Assessment of the effects of zinc on the growth and antioxidant enzymes in Scenedesmus ellipsoideus Chodat

Hediye Elif Kiliç, Hatice Tunca, Tuğba Ongun Sevindik, Ali Doğru

Paper category: Original research paper
Corresponding author: Hatice Tunca (
DOI: 10.2478/ohs-2019-0024
Received: 17/01/2019
Accepted: 11/03/2019
Full text: here

Citation (APA style): Elif Kiliç, H., Tunca, H., Ongun Sevindik, T., et al. (2019). Assessment of the effects of zinc on the growth and antioxidant enzymes in Scenedesmus ellipsoideus Chodat. Oceanological and Hydrobiological Studies, 48(3), pp. 270-278. Retrieved 3 Oct. 2019, from doi:10.2478/ohs-2019-0024


This study explores the activity of total superoxide dismutase (SOD), ascorbate peroxidase (APX) and glutathione reductase (GR), biomass accumulation and chlorophyll a content in Scenedesmus ellipsoideus Chodat grown under conditions of varying zinc (Zn) concentrations. In addition, the activity of different SOD isozymes (MnSOD, FeSOD and CuZnSOD) was measured separately to determine the intracellular extent of oxidative stress resulting from Zn toxicity. We found that the activity of FeSOD and MnSOD was induced by lower Zn concentration (2 μg ml<sup>−1</sup> and 4 μg ml<sup>−1</sup>, respectively), whereas CuZnSOD activity was not affected, which indicates that chloroplasts are the first location in S. ellipsoideus cells where superoxide accumulation is accelerated by Zn toxicity. The activity of total SOD and APX was significantly increased by moderate Zn concentrations, probably due to some oxidative stress caused by Zn toxicity. The higher level of Zn application, however, led not only to the inhibition of total SOD and APX activity, but also to the reduction of biomass accumulation and chlorophyll a content. As a result, it can be concluded that the accumulation of superoxide radicals and H<sub>2</sub>O<sub>2</sub> in S. ellipsoideus cells induced by Zn toxicity may be responsible for the reduced growth rate and the impairment of photosynthetic pigments.


Aravind, P. & Prasad, M.N.V. (2005). Modulation of cadmium-induced oxidative stress in Ceratophyllum demersum by zinc involves ascorbate-glutathione cycle and glutathione metabolism. Plant Physiol. Bioch. 43(2): 107–116. DOI: 10.1016/j.plaphy.2005.01.002.
Asada, K. (1994). Production and action of active oxygen species in photosynthesis tissues. In C.H. Foyer & P.M. Mullineaux (Eds.) Causes of photooxidative stress and amelioration of defense systems in plants (pp. 77–104). CRC Press Inc, Boca Raton, USA: Fla.
Assche, F.V. & Clijsters, H. (1990). Effects of metals on enzyme activity in plants. Plant Cell Environ. 13(3): 195–206. DOI: 10.1111/j.1365-3040.1990.tb01304.x.
Atici, T., Ahiska, S., Altindag, A. & Aydin, D. (2008). Ecological effects of some heavy metals (Cd, Pb, Hg, Cr) pollution of phytoplanktonic algae and zooplanktonic organisms in Sarıyar Dam Reservoir in Turkey. Afr. J. Biotechnol. 7(12): 1972–1977. DOI: 10.5897/AJB2008.000-5044.
ATSDR. (2005). Toxicological profile for zinc. US Department of Health and Human Services. Retrieved April 12, 2012, from
Bajguz, A. (2010). An enhancing effect of exogenous brassinolide on the growth and antioxidant activity in Chlorella vulgaris cultures under heavy metals stress. Environ. Exp. Bot. 68(2): 175–179. DOI: 10.1016/j.envexpbot.2009.11.003.
Baş, L. & Demet, Ö. (1992). Çevresel toksikoloji yönünden bazı ağır metaller. Ekoloji. 5: 42–46.
Benavides, M.P., Gallego, S.M. & Tomaro, M.L. (2005). Cadmium toxicity in plants. Braz. J. Plant Physiol. 17(1): 21–34. DOI: 10.1590/S1677-04202005000100003.
Beyer, W.F. & Fridovich, I. (1987). Assaying for superoxide dismutase activity: Some large consequences of minor changes in conditions. Anal. Biochem. 161: 559–566. DOI: 10.1016/0003-2697(87)90489-1.
Bowler, C., Montagu, M.V. & Inzé, D. (1992). Superoxide dismutase and stress tolerance. Annu. Rev. Plant Biol. 43(1): 83–116. DOI: 10.1146/annurev.pp.43.060192.000503.
Bradford, M.M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72: 248–254. DOI: 10.1016/0003-2697(76)90527-3.
Broadley, M.R., White, P.J., Hammond, J.P., Zelko, I. & Lux, A. (2007). Zinc in plants. New Phytol. 173(4): 677–702. DOI: 10.1111/j.1469-8137.2007.01996.x.
Cargnelutti, D., Tabaldi, L.A., Spanevello, R.M., Jucoski, G.O., Battisti, V. et al. (2006). Mercury toxicity induces oxidative stress in growing cucumber seedlings. Chemosphere 65(6): 999–1006. DOI: 10.1016/j.chemosphere.2006.03.037.
Chen, J., Shiyab, S., Han, F.X., Monts, D.L., Waggoner, C.A. et al. (2009). Bioaccumulation and physiological effects of mercury in Pteris vittata and Nephrolepis exaltata. Ecotoxicol. 18: 110–121. DOI: 10.1007/s10646-008-0264-3.
Cho, U.H. & Park, J.O. (2000). Mercury-induced oxidative stress in tomato seedlings. Plant Sci. 156(1): 1–9. DOI: 10.1016/S0168-9452(00)00227-2.
Choudhary, M., Jetley, U.K., Khan, M.A., Zutshi, S. & Fatma, T. (2007). Effect of heavy metal stress on proline, malondialdehyde, and superoxide dismutase activity in the cyanobacterium Spirulina platensis-S5. Ecotox. Environ. Safe. 66(2): 204–209. DOI: 10.1016/j.ecoenv.2006.02.002.
Dundar, M.S. & Altundag, H. (2007). Investigation of heavy metal contaminations in the lower Sakarya river water and sediments. Environ. Monit. Assess. 128(1–3): 177–181. DOI: 10.1007/s10661-006-9303-9.
Duruibe, J.O., Ogwuegbu, M.O.C. & Egwurugwu, J.N. (2007). Heavy metal pollution and human biotoxic effects. Int. J. Phys. Sci. 2(5): 112–118.
Edreva, A. (2005). Generation and scavenging of reactive oxygen species in chloroplasts: a submolecular approach. Agric. Ecosyst. Environ. 106(2–3): 119–133. DOI: 10.1016/j.agee.2004.10.022.
Fisher, N.S. (1981). On the selection for heavy metal tolerance in diatoms from the Derwent Estuary, Tasmania. Mar. Freshwater Res. 32(4): 555–561. DOI: 10.1071/MF9810555.
Foyer, C.H., Descourvieres, P. & Kunert, K.J. (1994). Protection against oxygen radicals: an important defence mechanism studied in transgenic plants. Plant Cell Environ. 17: 507–523. DOI: 10.1111/j.1365-3040.1994.tb00146.x.
Fridovich, I. (1997). Superoxide anion radical (O2−.), superoxide dismutases, and related matters. J. Biol. Chem. 272(30): 18515–18517. DOI: 10.1074/jbc.272.30.18515.
Gaur, A. & Adholeya, A. (2004). Prospects of arbuscular mycorrhizal fungi in phytoremediation of heavy metal contaminated soils. Curr. Sci. India 86(4): 528–534.
Guang, J.Z., Fu, Q.P., Li, J.Z. & Guang, G.Y. (2012). Biosorption of zinc and copper from aqueous solutions by two freshwater green microalgae Chlorella pyrenoidosa and Scenedesmus obliquus. Environ. Sci. Pollut. Res. 19: 2918–2929. DOI: 10.1007/s11356-012-0800-9.
Kumar, K.S., Dahms, H.U., Won, E.J., Lee, J.S. & Shin, K.H. (2015). Microalgae – A promising tool for heavy metal remediation. Ecotox. Environ. Safe. 113: 329–352. DOI: 10.1016/j.ecoenv.2014.12.019.
Lamai, C., Kruatrachue, M., Pokethitiyook, P., Upatham, E.S. & Soonthornsarathool, V. (2005). Toxicity and accumulation of lead and cadmium in the filamentous green alga Cladophora fracta (OF Müller ex Vahl) Kützing: A laboratory study. Scienceasia 31: 121–127. DOI: 10.2306/scienceasia1513-1874.2005.31.121.
Lasat, M.M. (2000). The use of plants for the removal of toxic metals from contaminated soils. US: Environmental Protection Agency.
Lesser, M.P., Stochaj, W.R., Tapley, D.W. & Shick, J.M. (1990). Bleaching in coral reef anthozoans: effects of irradiance, ultraviolet radiation, and temperature on the activities of protective enzymes against active oxygen. Coral reefs 8(4): 225–232. DOI: 10.1007/bf00265015.
Lu, CM., Chau, C.W. & Zhang, J.H. (2000). Acute toxicity of excess mercury on the photosynthetic performance of cyanobacterium, S. platensis – assessment by chlorophyll fluorescence analysis. Chemosphere 41(1–2): 191–196. DOI: 10.1016/S0045-6535(99)00411-7.
Marschner, H. (2012). Marschner's mineral nutrition of higher plants. USA: Academic press pp. 1–672.
Myśliwa-Kurdziel, B. & Strzałka, K. (2002). Influence of metals on biosynthesis of photosynthetic pigments. In Physiology and biochemistry of metal toxicity and tolerance in plants (pp. 201–227). Netherlands: Springer Netherlands.
Myśliwa‐Kurdziel, B., Amirjani, M.R., Strzałka, K. & Sundqvist, C. (2003). Fluorescence Lifetimes of Protochlorophyllide in Plants with Different Proportions of Short‐wavelength and Long‐wavelength Protochlorophyllide Spectral Forms. Photochem. Photobiol. 78(2): 205–212. DOI: 10.1562/0031-8655(2003)0780205FLOPIP2.0.CO2.
Omar, H.H. (2002). Bioremoval of zinc ions by Scenedesmus obliquus and Scenedesmus quadricauda and its effect on growth and metabolism. Int. Biodeter. Biodegr. 50(2): 95–100. DOI: 10.1016/S0964-8305(02)00048-3.
Önem, B., Doğru, A., Ongun Sevindik, T. & Tunca, H. (2018). Preliminary study on the effects of heavy metals on the growth and some antioxidant enzymes in Arthrospira platensis‐M2 strain. Phycol. Res. 66(1): 23–30. DOI: 10.1111/pre.12202.
Pekey, H., Karakaş, D. & Bakoglu, M. (2004). Source apportionment of trace metals in surface waters of a polluted stream using multivariate statistical analyses. Mar. Pollut. Bull. 49(9–10): 809–818. DOI: 10.1016/j.marpolbul.2004.06.029.
Petersen, R. (1982). Influence of copper and zinc on the growth of a freshwater alga, Scenedesmus quadricauda: the significance of chemical speciation. Environ. Sci. Technol. 16(8): 443–447.
Prasad, M.N.V. & Strzałka, K. (1999). Impact of heavy metals on photosynthesis. In Heavy metal stress in plants Germany (pp. 117–138). Springer Berlin Heidelberg.
Raychaudhuri, S.S. & Deng, X.W. (2000). The role of superoxide dismutase in combating oxidative stress in higher plants. Bot. Rev. 66(1): 89–98.
Rosko, J.J. & Rachlin, J.W. (1977). The effect of cadmium, copper, mercury, zinc and lead on cell division, grown and chlorophyll a content of the chlorophyte Chlorella vulgaris. Bull. Torrey Bot. Club 104: 226–275. DOI: 10.2307/2484302.
Ruano, A., Poschenrieder, C.H. & Barcelo, J. (1988). Growth and biomass partitioning in zinc‐toxic bush beans. Journal Plant Nutr. 11(5): 577–588.
Sagardoy, R., Morales, F., López‐Millán, A.F., Abadía, A. & Abadía, J. (2009). Effects of zinc toxicity on sugar beet (Beta vulgaris L.) plants grown in hydroponics. Plant Biol. 11(3): 339–350. DOI: 10.1080/01904168809363824.
Saygı, Y. & Yiğit, S.A. (2012). Assessment of metal concentrations in two cyprinid fish species (Leuciscus cephalus and Tinca tinca) captured from Yeniçağa Lake, Turkey. Bulletin Environ. Contam. Tox. 89(1): 86–90. DOI: 10.1007/s00128-012-0647-2.
Schoefs, B. & Bertrand, M. (2005). Chlorophyll biosynthesis – a review. In M. Pessarakli (Ed.), Handbook of Photosynthesis. 2nd Ed. (pp. 37–54). Boca Raton-London-New York-Singapore: CRC Pres book.
Sentsova, O.Y. & Maksimov, V.N. (1985). Effects of Heavy Metals on Microorganisms. Usp. Mikrobiol. 20: 227–252.
Sgherri, C.L.M., Loggini, B., Puliga, S. & Navari-Izzo, F. (1994.) Antioxidant system in Sporobolus stapfianus: changes in response to desiccation and rehydration. Phytochemistry. 35: 561–565. DOI: 10.1016/S0031-9422(00)90561-2.
Solymosi, K., Lenti, K., Mysliwa-Kurdziel, B., Fidy, J., Strzałka, K. et al. (2004). Depending on concentration, Hg2+ reacts with different components of the NADPH: protochlorophyllide oxidoreductase macrodomains. Plant Biol. 6: 358–63. DOI: 10.1055/s-2004-817893.
Sousa, S.F., Lopes, A.B., Fernandes, P.A. & Ramos, M.J. (2009). The Zinc proteome: a tale of stability and functionality. Dalton Trans. (38): 7946–7956. DOI: 10.1039/b904404c.
Surosz, W. & Palinska, K.A. (2004). Effects of heavy-metal stress on cyanobacterium Anabaena flos-aquae. Archives Environ. Con. Tox. 48(1): 40–48. DOI: 10.1007/s00244-004-0163-4.
Tripathi, B.N., Mehta, S.K., Amar, A. & Gaur, J.P. (2006). Oxidative stress in Scenedesmus sp. during short-and long-term exposure to Cu2+ and Zn2+. Chemosphere 62(4): 538–544. DOI: 10.1016/j.chemosphere.2005.06.031.
Tukaj, Z., Bohdanowicz, J. & Aksmann, A. (1998). A morphometric and stereological analysis of ultrastructural changes in two Scenedesmus (Chlorococcales, Chlorophyta) strains subjected to diesel fuel oil pollution. Phycologia 37(5): 388–393. DOI: 10.2216/i0031-8884-37-5-388.1.
Urso, M.L. & Clarkson, P.M. (2003). Oxidative stress, exercise, and antioxidant supplementation. Toxicology 189: 41–54. DOI: 10.1016/S0300-483X(03)00151-3.
USEPA. (2006). USEPA region III risk-based concentration table: technical background information.
Valentine, J.S., Wertz, D.L., Lyons, T.J., Liou, L.L., Goto, J.J. et al. (1998). The dark side of dioxygen biochemistry. Curr. Opin. Chem. Biol. 2: 253–262. DOI: 10.1016/S1367-5931(98)80067-7.
Visviki, I. & Rachlin, J.W. (1994). Acute and chronic exposure of Dunaliella salina and Chlamydomonas bullosa to copper and cadmium: effects on ultrastructure. Archives Environ. Con. Tox. 26(2): 154–162.
Wang, S.Y., Jiao, H. & Faust, M. (1991). Changes in ascorbate, glutathione and related enzyme activity during thidiazuron-induced bud break of apple. Physiol. Plantarum 82: 231–236. DOI: 10.1111/j.1399-3054.1991.tb00086.x.
Yalçın, N. & Sevinç, V. (2001). Heavy metal contents of Lake Sapanca. Turk. J. Chem. 25(4): 521–526.
Zhou, Z.S., Huang, S.Q., Guo, K., Mehta, S.K., Zhang, P.C. et al. (2007). Metabolic adaptations to mercury-induced oxidative stress in roots of Medicago sativa L. J. Inorg. Biochem. 101: 1–9. DOI: 10.1016/j.jinorgbio.2006.05.011.

Bądź pierwszy, który skomentuje ten wpis

Dodaj komentarz