Mg, Sn, Cd, Zn and Fe accumulation in unicellular green alga Chlorella vulgaris and its effects on growth, content of photosynthetic pigments and protein
Article Sidebar
Main Article Content
Abstract
A technique to purify wastewater based on microalgae is an attractive and promising idea for its potential to clean water and as supplementary aquaculture feedstocks. The present study aimed to investigate magnesium (Mg), tin (Sn), cadmium (Cd), zinc (Zn), and iron (Fe) effects in the unicellular green algae Chlorella vulgaris as a primary producer and the relationship with the growth, the content of photosynthetic pigments and protein. The ions effects were evaluated by measuring the effect of different ion concentrations on algal growth during a 15-day exposure period. Samples were collected every 3 days over 15 days of the cultivation period to estimate the growth of C. vulgaris. Chlorophyll-a (Chl-a) and protein contents of samples were determined on the 15th day of cultivation. Statistical analysis showed that there were significant differences (P < 0.05) in the growth and Chl-a content of C. vulgaris at different ion concentrations. These could be related to the specific differences in cell metabolism. The highest protein content was found at 5 ppm concentration of Mg (23.03 ± 0.02 μg/mL), Sn (18.82 ± 0.02 μg/mL), Cd (12.52 ± 0.11 μg/mL), Zn (18.99 ± 0.02 μg/mL), and Fe (17.42 ± 0.02 μg/mL) ions. There were significant differences (P < 0.05) between the protein content of Mg, Sn, Cd, Zn, and Fe. Growth rate and total Chl-a content (mg/L) were highest at 5 ppm concentration of all ions and the specific growth rate (mg/L), Chl-a, and protein content of C. vulgaris were highest at 5 ppm concentration of Mg ions. This study can be a good model for the use of microalgae in the bioremediation of water contaminated with Mg, Sn, Cd, Zn, and Fe.
Article Details
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
References
Baumann, H.A., L. Morrison and D.B. Stengel. 2009. Metal accumulation and toxicity measured by PAM-chlorophyll fluorescence in seven species of marine macroalgae. Ecotoxicol. Environ. Saf. 72(4): 1063–1075.
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.
Çelekli, A., E. Gültekin and H. Bozkurt. 2016. Morphological and biochemical responses of Spirogyra setiformis exposed to cadmium. Clean (Weinh) 44(3): 256–262.
Chen, L., Q.S. Zheng and Z.P. Liu. 2009. Effects of different concentrations of copper ion on the growth and chlorophyll fluorescence characteristics of Scendesmus obliquus L. Ecol. Environ. Sci. 18: 1231–1235.
Cheng, J., H. Qiu, Z. Chang, Z. Jiang and W. Yin. 2016. The effect of cadmium on the growth and antioxidant response for freshwater algae Chlorella vulgaris. Springerplus 5(1): 1290.
Darmono, O. 1995. Logam Dalam Sistem Biology Makhluk Hidup. UI-Press, Penerbit Universitas Indonesia, Jakarta, Indonesia.
Davies, A.G. 1974. The growth kinetics of Isochrysis galbana in cultures containing sub lethal concentrations of mercuric chloride. J. Mar. Biol. Assoc. UK. 54(1): 157–169.
De Filippis, L.F.C. and K. Pallaghy. 1994. Heavy metals: sources and biological effects, pp. 31–77. In: L.C. Rai, J.P. Gaur and C.J. Soeder, (Eds), Algaeand Water Pollution. E. Schweizeerbartsche Verlagsbuchhandlung, Science Publisher, Stuttgart, Germany.
De Philippis, R. and M. Vincenzini. 1998. Exocellular polysaccharides from cyanobacteria and their possible applications. FEMS Microbiol. Rev. 22(3): 151–175.
Dias, M.A., I.C.A. Lacerda, P.F. Pimentel, H.F. de Castro and C.A. Rosa. 2002. Removal of heavy metals by an Aspergillus terreusstrain immobilized in polyurethanematrix. Lett. Appl. Microbiol. 34(1): 46–50.
Dinesh Kumar, S., P. Santhanam, S. Ananth, A. Shenbaga Devi, R. Nandakumar, B. Balaji Prasath, S. Jeyanthi, T. Jayalakshmi and P. Ananthi. 2014. Effect of different dosages of zinc on the growth and biomass in five marine microalgae. Int. J. Fish. Aquac. 6(1): 1–8.
Dinesh Kumar, S., P. Santhanam, T. Jayalakshmi, R. Nandakumar, S. Ananth, A. Shenbaga Devi and B. Balaji Prasath. 2013. Optimization of pH and retention time on the removal of nutrients and heavy metal (zinc) using immobilized marine microalga Chlorella marina. J. Biol. Sci. 13(5): 400–405.
Estevez, M.S., G. Malanga and S. Puntarulo. 2001. Iron-dependent oxidative stress in Chlorella vulgaris. Plant Sci. 161(1): 9–17.
Fenchel, T. 1988. Marine plankton food chains. Ann. Rev. Ecol. Syst. 19: 19–38.
Gao, K., Y. Ji and J. Tanaka. 2004. Quantitative evaluation of wind effect during emersion on Porhpyra haitanensis (Rhodophyta), a farmed species in southern China. Fish. Sci. 70: 710–712.
Godt, J., F. Scheidig, C. Grosse-Siestrup, V. Esche, P. Brandenburg, A. Reich and D.A. Groneberg. 2006. The toxicity of cadmium and resulting hazards for human health. J. Occup. Med. Toxicol. 1: 22.
Iriani, D., O. Suriyaphan and N. Chaiyanate. 2011. Effect of iron concentration on growth, protein content and total phenolic content of Chlorella sp. cultured in basal medium. Sains Malays. 40(4): 353–358.
Kapkov, V.I. and O.A. Belenikina. 2003. Biomarkers of pollution of marine ecosystems with heavy metals. Water Ecosyst. Organ. (Moscow) 6: 68–69.
Kapkov, V.I. and O.A. Belenikina. 2007. A study of the resistance of mass marine algae to heavy metals. Moscow Univ. Biol. Sci. Bull. 62(1): 30–33.
Kean, M.A., E. Brons Delgado, B.P. Mensink and M.H.J. Bugter. 2015. Iron chelating agents and their effects on the growth of Pseudokirchneriella subcapitata, Chlorella vulgaris, Phaeodactylum tricornutum and Spirulina platensis in comparison to Fe- EDTA. J. Algal Biomass Utln. 6(1): 56–73.
Küpper, H., I. Šetík, E. Šetliková, N. Ferimazova, M. Spiller and F.C. Küpper. 2003. Copper-induced inhibition of photosynthesis: limiting steps of in vivo copper chlorophyll formation in Scenedesmus quadricauda. Funct. Plant Biol. 30(12): 1187–1196.
Lananan, F., S.H. Abdul Hamid, W.N.S. Din, N. Ali, H. Khatoon, A. Jusoh and A. Endut. 2014. Symbiotic bioremediation of aquaculture wastewater in reducing ammonia and phosphorus utilizing effective microorganism (EM-1) and microalgae (Chlorella sp.). Int. Biodeterior. Biodegradation. 95: 127–134.
Lavajoo, F., M. Taherizadeh and M. Dehghani. 2015. The absorption of nitrate and phosphate from urban sewage by blue-green algae (Spirolina platensis) (an alternative medium) as application for removing the pollution. J. Appl. Sci. Environ. Manage. 19(3): 353–356.
Leborans, G.F. and A. Novillo. 1996. Toxicity and bioaccumulation of cadmium in Olisthodiscus luteus (Raphidophyceae). Water Res. 30(1): 57–62.
Lim, C.Y., Y.H. Yoo, M. Sidharthan, C.W. Ma, I.C. Bang, J.M. Kim, K.S. Lee, N.S. Park and H.W. Shin. 2006. Effects of copper (I) oxide on growth and biochemical compositions of two marine microalgae. J. Environ. Biol. 27(3): 461–466.
Mallick, N. and L.C. Rai. 1989. Response of Anabaena doliolumto bimetallic combinations of Cu, Ni and Fe with special reference to sequential addition. J. Appl. Phycol. 1: 301–306.
Mantoura, R.F.C. and C.A. Llewellyn. 1983. The rapid determination of algal chlorophyll and carotenoid and their breakdown products in natural waters by reverse-phase high-performance liquid chromatography. Anal. Chim. Acta 151: 297–314.
Miao, X. and Q. Wu. 2006. Biodiesel production from heterotrophic microalgal oil. Bioresour. Technol. 97(6): 841–846.
Mohammed, M.H. and B. Markert. 2006. Toxicity of heavy metals on Scenedesmus quadricauda (Turp.) de Brebisson in batch cultures. Environ. Sci. Pollut. Res. Int. 13(2): 98–104.
Nasir, N.M., N.S.A. Bakar, F. Lananan, S.H. Abdul Hamid, S.S. Lam and A. Jusoh. 2015. Treatment of African catfish, Clarias gariepinus wastewater utilizing phytoreediation of microalgae, Chlorella sp. with Aspergillus niger bio-harvesting. Bioresour. Technol. 190: 492–498.
Oh-Hama, T. and S. Miyachi. 1988. Chlorella, pp. 3–26. In: M.A. Borowitzka and L.J. Borowitzka, (Eds), Microalgal Biotechnology. Cambridge University Press, Cambridge, UK.
Orús, M.I., E. Marco and F. Martínez. 1991. Suitability of Chlorella vulgaris UAM 101 for heterotrophic biomass production. Bioresour. Technol. 38: 179–184.
Peters, K., M. Bundschuh and R.B. Schafer. 2013. Review on the effects of toxicants on freshwater ecosystem functions. Environ. Pollut. 180: 324–329.
Piovár, J., E. Stavrou, J. Kaduková, T. Kimáková and M. Bačkor. 2011. Influence of long-term exposure to copper on the lichen photobiont Trebouxia erici and the free-living algae Scenedesmus quadricauda. Plant Growth Regul. 63: 81–88.
Porra, R.J., W.A. Thompson and P.E. Kriedemann. 1989. Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim. Biophys. Acta 975(3): 384–394.
Rai, L.C., A.K. Singh and N. Mallick. 1991. Studies on photosynthesis, the associated electron transport system and some physiological variables of Chlorella vulgaris under heavy metal stress. J. Plant Physiol. 137(4): 419–424.
Rai, U.N., N.K. Singh, A.K. Upadhyay and S. Verma. 2013. Chromate tolerance and accumulation in Chlorella vulgaris L.: role of antioxidant enzymes and biochemical changes in detoxification of metals. Bioresour. Technol. 136: 604–609.
Rausch, T. 1981. The estimation of micro-algal protein content and its meaning to the evaluation of algal biomass I. Comparison of methods for extracting protein. Hidrobiologia 78: 237–251.
Rijstenbeil, J.W., J.W.M. Derksen, L.J.A. Gerringa, T.C.W. Poortvliet, A. Sandee, M. van den Berg, J. van Drie and J.A. Wijnholds. 1994. Oxidative stress induced by copper: defense and damages in the marine planktonic diatom Ditylum brightwellii, grown in continuous cultures with high and low zinc levels. Mar. Biol. 119: 583–590.
Rosko, J.J. and J.W. Rachlin. 1977. The effect of cadmium, copper, mercury, zinc and lead on cell division, growth and chlorophyll a content of the chlorophyte Chlorella vulgaris. Bull. Torrey Bot. Club 104(3): 226–233.
Shaul, O. 2002. Magnesium transport and function in plants: the tip of the iceberg. Biometals 15: 309–323.
Sicko-Goad, L. 1982. A morphometric analysis of algal response to low dose, short-term heavy metal exposure. Protoplasma 110: 75–86.
Stork, F., M. Backor, B. Klejdus, J. Hedbavny and J. Kovacik. 2013. Changes of metal-induced toxicity by H2O2/NO modulators in Scenedesmus quadricauda (Chlorophyceae). Environ. Sci. Pollut. Res. 20: 5502–5511.
Stratton, G.W., A.L. Huber and C.T. Corke. 1979. Effect of mercuric ion on the growth, photosynthesis, and nitrogenase activity of Anabaena inaequalis. Appl. Environ. Microbiol. 38(3): 537–543.
Sydney, E.B., W. Sturm, J.C. de Carvalho, V. Thomaz-Soccol, C. Larroche, A. Pandey and C.R. Soccol. 2010. Potential carbon dioxide fixation by industrially important microalgae. Bioresour. Technol. 101(15): 5892–5896.
Takamura, N., F. Kasai and M.M. Watanabe. 1990. Unique response of cyanophyceae to copper. J. Appl. Phycol. 2: 293–296.
Tukaj, Z., A. Bascik-Remisiewicz, T. Skowronski and C. Tukaj. 2007. Cadmium effect on growth, photosynthesis, ultrastructure and phytochelatin content of green microalga Scenedesmus armatus: a study at low and elevated CO2 concentration. Environ. Exp. Bot. 60(3): 291–299.
Van Baalen, C. and R. O’Donnell. 1978. Isolation of a nickel-dependent blue-green alga. J. Gen. Microbiol. 105(2): 351–353.
Vonshak, A. 1986. Laboratory techniques for the cultivation of microalgae, pp. 117–145. In: A. Richmond, (Ed), Handbook of Microalgal Mass Culture. CRC Press, Florida, USA.
Wang, M., W.C. Kuo-Dahab, S. Dolan and C. Park. 2014. Kinetics of nutrient removal and expression of extracellular polymeric substances of the microalgae, Chlorella sp. and Micractinium sp., in wastewater treatment. Bioresour. Technol. 154: 131–137.
Webb, M. 1949. The influence of magnesium on cell division. 2. The effect of magnesium on the growth and cell division of various bacterial species in complex media. J. Gen. Microbiol. 3: 410.
Wetherell, D.F. 1961. Culture of fresh water algae in enriched natural sea water. Physiol. Plant. 14(1): 1–6.
Wiesnner, W. 1962. Inorganic micronutrients, pp. 267–286. In: R.A. Lewin, (Ed), Physiology and Biochemistry of Algae. Academic Press, New York, USA.
Xiaoling, Y. and G. Jinyao. 2006. Regulation of Fe growth and material accumulation of Dunaliella salina. Chinese Agricultural Science Bulletin 22(10): 476–476.