Assessment of optimal growth conditions for specific carotenoids production by Chlorella vulgaris
Article Main
Abstract
Exploration of regional microalgae for carotenoids production under optimized cultural conditions is a sustainable economic and technical perspective. This study details comprehensive research on the influence of growth conditions on microalgal carotenoids. Carotenoid triggering factors were optimized to identify suitable growth conditions to produce specific carotenoids by Chlorella vulgaris. Media optimization and cultivation conditions were the factors considered and the results revealed the optimum growth conditions for carotenoid production by C. vulgaris was pH 8, 35°C temperature, 0.04 M salinity and 160 µE\m²\sec light intensity. Among the nutrient sources, potassium nitrate and potassium phosphate were suitable for nitrogen and phosphorous supplements. The results indicated optimizing the culture conditions and nutrient sources help to attain desirable carotenoid production by C. vulgaris. Specific carotenoids were extracted from the algal extract and were identified by high-performance liquid chromatography in which lutein (8.8%) was present as major carotenoid followed by astaxanthin (4.6%) and ?-carotene (3.9%). This study revealed that that carotenoid production by C. vulgaris could be enhanced by manipulating culture conditions thereby attain desirable carotenoid production.
Article Details
Article Details
Keywords
Astaxanthin, ?-carotene, Chlorella vulgaris, Carotenoids, Lutein
References
Ambati, R.R., Phang, S.M., Ravi, S. and Aswathanarayana, R.G. (2014). Astaxanthin: sources, extraction, stability, biological activities and its commercial applications - a review. Mar Drugs, 12(1): 128-152. DOI: 10.3390/md12010128
Begum, H., Yusoff, F.M., Banerjee, S., Khatoon, H. and Shariff, M. (2016). Availability and utilization of pigments from microalgae. Crit Rev Food Sci Nutr., 56: 2209–2222. DOI: 10.1080/10408398.2013.7 64 84 1.
Ben-Amotz, A. (1996). Effect of low temperature on the stereoisomer composition of b-carotene in the halotolerant alga, Dunaliella bardawil (Chlorophyta), J Phycol., 32: 272-275. DOI: 10.1111/j.0022-3646.1996.00272.x
Benavente-Vald, J.R., Aguilar, C., Contreras-Esquivel, J.C., Mendez-Zavala, A. and Montanez, J. (2016). Strategies to enhance the production of photosynthetic pigments and lipids in chlorophycae species. Biotechnology Reports. 10: 117-125. DOI: 10.1016/j.btre.2016.04.001
Berman, J., Zorrilla-Lopez, U., Farre, G., Zhu, C., Sandmann, G., Twyman, R.M, Capell, T. and Christou, P. (2015). Nutritionally important carotenoids as consumer products. Phytochem Rev., 14: 727-743. DOI: 10.1007/s11101-014-9373-1
Bhosale, P. (2004). Environmental and cultural stimulants in the production of carotenoids from microorganisms. Appl Microbiol Biotechnol., 63: 351–361. DOI: 10.1007/s00253-003-1441-1
Cha, K.H., Koo, S.Y. and Lee, D.U. (2008). Antiproliferative effects of carotenoids extracted from Chlorella ellipsoidea and Chlorella vulgaris on human colon cancer cells. J Agric Food Chem., 56: 10521–10526. DOI: 10.1021/jf802111x
Chuyen, H.V. and Eun, J.B. (2017). Marine carotenoids: Bioactivities and potential benefits to human health. Crit Rev Food Sci Nutr., 57: 2600-2610. DOI:
10.1080/10408398.2015.1063477
Fernandez-Sevilla, J.M.J.M., Acien Fernandez, F.G. and Molina Grima, E. (2010). Biotechnological production of lutein and its applications. Appl Microbiol Biotechnol., 86:
27–40. DOI: 10.1007/s00253-009-2420-y
Garcia-Gonzalez, M., Moreno, J., Manzano, J.C., Florencio, F.J. and Guerrero, M.G. (2005). Production of Dunaliella salina biomass rich in 9-cis-beta-carotene and lutein in a closed tubular photobioreactor. J Biotechnol., 115(1): 81–90. DOI: 10.1016/j.jbiotec.2004.07.010
Gayathri, S., Rajasree S.R.R., Kirubagaran, R., Aranganathan, L. and Suman, T.Y. (2016) Spectral characterization of ?, ?-carotene-3, 3?- diol (lutein) from marine microalgae Chlorella salina. Renewable Energy. 98: 78–83. DOI: 10.1016/j.renene.2016.04.065
Gayathri, S., Rajasree, S.R.R., Suman, T.Y., Aranganathan, L., Thriuganasambandam, R. and Narendrakumar, G. (2020). Induction of ?, ?-carotene-3, 3?-diol (lutein) production in green algae Chlorella salina with airlift photobioreactor: interaction of different aeration and light-related strategies. Biomass Conv Bioref., DOI: 10.1007/s13399-019-00580-5
Guerin, M., Huntley, M.E. and Olaizola, M. (2003). Haematococcus astaxanthin: applications for human health and nutrition. Trends Biotechnol., 21: 210–216. DOI: 10.1016/S0167-7799(03)00078-7
Harasym, J., and Oledzki, R. (2014). Effect of fruit and vegetable antioxidants on total antioxidant capacity of blood plasma. Nutrition., 30: 511–517. DOI: 10.1016/j.nut.2013.08.019
Huang, W., Lin, Y., He, M., Gong, Y. and Huang, J. (2018). Induced High-Yield Production of Zeaxanthin, Lutein, and ?-Carotene by a mutant of Chlorella zofingiensis. J Agric Food Chem., 66(4): 891–897. DOI: 10.1021/acs.jafc.7b05400
Johnson, E.J. (2002). The role of carotenoids in human health. Nutr Clin Care., 5: 56-65. DOI: 10.1046/j.1523-5408.2002.00004.x
Khan, I.M., Shin, H.J. and Kim D.J. (2018). The promising future of microalgae: current status, challenges, and optimization of a sustainable and renewable industry for biofuels, feed, and other products. Microb Cell Fact., 17: 36. DOI: 10.1186/s12934-018-0879-x
Kleinegris, D.M., Janssen, M., Brandenburg, W.A. and Wijffels, R.H. (2011). Continuous production of carotenoids from Dunaliella salina. Enzyme Microb Technol., 48(3): 253–259. DOI: 10.1016/j.enzmictec.2010.11.005
Li, J., Zhu, D., Niu, J., Shen, S. and Wang, G. (2011). An economic assessment of astaxanthin production by large scale cultivation of Haematococcus pluvialis. Biotechnol Adv., 29: 568–574. DOI: 10.1016/j.biotechad v.20 11.04.001
Lichtenthaler, H.K. and Buschmann, C. (2001). Chlorophylls and carotenoids: Measurements and characterization by UV-VIS spectroscopy. Current Protocols in Food Analytical Chemistry. 1(1): F4.3.1–F4.3.8. DOI: 10.1002/0471142913.faf0403s01
Malis, S.A., Cohen, E. and Ben Amotz, A. (1993). Accumulation of canthaxanthin in Chlorella emersonii. Physiologia Plantarum., 87: 232–236. DOI: 10.1111/j.1399-3054.1993.tb00148.x
Manayi, A., Abdollahi, M., Raman, T., Nabavi, S.F., Habtemariam, S., Daglia, M. and Nabavi, S.M. (2015). Lutein and cataract: from bench to bedside. Crit Rev Biotechnol., 8551: 1–11. DOI: 10.3109/07388551.2015.1049510
Mimuro, M. and Akimoto, S. (2003). Carotenoids of light harvesting systems: energy transfer processes from fucoxanthin and peridinin to chlorophyll Photosynthesis in Algae, Springer, Netherlands, Dordrecht. pp. 335-349. DOI: 10.1007/978-94-007-1038-2_15
Minyuk, G., Sidorov, R. and Solovchenko, A. (2020). Effect of nitrogen source on the growth, lipid, and valuable carotenoid production in the green microalga Chromochloris zofingiensis. J Appl Phycol. 32: 923–935. DOI: 10.1007/s10811-020-02060-0
Mokashi, K., Shetty, V., George, S.A. and Sibi, G. (2016). Sodium bicarbonate as inorganic carbon source for higher biomass and lipid production integrated carbon capture in Chlorella vulgaris. Achievements in the Life Sciences. 10: 111-117. DOI: 10.1016/j.als.2016.05.011
Molino, A., Mehariya, S., Iovine, A., Casella, P., Marino, T., Karatza, D., Chianese, S. and Musmarra, D. (2020). Enhancing biomass and lutein production from Scenedesmus almeriensis: Effect of carbon dioxide concentration and culture medium. Fron Plant Sci., 11: 415. DOI: 10.3389/fpls.2020.00415
Mulders, K.J.M. Lamers, P.P.., Martens, D.E. and Wijffels, R.H. (2014). Phototrophic pigment production with microalgae: biological constraints and opportunities. J Phycol., 50: 229-242. DOI: 10.1111/jpy.12173
Pelah, D., Sintov, A. and Cohen, E. (2004). The effect of salt stress on the production of canthaxanthin and astaxanthin by Chlorella zofingiensis grown under limited light intensity. World Journal of Microbiology and Biotechnology, 20: 483–486. DOI: 10.1023/b:wibi.0000040398.9 3103.21
Raposo, M.F.J., De Morais, A.M.M.B. and De Morais, R.M.S.C. (2015). Carotenoids from marine microalgae: A valuable natural source for the prevention of chronic diseases. Mar Drugs., 13: 5128-5155. DOI: 10.3390/md13085128
Roberts, R.L., Green, J. and Lewis, B. (2009). Lutein and zeaxanthin in eye and skin health. Clin Dermatol. 27: 195-201. DOI: 10.1016/j.clindermatol.2008.01.011
Shi, X.M. and Chen, F. (1997). Stability of lutein under various storage conditions. Molecular Nutrition. Food Research. 41: 38–41. DOI:10.1002/food.19970410110
Taucher, J., Baer, S., Schwerna, P., Hofmann, D., Hummer, M., Buchholz, R. and Becker, A. (2016). Cell Disruption and pressurized liquid extraction of carotenoids from microalgae. J Thermodyn Catal., 7: 158. DOI: 10.4172/2158-7544.1000158
Wei, D., Chen, F., Chen, G., Zhang, X., Liu, L. and Zhang, H. (2008). Enhanced production of lutein in heterotrophic Chlorella protothecoides by oxidative stress. Sci China C Life Sci., 51: 1088-1093. DOI: 10.1007/s11427-008-0145-2
Wellburn, A. and Lichtenthaler, H. (1984). Formulae and Program to Determine Total Carotenoids and Chlorophylls A and B of Leaf Extracts in Different Solvents. In: Sybesma C. (eds) Advances in Photosynthesis Research. Advances in Agricultural Biotechnology, vol 2. Springer, Dordrecht. DOI: 10.1007/978-94-017-6368-4_3
Xie, Y., Ho, S.H., Chen, C.N.N., Chen, C.Y., Ng, I.S., Jing, K.J., Chang, J.S. and Lu, Y., (2013). Phototrophic cultivation of a thermo-tolerant Desmodesmus sp. for lutein production: Effects of nitrate concentration, light intensity and fed-batch operation. Bioresour Technol., 144: 435–444. DOI: 10.1016/j.biortech.2013.06.064
Zhang, D., Wan, M., del Rio-Chanona, E.A., Huang, J., Wang, W., Li, Y. and Vassiliadis, V.S., (2015). Dynamic modelling of Haematococcus pluvialis photoinduction for astaxanthin production in both attached and suspended photobioreactors. Algal Res., 13: 69-78. DOI: 10.1016/j.algal.2015.11.019
Begum, H., Yusoff, F.M., Banerjee, S., Khatoon, H. and Shariff, M. (2016). Availability and utilization of pigments from microalgae. Crit Rev Food Sci Nutr., 56: 2209–2222. DOI: 10.1080/10408398.2013.7 64 84 1.
Ben-Amotz, A. (1996). Effect of low temperature on the stereoisomer composition of b-carotene in the halotolerant alga, Dunaliella bardawil (Chlorophyta), J Phycol., 32: 272-275. DOI: 10.1111/j.0022-3646.1996.00272.x
Benavente-Vald, J.R., Aguilar, C., Contreras-Esquivel, J.C., Mendez-Zavala, A. and Montanez, J. (2016). Strategies to enhance the production of photosynthetic pigments and lipids in chlorophycae species. Biotechnology Reports. 10: 117-125. DOI: 10.1016/j.btre.2016.04.001
Berman, J., Zorrilla-Lopez, U., Farre, G., Zhu, C., Sandmann, G., Twyman, R.M, Capell, T. and Christou, P. (2015). Nutritionally important carotenoids as consumer products. Phytochem Rev., 14: 727-743. DOI: 10.1007/s11101-014-9373-1
Bhosale, P. (2004). Environmental and cultural stimulants in the production of carotenoids from microorganisms. Appl Microbiol Biotechnol., 63: 351–361. DOI: 10.1007/s00253-003-1441-1
Cha, K.H., Koo, S.Y. and Lee, D.U. (2008). Antiproliferative effects of carotenoids extracted from Chlorella ellipsoidea and Chlorella vulgaris on human colon cancer cells. J Agric Food Chem., 56: 10521–10526. DOI: 10.1021/jf802111x
Chuyen, H.V. and Eun, J.B. (2017). Marine carotenoids: Bioactivities and potential benefits to human health. Crit Rev Food Sci Nutr., 57: 2600-2610. DOI:
10.1080/10408398.2015.1063477
Fernandez-Sevilla, J.M.J.M., Acien Fernandez, F.G. and Molina Grima, E. (2010). Biotechnological production of lutein and its applications. Appl Microbiol Biotechnol., 86:
27–40. DOI: 10.1007/s00253-009-2420-y
Garcia-Gonzalez, M., Moreno, J., Manzano, J.C., Florencio, F.J. and Guerrero, M.G. (2005). Production of Dunaliella salina biomass rich in 9-cis-beta-carotene and lutein in a closed tubular photobioreactor. J Biotechnol., 115(1): 81–90. DOI: 10.1016/j.jbiotec.2004.07.010
Gayathri, S., Rajasree S.R.R., Kirubagaran, R., Aranganathan, L. and Suman, T.Y. (2016) Spectral characterization of ?, ?-carotene-3, 3?- diol (lutein) from marine microalgae Chlorella salina. Renewable Energy. 98: 78–83. DOI: 10.1016/j.renene.2016.04.065
Gayathri, S., Rajasree, S.R.R., Suman, T.Y., Aranganathan, L., Thriuganasambandam, R. and Narendrakumar, G. (2020). Induction of ?, ?-carotene-3, 3?-diol (lutein) production in green algae Chlorella salina with airlift photobioreactor: interaction of different aeration and light-related strategies. Biomass Conv Bioref., DOI: 10.1007/s13399-019-00580-5
Guerin, M., Huntley, M.E. and Olaizola, M. (2003). Haematococcus astaxanthin: applications for human health and nutrition. Trends Biotechnol., 21: 210–216. DOI: 10.1016/S0167-7799(03)00078-7
Harasym, J., and Oledzki, R. (2014). Effect of fruit and vegetable antioxidants on total antioxidant capacity of blood plasma. Nutrition., 30: 511–517. DOI: 10.1016/j.nut.2013.08.019
Huang, W., Lin, Y., He, M., Gong, Y. and Huang, J. (2018). Induced High-Yield Production of Zeaxanthin, Lutein, and ?-Carotene by a mutant of Chlorella zofingiensis. J Agric Food Chem., 66(4): 891–897. DOI: 10.1021/acs.jafc.7b05400
Johnson, E.J. (2002). The role of carotenoids in human health. Nutr Clin Care., 5: 56-65. DOI: 10.1046/j.1523-5408.2002.00004.x
Khan, I.M., Shin, H.J. and Kim D.J. (2018). The promising future of microalgae: current status, challenges, and optimization of a sustainable and renewable industry for biofuels, feed, and other products. Microb Cell Fact., 17: 36. DOI: 10.1186/s12934-018-0879-x
Kleinegris, D.M., Janssen, M., Brandenburg, W.A. and Wijffels, R.H. (2011). Continuous production of carotenoids from Dunaliella salina. Enzyme Microb Technol., 48(3): 253–259. DOI: 10.1016/j.enzmictec.2010.11.005
Li, J., Zhu, D., Niu, J., Shen, S. and Wang, G. (2011). An economic assessment of astaxanthin production by large scale cultivation of Haematococcus pluvialis. Biotechnol Adv., 29: 568–574. DOI: 10.1016/j.biotechad v.20 11.04.001
Lichtenthaler, H.K. and Buschmann, C. (2001). Chlorophylls and carotenoids: Measurements and characterization by UV-VIS spectroscopy. Current Protocols in Food Analytical Chemistry. 1(1): F4.3.1–F4.3.8. DOI: 10.1002/0471142913.faf0403s01
Malis, S.A., Cohen, E. and Ben Amotz, A. (1993). Accumulation of canthaxanthin in Chlorella emersonii. Physiologia Plantarum., 87: 232–236. DOI: 10.1111/j.1399-3054.1993.tb00148.x
Manayi, A., Abdollahi, M., Raman, T., Nabavi, S.F., Habtemariam, S., Daglia, M. and Nabavi, S.M. (2015). Lutein and cataract: from bench to bedside. Crit Rev Biotechnol., 8551: 1–11. DOI: 10.3109/07388551.2015.1049510
Mimuro, M. and Akimoto, S. (2003). Carotenoids of light harvesting systems: energy transfer processes from fucoxanthin and peridinin to chlorophyll Photosynthesis in Algae, Springer, Netherlands, Dordrecht. pp. 335-349. DOI: 10.1007/978-94-007-1038-2_15
Minyuk, G., Sidorov, R. and Solovchenko, A. (2020). Effect of nitrogen source on the growth, lipid, and valuable carotenoid production in the green microalga Chromochloris zofingiensis. J Appl Phycol. 32: 923–935. DOI: 10.1007/s10811-020-02060-0
Mokashi, K., Shetty, V., George, S.A. and Sibi, G. (2016). Sodium bicarbonate as inorganic carbon source for higher biomass and lipid production integrated carbon capture in Chlorella vulgaris. Achievements in the Life Sciences. 10: 111-117. DOI: 10.1016/j.als.2016.05.011
Molino, A., Mehariya, S., Iovine, A., Casella, P., Marino, T., Karatza, D., Chianese, S. and Musmarra, D. (2020). Enhancing biomass and lutein production from Scenedesmus almeriensis: Effect of carbon dioxide concentration and culture medium. Fron Plant Sci., 11: 415. DOI: 10.3389/fpls.2020.00415
Mulders, K.J.M. Lamers, P.P.., Martens, D.E. and Wijffels, R.H. (2014). Phototrophic pigment production with microalgae: biological constraints and opportunities. J Phycol., 50: 229-242. DOI: 10.1111/jpy.12173
Pelah, D., Sintov, A. and Cohen, E. (2004). The effect of salt stress on the production of canthaxanthin and astaxanthin by Chlorella zofingiensis grown under limited light intensity. World Journal of Microbiology and Biotechnology, 20: 483–486. DOI: 10.1023/b:wibi.0000040398.9 3103.21
Raposo, M.F.J., De Morais, A.M.M.B. and De Morais, R.M.S.C. (2015). Carotenoids from marine microalgae: A valuable natural source for the prevention of chronic diseases. Mar Drugs., 13: 5128-5155. DOI: 10.3390/md13085128
Roberts, R.L., Green, J. and Lewis, B. (2009). Lutein and zeaxanthin in eye and skin health. Clin Dermatol. 27: 195-201. DOI: 10.1016/j.clindermatol.2008.01.011
Shi, X.M. and Chen, F. (1997). Stability of lutein under various storage conditions. Molecular Nutrition. Food Research. 41: 38–41. DOI:10.1002/food.19970410110
Taucher, J., Baer, S., Schwerna, P., Hofmann, D., Hummer, M., Buchholz, R. and Becker, A. (2016). Cell Disruption and pressurized liquid extraction of carotenoids from microalgae. J Thermodyn Catal., 7: 158. DOI: 10.4172/2158-7544.1000158
Wei, D., Chen, F., Chen, G., Zhang, X., Liu, L. and Zhang, H. (2008). Enhanced production of lutein in heterotrophic Chlorella protothecoides by oxidative stress. Sci China C Life Sci., 51: 1088-1093. DOI: 10.1007/s11427-008-0145-2
Wellburn, A. and Lichtenthaler, H. (1984). Formulae and Program to Determine Total Carotenoids and Chlorophylls A and B of Leaf Extracts in Different Solvents. In: Sybesma C. (eds) Advances in Photosynthesis Research. Advances in Agricultural Biotechnology, vol 2. Springer, Dordrecht. DOI: 10.1007/978-94-017-6368-4_3
Xie, Y., Ho, S.H., Chen, C.N.N., Chen, C.Y., Ng, I.S., Jing, K.J., Chang, J.S. and Lu, Y., (2013). Phototrophic cultivation of a thermo-tolerant Desmodesmus sp. for lutein production: Effects of nitrate concentration, light intensity and fed-batch operation. Bioresour Technol., 144: 435–444. DOI: 10.1016/j.biortech.2013.06.064
Zhang, D., Wan, M., del Rio-Chanona, E.A., Huang, J., Wang, W., Li, Y. and Vassiliadis, V.S., (2015). Dynamic modelling of Haematococcus pluvialis photoinduction for astaxanthin production in both attached and suspended photobioreactors. Algal Res., 13: 69-78. DOI: 10.1016/j.algal.2015.11.019
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Assessment of optimal growth conditions for specific carotenoids production by Chlorella vulgaris. (2020). Journal of Applied and Natural Science, 12(4), 550-555. https://doi.org/10.31018/jans.v12i4.2399
