LIGHT INTENSITY EFFECT ON THE GROWTH, PIGMENT, PHENOLIC COMPOUND ACCUMULATION, AND ANTIOXIDANT CAPACITY OF HAEMATOCOCCUS PLUVIALIS MICROALGAE
Main Article Content
Abstract
Haematococcus pluvialis is a green unicellular microalga highly valued for its ability to accumulate a large amount of astaxanthin in cells. Cultivation light is one of the most factors affecting the growth, pigment synthesis, capacity for antioxidant, and phenolic compound accumulation of H. pluvialis cells. In this research, four light intensities from 20 to 100 µmol photon.m-2.s-1 were used to investigate the organismal growth, pigment, and phenolic compound accumulation, as well as antioxidant capacity of H. pluvialis cells in OHM and BG11 media. In both media tested, we observed that under low light intensities from 20 to 50 µmol photon.m-2.s-1, H. pluvialis cells sustained a prolonged green vegetative stage and high cell density. On the contrary, under the high light intensities from 70 to 100 µmol photon.m-2.s-1, H. pluvialis cells developed cyst forms faster and exhibited lower growth while higher pigment synthesis and higher phenolic contents and antioxidant capacity.
Keywords
antioxidant capacity, carotenoid, Haematococcus pluvialis, phenolic
Article Details
References
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Ceron, M. C., Garcia-Malea, M. C., Rivas, J., Acien, F. G., Fernandez, J. M., Del Rio, E., . . . Molina, E. (2007). Antioxidant activity of Haematococcus pluvialis cells grown in continuous culture as a function of their carotenoid and fatty acid content. Appl Microbiol Biotechnol, 74(5), 1112-1119. doi:10.1007/s00253-006-0743-5
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Dominguez-Bocanegra, A. R., Ponce-Noyola, T., & Torres-Munoz, J. A. (2007). Astaxanthin production by Phaffia rhodozyma and Haematococcus pluvialis: a comparative study. Appl Microbiol Biotechnol, 75(4), 783-791. doi:10.1007/s00253-007-0889-9
Fabregas, J., Otero, A., Maseda, A., & Dominguez, A. (2001). Two-stage cultures for the production of astaxanthin from Haematococcus pluvialis. J Biotechnol, 89(1), 65-71.
Fan, L., Vonshak, A., Gabbay, R., Hirshberg, J., Cohen, Z., & Boussiba, S. (1995). The biosynthetic pathway of astaxanthin in a green alga Haematococcus pluvialis as indicated by inhibition with diphenylamine. Plant and cell Physiology, 36(8), 1519-1524.
Goiris, K., Muylaert, K., Fraeye, I., Foubert, I., De Brabanter, J., & De Cooman, L. (2012). Antioxidant potential of microalgae in relation to their phenolic and carotenoid content. Journal of Applied Phycology, 24(6), 1477-1486.
Harker, M., Tsavalos, A. J., & Young, A. J. (1996). Factors responsible for astaxanthin formation in the chlorophyte Haematococcus pluvialis. Bioresource Technology, 55(3), 207-214.
Kobayashi, M., Kakizono, T., Nishio, N., & Nagai, S. (1992). Effects of light intensity, light quality, and illumination cycle on astaxanthin formation in a green alga, Haematococcus pluvialis. Journal of Fermentation and Bioengineering, 74(1), 61-63.
Kobayashi, M., Kakizono, T., Nishio, N., Nagai, S., Kurimura, Y., & Tsuji, Y. (1997). Antioxidant role of astaxanthin in the green alga Haematococcus pluvialis. Applied microbiology and biotechnology, 48(3), 351-356.
Levasseur, M., Thompson, P. A., & Harrison, P. J. (1993). Physiological acclimation of marine phytoplankton to different nitrogen sources 1. Journal of phycology, 29(5), 587-595.
Li, F., Cai, M., Lin, M., Huang, X., Wang, J., Ke, H., . . . Wu, S. (2019). Differences between Motile and Nonmotile Cells of Haematococcus pluvialis in the Production of Astaxanthin at Different Light Intensities. Marine drugs, 17(1), 39.
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Plaza, M., Cifuentes, A., & Ibáñez, E. (2008). In the search of new functional food ingredients from algae. Trends in Food Science & Technology, 19(1), 31-39.
Prieto, A., Pedro Canavate, J., & Garcia-Gonzalez, M. (2011). Assessment of carotenoid production by Dunaliella salina in different culture systems and operation regimes. J Biotechnol, 151(2), 180-185. doi:10.1016/j.jbiotec.2010.11.011
Rodriguez-Meizoso, I., Jaime, L., Santoyo, S., Senorans, F. J., Cifuentes, A., & Ibanez, E. (2010). Subcritical water extraction and characterization of bioactive compounds from Haematococcus pluvialis microalga. J Pharm Biomed Anal, 51(2), 456-463. doi:10.1016/j.jpba.2009.03.014
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Safafar, H., Van Wagenen, J., Møller, P., & Jacobsen, C. (2015). Carotenoids, phenolic compounds and tocopherols contribute to the antioxidative properties of some microalgae species grown on industrial wastewater. Marine drugs, 13(12), 7339-7356.
Suh, I. S., Joo, H. N., & Lee, C. G. (2006). A novel double-layered photobioreactor for simultaneous Haematococcus pluvialis cell growth and astaxanthin accumulation. J Biotechnol, 125(4), 540-546. doi:10.1016/j.jbiotec.2006.03.027
Tocquin, P., Fratamico, A., & Franck, F. (2012). Screening for a low-cost Haematococcus pluvialis medium reveals an unexpected impact of a low N/P ratio on vegetative growth. Journal of Applied Phycology, 24(3), 365-373.
Tran, N.-P., Park, J.-K., & Lee, C.-G. (2009). Proteomics analysis of proteins in green alga Haematococcus lacustris (Chlorophyceae) expressed under combined stress of nitrogen starvation and high irradiance. Enzyme and microbial technology, 45(4), 241-246.
Trinh, N. N., Trương, N. B. T., Huynh, T. H., Nguyen, T. D. H., & Tran, T. B. L. (2017). Nang cao su tich luy astaxanthin o vi tao Haematococcus pluvialis boi cac dieu kien stress cua moi truong nuoi cay [Enhancement of astaxanthin accumulation in Haematococcus pluvialis under various stress conditions]. Proceedings of the 35th Anniversary of the Establishment of Ho Chi Minh City University of Food Industry, 74-83.
Wong, Y. (2016). Effects of Light Intensity, Illumination Cycles on Microalgae Haematococcus Pluvialis for Production of Astaxanthin. Journal of Marine Biology and Aquaculture, 1-6.
Yaltirak, T., Aslim, B., Ozturk, S., & Alli, H. (2009). Antimicrobial and antioxidant activities of Russula delica Fr. Food and Chemical Toxicology, 47(8), 2052-2056.
Yuan, J.-P., & Chen, F. (1998). Chromatographic separation and purification of trans-astaxanthin from the extracts of Haematococcus pluvialis. Journal of Agricultural and Food Chemistry, 46(8), 3371-3375.
Ceron, M. C., Garcia-Malea, M. C., Rivas, J., Acien, F. G., Fernandez, J. M., Del Rio, E., . . . Molina, E. (2007). Antioxidant activity of Haematococcus pluvialis cells grown in continuous culture as a function of their carotenoid and fatty acid content. Appl Microbiol Biotechnol, 74(5), 1112-1119. doi:10.1007/s00253-006-0743-5
CHEN, S., & LIANG, Y. (2009). Effects of illumination on the chlorophyll fluorescence parameters and astaxanthin content of Haematococcus pluvialis [J]. South China Fisheries Science, 1.
Das, B., Das, B., Arpita, F., Morshed, M., Uddin, A., Bhattacherjee, R., & Hannan, J. (2011). Phytochemical screening and antioxidant activity of Leucas aspera. International Journal of Pharmaceutical Sciences and Research, 2(7), 1746.
Dominguez-Bocanegra, A. R., Ponce-Noyola, T., & Torres-Munoz, J. A. (2007). Astaxanthin production by Phaffia rhodozyma and Haematococcus pluvialis: a comparative study. Appl Microbiol Biotechnol, 75(4), 783-791. doi:10.1007/s00253-007-0889-9
Fabregas, J., Otero, A., Maseda, A., & Dominguez, A. (2001). Two-stage cultures for the production of astaxanthin from Haematococcus pluvialis. J Biotechnol, 89(1), 65-71.
Fan, L., Vonshak, A., Gabbay, R., Hirshberg, J., Cohen, Z., & Boussiba, S. (1995). The biosynthetic pathway of astaxanthin in a green alga Haematococcus pluvialis as indicated by inhibition with diphenylamine. Plant and cell Physiology, 36(8), 1519-1524.
Goiris, K., Muylaert, K., Fraeye, I., Foubert, I., De Brabanter, J., & De Cooman, L. (2012). Antioxidant potential of microalgae in relation to their phenolic and carotenoid content. Journal of Applied Phycology, 24(6), 1477-1486.
Harker, M., Tsavalos, A. J., & Young, A. J. (1996). Factors responsible for astaxanthin formation in the chlorophyte Haematococcus pluvialis. Bioresource Technology, 55(3), 207-214.
Kobayashi, M., Kakizono, T., Nishio, N., & Nagai, S. (1992). Effects of light intensity, light quality, and illumination cycle on astaxanthin formation in a green alga, Haematococcus pluvialis. Journal of Fermentation and Bioengineering, 74(1), 61-63.
Kobayashi, M., Kakizono, T., Nishio, N., Nagai, S., Kurimura, Y., & Tsuji, Y. (1997). Antioxidant role of astaxanthin in the green alga Haematococcus pluvialis. Applied microbiology and biotechnology, 48(3), 351-356.
Levasseur, M., Thompson, P. A., & Harrison, P. J. (1993). Physiological acclimation of marine phytoplankton to different nitrogen sources 1. Journal of phycology, 29(5), 587-595.
Li, F., Cai, M., Lin, M., Huang, X., Wang, J., Ke, H., . . . Wu, S. (2019). Differences between Motile and Nonmotile Cells of Haematococcus pluvialis in the Production of Astaxanthin at Different Light Intensities. Marine drugs, 17(1), 39.
LICHTENTHALER, H. K., & Wellburn, A. R. (1983). Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Portland Press Ltd.
Plaza, M., Cifuentes, A., & Ibáñez, E. (2008). In the search of new functional food ingredients from algae. Trends in Food Science & Technology, 19(1), 31-39.
Prieto, A., Pedro Canavate, J., & Garcia-Gonzalez, M. (2011). Assessment of carotenoid production by Dunaliella salina in different culture systems and operation regimes. J Biotechnol, 151(2), 180-185. doi:10.1016/j.jbiotec.2010.11.011
Rodriguez-Meizoso, I., Jaime, L., Santoyo, S., Senorans, F. J., Cifuentes, A., & Ibanez, E. (2010). Subcritical water extraction and characterization of bioactive compounds from Haematococcus pluvialis microalga. J Pharm Biomed Anal, 51(2), 456-463. doi:10.1016/j.jpba.2009.03.014
Ruiz-Domínguez, M. C., Espinosa, C., Paredes, A., Palma, J., Jaime, C., Vílchez, C., & Cerezal, P. (2019). Determining the Potential of Haematococcus pluvialis Oleoresin as a Rich Source of Antioxidants. Molecules, 24(22), 4073.
Safafar, H., Van Wagenen, J., Møller, P., & Jacobsen, C. (2015). Carotenoids, phenolic compounds and tocopherols contribute to the antioxidative properties of some microalgae species grown on industrial wastewater. Marine drugs, 13(12), 7339-7356.
Suh, I. S., Joo, H. N., & Lee, C. G. (2006). A novel double-layered photobioreactor for simultaneous Haematococcus pluvialis cell growth and astaxanthin accumulation. J Biotechnol, 125(4), 540-546. doi:10.1016/j.jbiotec.2006.03.027
Tocquin, P., Fratamico, A., & Franck, F. (2012). Screening for a low-cost Haematococcus pluvialis medium reveals an unexpected impact of a low N/P ratio on vegetative growth. Journal of Applied Phycology, 24(3), 365-373.
Tran, N.-P., Park, J.-K., & Lee, C.-G. (2009). Proteomics analysis of proteins in green alga Haematococcus lacustris (Chlorophyceae) expressed under combined stress of nitrogen starvation and high irradiance. Enzyme and microbial technology, 45(4), 241-246.
Trinh, N. N., Trương, N. B. T., Huynh, T. H., Nguyen, T. D. H., & Tran, T. B. L. (2017). Nang cao su tich luy astaxanthin o vi tao Haematococcus pluvialis boi cac dieu kien stress cua moi truong nuoi cay [Enhancement of astaxanthin accumulation in Haematococcus pluvialis under various stress conditions]. Proceedings of the 35th Anniversary of the Establishment of Ho Chi Minh City University of Food Industry, 74-83.
Wong, Y. (2016). Effects of Light Intensity, Illumination Cycles on Microalgae Haematococcus Pluvialis for Production of Astaxanthin. Journal of Marine Biology and Aquaculture, 1-6.
Yaltirak, T., Aslim, B., Ozturk, S., & Alli, H. (2009). Antimicrobial and antioxidant activities of Russula delica Fr. Food and Chemical Toxicology, 47(8), 2052-2056.
Yuan, J.-P., & Chen, F. (1998). Chromatographic separation and purification of trans-astaxanthin from the extracts of Haematococcus pluvialis. Journal of Agricultural and Food Chemistry, 46(8), 3371-3375.