C.H., and Noctor, G. (2000). Tansley Review No. 112 Oxygen processing in photosynthesis: regulation and signalling. The New Phytologist.146: 359-388.
Heath, R.L., and Packer, L. (1968). Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Archives of Biochemistry and Biophysics. 125: 189-198.
Jaishankar, M., Tseten, T., Anbalagan, N., Mathew, B.B., and Beeregowda, K.N. (2014). Toxicity, mechanism and health effects of some heavy metals. Interdisciplinary Toxicology.7: 60-72.
Ji, L., Xie, S., Feng, J., Li, Y., and Chen, L. (2012). Heavy metal uptake capacities by the common freshwater green alga Cladophora fracta. Journal of Applied Phycology.24: 979-983.
Kuo, S., Lai, M.S., and Lin, C.W. (2006). Influence of solution acidity and CaCl2 concentration on the removal of heavy metals from metal-contaminated rice soils. Environmental Pollution.144: 918-925.
Küpper, H., Küpper, F., and Spiller, M. (1996). Environmental relevance of heavy metal-substituted chlorophylls using the example of water plants. Journal of Experimental Botany.47: 259-266.
Lamaia, C., Kruatrachuea, M., Pokethitiyooka, P., Upathamb, E.S., and Soonthornsarathoola, V. (2005). Toxicity and accumulation of lead and cadmium in the filamentous green alga Cladophorafracta (OF Muller ex Vahl) Kutzing: A laboratory study. Science Asia.31: 121-127.
Lichtenthaler, H.K., and Wellburn, A.R. (1983). Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Portland Press Limited.
Maraga, J.O., Kimaiyo, P.K., Kituyi, L., and Lutta, S. (2016). Biosorption of Cu+2 and Zn+2 Heavy Metal Ions from Test Solutions Using Green Algae Biosorbent. Scientific Research Journal. 4:13-19.
Mehta, S., and Gaur, J. (2005). Use of algae for removing heavy metal ions from wastewater: progress and prospects. Critical Reviews in Biotechnology.25: 113-152.
Morcillo, P., Esteban, M.Á., and Cuesta, A. (2016). Heavy metals produce toxicity, oxidative stress and apoptosis in the marine teleost fish SAF-1 cell line. Chemosphere.144: 225-233.
Nakano, Y., and Asada, K. (1981). Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant and Cell Physiology.22: 867-880.
Nicoli, M.C., Elizalde, B.E., Pitotti, A., and Lerici, C.R. (1991). Effect of sugars and maillard reaction products on polyphenol oxidase and peroxidase activity in food. Journal of Food Biochemistry.15: 169-184.
Okamoto, O., Pinto, E., Latorre, L., Bechara, E., and Colepicolo, P. (2001). Antioxidant modulation in response to metal-induced oxidative stress in algal chloroplasts. Archives of Environmental Contamination and Toxicology.40: 18-24.
Ouyang, H., Kong, X., He, W., Qin, N., He, Q., Wang, Y., Wang, R., and Xu, F. (2012). Effects of five heavy metals at sub-lethal concentrations on the growth and photosynthesis of Chlorella vulgaris. Chinese Science Bulletin.57: 3363-3370.
Pinto, E., Sigaud‐kutner, T., Leitao, M.A., Okamoto, O.K., Morse, D., and Colepicolo, P. (2003). Heavy metal–induced oxidative stress in algae. Journal of Phycology.39: 1008-1018.
Piotrowska-Niczyporuk, A., Bajguz, A., Talarek, M., Bralska, M., and Zambrzycka, E. (2015). The effect of lead on the growth, content of primary metabolites, and antioxidant response of green alga Acutodesmus obliquus (Chlorophyceae). Environmental Science and Pollution Research.22: 19112-19123.
Piotrowska-Niczyporuk, A., Bajguz, A., Zambrzycka-Szelewa, E., and Bralska, M. (2018). Exogenously applied auxins and cytokinins ameliorate lead toxicity by inducing antioxidant defence system in green alga Acutodesmus obliquus. Plant Physiology and Biochemistry.132: 535-546.
Posmyk, M., Kontek, R., and Janas, K. (2009). Antioxidant enzymes activity and phenolic compounds content in red cabbage seedlings exposed to copper stress. Ecotoxicology and Environmental Safety.72: 596-602.
Ratkevicius, N., Correa, J., and Moenne, A. (2003). Copper accumulation, synthesis of ascorbate and activation of ascorbate peroxidase in Enteromorpha compressa (L.) Grev.(Chlorophyta) from heavy metal‐enriched environments in northern Chile. Plant, Cell & Environment.26: 1599-1608.
Shaw, B., Sahu, S., and Mishra, R. (2004). Heavy metal induced oxidative damage in terrestrial plants. In: Heavy metal stress in plants. pp. 84-126.Springer.
Sofo, A., Scopa, A., Nuzzaci, M., and Vitti, A. (2015). Ascorbate peroxidase and catalase activities and their genetic regulation in plants subjected to drought and salinity stresses. International Journal of Molecular Sciences.16: 13561-13578.
Soto, P., Gaete, H., and Hidalgo, M.E. (2011). Assessment of catalase activity, lipid peroxidation, chlorophyll-a, and growth rate in the freshwater green algae Pseudokirchneriella subcapitata exposed to copper and zinc. Latin American Journal of Aquatic Research.39: 280-285.
Tabaraki, R., Nateghi, A., and Ahmady-Asbchin, S. (2014). Biosorption of lead (II) ions on Sargassum ilicifolium: Application of response surface methodology. International Biodeterioration & Biodegradation.93: 145-152.
Teoh, M.L., and Wong, S.W. (2018). Influence of lead on growth and physiological characteristics of a freshwater green alga Chlorella sp. Malaysian Journal of Science.37: 82-93.
Vetrivel, S.A., Diptanghu, M., Ebhin, M.R., Sydavalli, S., Gaurav, N., and Tiger, K.P. (2017). Green algae of the genus Spirogyra: A potential absorbent for heavy metal from coal mine water. Remediation Journal.27: 81-90.
Xiong, B., Zhang, W., Chen, L., Lin, K.F., Guo, M.J., Wang, W.L., Cui, X.H., Bi, H.S., and Wang, B. (2014). Effects of Pb (Ⅱ) exposure on Chlorella protothecoides and Chlorella vulgaris growth, malondialdehyde, and photosynthesis‐related gene transcription. Environmental Toxicology.29: 1346-1354.
Yalçın, S. (2014). The mechanism of heavy metal biosorption on green marine macroalga Enteromorpha linza. Clean–Soil, Air, Water.42: 251-259.