EFFECT OF NITROGEN (NITRATE) ON GROWTH, PROTEIN CONTENT, AND ANTIOXIDANT CAPACITY OF THE SPIRULINA SP.
Main Article Content
Abstract
Spirulina sp. is a natural product known as a natural source of nutraceuticals and bioactive compounds, responding to the demand of both food and medicinal products. Cultural conditions are the key point to determine the quality of Spirulina’s products. Under the high NaNO3 concentration supplied Zarrouk medium (5.0 g/L), the dry biomass (0.60 g/L) and the protein content (34.41%) which were higher than those under low NaNO3 concentration supplied medium (1.25 g/L and 2.5g/L, the antioxidant capacity, protein content, and amino acid profiles were high in both strains of Spirulina sp. from USA and Japan under the cultural condition in which NaNO3 concentration was of 5.0 g/L. In addition, there was a positive correlation between the total phenolic content and the antioxidant capacity of the two strains of Spirulina sp.
Keywords
Spirulina sp., Bradford method, nitrate, protein, amino acid, antioxidant capacity
Article Details
References
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Bartley, M. L., Boeing, W. J., Daniel, D., Dungan, B. N., & Schaub, T. (2016). Optimization of environmental parameters for Nannochloropsis salina growth and lipid content using the response surface method and invading organisms. Journal of Applied Phycology, 28(1),
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Delrue, F., Alaux, E., Moudjaoui, L., Gaignard, C., Fleury, G., Perilhou, A.,… & Sassi, J. F. (2017). Optimization of Arthrospira platensis (Spirulina) Growth: From Laboratory Scale to Pilot Scale. Fermentation, 3(4), 59.
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Esen, M., & ÜREK, R. Ö. (2014). Nitrate and iron nutrition effects on some nitrate assimilation enzymes and metabolites in Spirulina platensis. Turkish Journal of Biology, 38(5), 690-700.
Felig, P., Pozefsky, T., Marliss, E., & Cahill, G. F., Jr. (1970). Alanine: key role in gluconeogenesis. Science, 167(3920), 1003-1004.
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.
Guillard RRL. (1973). Culture Methods and Growth Measurements. Chambridge: Chambridge University Pres.
Hajimahmoodi, M., Faramarzi, M. A., Mohammadi, N., Soltani, N., Oveisi, M. R., & Nafissi-Varcheh, N. (2010). Evaluation of antioxidant properties and total phenolic contents of some strains of microalgae. Journal of Applied Phycology, 22(1), 43-50.
Ho, S. H., Ye, X., Hasunuma, T., Chang, J. S., & Kondo, A. (2014). Perspectives on engineering strategies for improving biofuel production from microalgae--a critical review. Biotechnol Adv, 32(8), 1448-1459. doi:10.1016/j.biotechadv.2014.09.002
Ito, T., Tanaka, M., Shinkawa, H., Nakada, T., Ano, Y., Kurano, N.,… & Tomita, M. (2013). Metabolic and morphological changes of an oil accumulating trebouxiophycean alga in nitrogen-deficient conditions. Metabolomics, 9(1), 178-187. doi:10.1007/s11306-012-0463-z
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Kim, D. G., & Bum Hur, S. (2013). Growth and fatty acid composition of three heterotrophic Chlorella species. Algae, 28(1), 101-109. doi:10.4490/algae.2013.28.1.101
Konickova, R., Vankova, K., Vanikova, J., Vanova, K., Muchova, L., Subhanova, I.,…& Vitek, L. (2014). Anti-cancer effects of blue-green alga Spirulina platensis, a natural source of bilirubin-like tetrapyrrolic compounds. Ann Hepatol, 13(2), 273-283.
Lim, S. N., Cheung, P. C., Ooi, V. E., & Ang, P. O. (2002). Evaluation of antioxidative activity of extracts from a brown seaweed, Sargassum siliquastrum. J Agric Food Chem, 50(13),
3862-3866.
Levasseur M., Thompson P. A., & Harrison, P. J. (1993). Physiological acclimation of marine phytoplankton to different nitrogen sources. J. Phycol, 29(5), 587-595.
Miranda, M. S., Cintra, R. G., Barros, S. B., & Mancini Filho, J. (1998). Antioxidant activity of the microalga Spirulina maxima. Braz J Med Biol Res, 31(8), 1075-1079.
Norici, A., Dalsass, A., & Giordano, M. (2002). Role of phosphoenolpyruvate carboxylase in anaplerosis in the green microalga Dunaliella salina cultured under different nitrogen regimes. Physiol Plant, 116(2), 186-191.
Pandey J. P., Tiwari A., & Mishra, R. M. (2010). Evaluation of Biomass Production of Spirulina maxima on Different Reported Media. J. Algal Biomass Utln., 1(3), 70-81.
Pinero Estrada, J. E., Bermejo Bescos, P., & Villar del Fresno, A. M. (2001). Antioxidant activity of different fractions of Spirulina platensis protean extract. Farmaco, 56(5-7), 497-500.
Pruvost, J., Van Vooren, G., Cogne, G., & Legrand, J. (2009). Investigation of biomass and lipids production with Neochloris oleoabundans in photobioreactor. Bioresource Technology, 100(23), 5988-5995. doi:https://doi.org/10.1016/j.biortech.2009.06.004
Sahu, R., Kar, M., & Routray, R. (2013). DPPH Free radical scavenging activity of some leafy vegetables used by tribals of Odisha. India. Journal of Medicinal Plants Studies, 4(1), 21-27.
Schwartz J., G., S., & Suda D. Growth. (1988). Inhibition and destruction of oral cancer cells by extracts from spirulina. Cancer & Nutrition, 11(2), 127-134.
Sharoba, A. M. (2014). Nutritional value of spirulina and its use in the preparation of some complementary baby food formulas. Journal of Food and Dairy Sciences, Mansoura University, 8, 517-538.
Sukenik, A., Zmora, O., & Carmeli, Y. (1993). Biochemical quality of marine unicellular algae with special emphasis on lipid composition. II. Nannochloropsis sp. Aquaculture, 117(3), 313-326. doi:https://doi.org/10.1016/0044-8486(93)90328-V
Thompson, G. A. (1996). Lipids and membrane function in green algae. Biochimica et Biophysica Acta (BBA) - Lipids and Lipid Metabolism, 1302(1), 17-45. doi:https://doi.org/10.1016/0005-2760(96)00045-8
Tran, D., Doan, N., Louime, C., Giordano, M., & Portilla, S. (2014). Growth, antioxidant capacity and total carotene of Dunaliella salina DCCBC15 in a low cost enriched natural seawater medium. World J Microbiol Biotechnol, 30(1), 317-322. doi:10.1007/s11274-013-1413-2
Uslu, L., Isik, O., Koç, K., & Göksan, T. (2011). The effects of nitrogen deficiencies on the lipid and protein contents of Spirulina platensis. African Journal of Biotechnology, 10(3), 386-389.
Wan, M.-X., Wang, R. M., Xia, J. L., Rosenberg, J. N., Nie, Z. Y., Kobayashi, N.,… & Betenbaugh, M. J. (2012). Physiological evaluation of a new Chlorella sorokiniana isolate for its biomass production and lipid accumulation in photoautotrophic and heterotrophic cultures. Biotechnology and Bioengineering, 109(8), 1958-1964. doi:10.1002/bit.24477
Yaltirak, T., Aslim, B., Ozturk, S., & Alli, H. (2009). Antimicrobial and antioxidant activities of Russula delica Fr. Food Chem Toxicol, 47(8), 2052-2056. doi:10.1016/j.fct.2009.05.029
Yen, H. W., Hu, I. C., Chen, C.Y., & Chang, J.S. (2014). Chapter 2 - Design of Photobioreactors for Algal Cultivation. In A. Pandey, D.J. Lee, Y. Chisti, & C. R. Soccol (Eds.), Biofuels from Algae (pp. 23-45). Amsterdam: Elsevier.
Zhu C. J., & Lee., K., Y. (1997). Determination of biomass dry weight of marine microalgae. Journal of Applied Phycology, 9(2), 189-194.
Adb El Baky, H., K. El Baz, F., & El baroty, G. (2009). Production of phenolic compounds from Spirulina maxima microalgae and its protective effects in vitro toward hepatotoxicity model. African journal of pharmacy and pharmacology, 3(4), 133-139.
Albayrak, S., Aksoy, A., Sagdic, O., & Hamzaoglu, E. (2010). Compositions, antioxidant and antimicrobial activities of Helichrysum (Asteraceae) species collected from Turkey. Food chemistry, 119(1), 114-122. doi:https://doi.org/10.1016/j.foodchem.2009.06.003
Bartley, M. L., Boeing, W. J., Daniel, D., Dungan, B. N., & Schaub, T. (2016). Optimization of environmental parameters for Nannochloropsis salina growth and lipid content using the response surface method and invading organisms. Journal of Applied Phycology, 28(1),
15-24. doi:10.1007/s10811-015-0567-8
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.
Cai, T., Park, S. Y., & Li, Y. (2013). Nutrient recovery from wastewater streams by microalgae: Status and prospects. Renewable and Sustainable Energy Reviews, 19, 360-369. doi:https://doi.org/10.1016/j.rser.2012.11.030
Colla, L., Badiale-Furlong, E., & Costa, J. A. (2007). Antioxidant properties of Spirulina (Arthospira) platensis cultivated under different temperatures and nitrogen regimes. Brazilian Archives Of Biology And Technology, 50(1). doi:10.1590/S1516-89132007000100020
Delrue, F., Alaux, E., Moudjaoui, L., Gaignard, C., Fleury, G., Perilhou, A.,… & Sassi, J. F. (2017). Optimization of Arthrospira platensis (Spirulina) Growth: From Laboratory Scale to Pilot Scale. Fermentation, 3(4), 59.
Deng, R., & Chow, T. J. (2010). Hypolipidemic, antioxidant, and antiinflammatory activities of microalgae Spirulina. Cardiovasc Ther, 28(4), e33-45. doi:10.1111/j.1755-5922.2010.00200.x
Esen, M., & ÜREK, R. Ö. (2014). Nitrate and iron nutrition effects on some nitrate assimilation enzymes and metabolites in Spirulina platensis. Turkish Journal of Biology, 38(5), 690-700.
Felig, P., Pozefsky, T., Marliss, E., & Cahill, G. F., Jr. (1970). Alanine: key role in gluconeogenesis. Science, 167(3920), 1003-1004.
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.
Guillard RRL. (1973). Culture Methods and Growth Measurements. Chambridge: Chambridge University Pres.
Hajimahmoodi, M., Faramarzi, M. A., Mohammadi, N., Soltani, N., Oveisi, M. R., & Nafissi-Varcheh, N. (2010). Evaluation of antioxidant properties and total phenolic contents of some strains of microalgae. Journal of Applied Phycology, 22(1), 43-50.
Ho, S. H., Ye, X., Hasunuma, T., Chang, J. S., & Kondo, A. (2014). Perspectives on engineering strategies for improving biofuel production from microalgae--a critical review. Biotechnol Adv, 32(8), 1448-1459. doi:10.1016/j.biotechadv.2014.09.002
Ito, T., Tanaka, M., Shinkawa, H., Nakada, T., Ano, Y., Kurano, N.,… & Tomita, M. (2013). Metabolic and morphological changes of an oil accumulating trebouxiophycean alga in nitrogen-deficient conditions. Metabolomics, 9(1), 178-187. doi:10.1007/s11306-012-0463-z
Jonker, R., Engelen, M. P., & Deutz, N. E. (2012). Role of specific dietary amino acids in clinical conditions. Br J Nutr, 108 Suppl 2, S139-148. doi:10.1017/s0007114512002358
Kim, D. G., & Bum Hur, S. (2013). Growth and fatty acid composition of three heterotrophic Chlorella species. Algae, 28(1), 101-109. doi:10.4490/algae.2013.28.1.101
Konickova, R., Vankova, K., Vanikova, J., Vanova, K., Muchova, L., Subhanova, I.,…& Vitek, L. (2014). Anti-cancer effects of blue-green alga Spirulina platensis, a natural source of bilirubin-like tetrapyrrolic compounds. Ann Hepatol, 13(2), 273-283.
Lim, S. N., Cheung, P. C., Ooi, V. E., & Ang, P. O. (2002). Evaluation of antioxidative activity of extracts from a brown seaweed, Sargassum siliquastrum. J Agric Food Chem, 50(13),
3862-3866.
Levasseur M., Thompson P. A., & Harrison, P. J. (1993). Physiological acclimation of marine phytoplankton to different nitrogen sources. J. Phycol, 29(5), 587-595.
Miranda, M. S., Cintra, R. G., Barros, S. B., & Mancini Filho, J. (1998). Antioxidant activity of the microalga Spirulina maxima. Braz J Med Biol Res, 31(8), 1075-1079.
Norici, A., Dalsass, A., & Giordano, M. (2002). Role of phosphoenolpyruvate carboxylase in anaplerosis in the green microalga Dunaliella salina cultured under different nitrogen regimes. Physiol Plant, 116(2), 186-191.
Pandey J. P., Tiwari A., & Mishra, R. M. (2010). Evaluation of Biomass Production of Spirulina maxima on Different Reported Media. J. Algal Biomass Utln., 1(3), 70-81.
Pinero Estrada, J. E., Bermejo Bescos, P., & Villar del Fresno, A. M. (2001). Antioxidant activity of different fractions of Spirulina platensis protean extract. Farmaco, 56(5-7), 497-500.
Pruvost, J., Van Vooren, G., Cogne, G., & Legrand, J. (2009). Investigation of biomass and lipids production with Neochloris oleoabundans in photobioreactor. Bioresource Technology, 100(23), 5988-5995. doi:https://doi.org/10.1016/j.biortech.2009.06.004
Sahu, R., Kar, M., & Routray, R. (2013). DPPH Free radical scavenging activity of some leafy vegetables used by tribals of Odisha. India. Journal of Medicinal Plants Studies, 4(1), 21-27.
Schwartz J., G., S., & Suda D. Growth. (1988). Inhibition and destruction of oral cancer cells by extracts from spirulina. Cancer & Nutrition, 11(2), 127-134.
Sharoba, A. M. (2014). Nutritional value of spirulina and its use in the preparation of some complementary baby food formulas. Journal of Food and Dairy Sciences, Mansoura University, 8, 517-538.
Sukenik, A., Zmora, O., & Carmeli, Y. (1993). Biochemical quality of marine unicellular algae with special emphasis on lipid composition. II. Nannochloropsis sp. Aquaculture, 117(3), 313-326. doi:https://doi.org/10.1016/0044-8486(93)90328-V
Thompson, G. A. (1996). Lipids and membrane function in green algae. Biochimica et Biophysica Acta (BBA) - Lipids and Lipid Metabolism, 1302(1), 17-45. doi:https://doi.org/10.1016/0005-2760(96)00045-8
Tran, D., Doan, N., Louime, C., Giordano, M., & Portilla, S. (2014). Growth, antioxidant capacity and total carotene of Dunaliella salina DCCBC15 in a low cost enriched natural seawater medium. World J Microbiol Biotechnol, 30(1), 317-322. doi:10.1007/s11274-013-1413-2
Uslu, L., Isik, O., Koç, K., & Göksan, T. (2011). The effects of nitrogen deficiencies on the lipid and protein contents of Spirulina platensis. African Journal of Biotechnology, 10(3), 386-389.
Wan, M.-X., Wang, R. M., Xia, J. L., Rosenberg, J. N., Nie, Z. Y., Kobayashi, N.,… & Betenbaugh, M. J. (2012). Physiological evaluation of a new Chlorella sorokiniana isolate for its biomass production and lipid accumulation in photoautotrophic and heterotrophic cultures. Biotechnology and Bioengineering, 109(8), 1958-1964. doi:10.1002/bit.24477
Yaltirak, T., Aslim, B., Ozturk, S., & Alli, H. (2009). Antimicrobial and antioxidant activities of Russula delica Fr. Food Chem Toxicol, 47(8), 2052-2056. doi:10.1016/j.fct.2009.05.029
Yen, H. W., Hu, I. C., Chen, C.Y., & Chang, J.S. (2014). Chapter 2 - Design of Photobioreactors for Algal Cultivation. In A. Pandey, D.J. Lee, Y. Chisti, & C. R. Soccol (Eds.), Biofuels from Algae (pp. 23-45). Amsterdam: Elsevier.
Zhu C. J., & Lee., K., Y. (1997). Determination of biomass dry weight of marine microalgae. Journal of Applied Phycology, 9(2), 189-194.