The effect of different concentrations of linoleic acid on physiological responses and production of bioactive compounds in Spirulina platensis

Document Type : Original Article

Authors

1 Department of Biology, Faculty of Basic Sciences, Islamic Azad University, Qaemshahr Branch, Qaemshahr, Iran

2 Department of Biology, Faculty of Basic Science, Islamic Azad University, Sari Branch, Sari, Iran.

3 Department of Biology, Faculty of Basic Sciences, Islamic Azad University, Qaemshahr Branch, Qaemshahr, Iran.

10.22091/ethc.2025.11770.1043

Abstract

Objective: Spirulina platensis is an important source of bioactive compounds, especially plant pigments, phenolic compounds, and antioxidants. In this study, the effect of linoleic acid (30 and 60 μM) on redox and biochemical changes of Spirulina platensis was studied during 3 and 7 days.
Methods: In the present study, the content of superoxide anion, the activity of catalase and peroxidase enzymes, as well as the content of photosynthetic pigments, proline, ascorbate, phenol, and total flavonoids were calculated via spectrophotometer.
Results: The dry weight of algae treated with different concentrations of linoleic acid increased after 3 days. Also, the superoxide anion content increased significantly at a concentration of 30 μM linoleic acid after 7 days. Also, linoleic acid treatment reduced the activity of catalase and peroxidase enzymes. Also, this treatment at a concentration of 60 μM increased the content of total chlorophyll, chlorophyll a, chlorophyll b, and carotenoids. The content of proline and ascorbic acid decreased significantly in response to concentrations of 30 and 60 μM linoleic acid. A significant increase in total phenols and flavonoid content was observed in response to linoleic acid, with the highest content of total phenols and flavonoids observed at a concentration of 60 μM after 7 days.
Conclusion: As a result, it can be suggested that linoleic acid can alter biochemical and metabolic responses in Spirulina platensis by changing the content of superoxide anion as a signaling molecule.

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Main Subjects


Akkol, E. K., Göger, F., Koşar, M., & Başer, K. H. C. (2008). Phenolic composition and biological activities of Salvia halophila and Salvia virgata from Turkey. Food Chemistry108(3), 942-949.
AlFadhly, N. K., Alhelfi, N., Altemimi, A. B., Verma, D. K., Cacciola, F., & Narayanankutty, A. (2022). Trends and technological advancements in the possible food applications of Spirulina and their health benefits: A Review. Molecules27(17), 5584.
Anjum, N. A., Gill, S. S., Corpas, F. J., Ortega-Villasante, C., Hernandez, L. E., Tuteja, N., ... & Fujita, M. (2022). Recent insights into the double role of hydrogen peroxide in plants. Frontiers in Plant Science13, 843274.
Ali, S. K., & Saleh, A. M. (2012). Spirulina-an overview. International Journal of Pharmacy and Pharmaceutical Sciences4(3), 9-15.
Ambati, R. R., Phang, S. M., Ravi, S., & Aswathanarayana, R. G. (2014). Astaxanthin: Sources, extraction, stability, biological activities and its commercial applications—A review. Marine Drugs12(1), 128-152.
Ameri, M., Baron-Sola, A., Khavari-Nejad, R. A., Soltani, N., Najafi, F., Bagheri, A., ... & Hernández, L. E. (2020). Aluminium triggers oxidative stress and antioxidant response in the microalgae Scenedesmus sp. Journal of Plant Physiology246, 153114.
Andrade, L. M., Andrade, C. J., Dias, M., Nascimento, C., & Mendes, M. A. (2018). Chlorella and Spirulina microalgae as sources of functional foods. Nutraceuticals, and Food Supplements6(1), 45-58.
Anvar, A. A., & Nowruzi, B. (2021). Bioactive properties of spirulina: A review. Microbial Bioactechnology4, 134-142.
Bates, A. (1973). Rapid determination of free proline for water-stress studies. Plant Soil, 39, 205-207.
Benelhadj, S., Gharsallaoui, A., Degraeve, P., Attia, H., & Ghorbel, D. (2016). Effect of pH on the functional properties of Arthrospira (Spirulina) platensis protein isolate. Food Chemistry194, 1056-1063.
Bradford, M. M. (1976). A rapid and sensitive method for the quantization of microgram quantities of protein utilizing the principle of protein dye binding. Anal Biochem, 72, 248-254.
Cakmak, I., & Marschner, H. (1992). Magnesium deficiency and high light intensity enhance activities of superoxide dismutase, ascorbate peroxidase, and glutathione reductase in bean leaves. Plant Physiology, 98, 1222-1227.
Costa, J. A. V., Freitas, B. C. B., Rosa, G. M., Moraes, L., Morais, M. G., & Mitchell, B. G. (2019). Operational and economic aspects of Spirulina-based biorefinery. Bioresource Technology292, 121946.
de Pinto, M. C., Francis, D., & De Gara, L. (1999). The redox state of the ascorbate-dehydroascorbate pair as a specific sensor of cell division in tobacco BY-2 cells. Protoplasma209, 90-97.
Deleu, M., Deboever, E., Nasir, M. N., Crowet, J. M., Dauchez, M., Ongena, M., ... & Lins, L. (2019). Linoleic and linolenic acid hydroperoxides interact differentially with biomimetic plant membranes in a lipid specific manner. Colloids and Surfaces B: Biointerfaces175, 384-391.
Dietz, K. J., Turkan, I., & Krieger-Liszkay, A. (2016). Redox-and reactive oxygen species-dependent signaling into and out of the photosynthesizing chloroplast. Plant Physiology171(3), 1541-1550.
Elstner, E. F., & Heupel, A. (1976). Inhibition of nitrite formation from hydroxylammoniumchloride: a simple assay for superoxide dismutase. Analytical Biochemistry, 70, 616-620.
Esmaeili, S., Sharifi, M., Ghanati, F., Soltani, B. M., Samari, E., & Sagharyan, M. (2023). Exogenous melatonin induces phenolic compounds production in Linum album cells by altering nitric oxide and salicylic acid. Scientific Reports13(1), 4158.
Eze, C. N., Onyejiaka, C. K., Ihim, S. A., Ayoka, T. O., Aduba, C. C., Nwaiwu, O., & Onyeaka, H. (2023). Bioactive compounds by microalgae and potentials for the management of some human disease conditions. AIMS Microbiology9(1), 55.
He, M., & Ding, N. Z. (2020). Plant unsaturated fatty acids: multiple roles in stress response. Frontiers in Plant Science11, 562785.
Hou, Q., Ufer, G., & Bartels, D. (2016). Lipid signalling in plant responses to abiotic stress. Plant, Cell & Environment39(5), 1029-1048.
Kachroo, A., & Kachroo, P. (2009). Fatty acid–derived signals in plant defense. Annual Review of Phytopathology47(1), 153-176.
Khalili, Z., Jalili, H., Noroozi, M., & Amrane, A. (2019). Effect of linoleic acid and methyl jasmonate on astaxanthin content of Scenedesmus acutus and Chlorella sorokiniana under heterotrophic cultivation and salt shock conditions. Journal of Applied Phycology31, 2811-2822.
Khalili, Z., Jalili, H., Noroozi, M., Amrane, A., & Ashtiani, F. R. (2020). Linoleic-acid-enhanced astaxanthin content of Chlorella sorokiniana (Chlorophyta) under normal and light shock conditions. Phycologia59(1), 54-62.
Khodamoradi, S., Sagharyan, M., Samari, E., & Sharifi, M. (2022). Changes in phenolic compounds production as a defensive mechanism against hydrogen sulfide pollution in Scrophularia striata. Plant Physiology and Biochemistry177, 23-31.
Kumar, A., Ramamoorthy, D., Verma, D. K., Kumar, A., Kumar, N., Kanak, K. R., ... & Mohan, K. (2022). Antioxidant and phytonutrient activities of Spirulina platensisEnergy Nexus6, 100070.
Kumar, A., Verma, D. K., Kumar, A., Kumar, N., & Ramamoorthy, D. (2019). Influence of Spirulina on food consumption and efficiency of Bombyx mori L. Bivoltive Hybrid race (CSR2 X CSR4). International Journal of Research and Analytical Reviews6(1), 722-740.
Kumar, M., Kulshreshtha, J., & Singh, G. P. (2011). Growth and biopigment accumulation of cyanobacterium Spirulina platensis at different light intensities and temperature. Brazilian Journal of Microbiology42, 1128-1135.
Lichtenthaler, H. K., & Wellburn, A. R. (1985). Determination of total carotenoids and chlorophylls a and b of leaf in different solvents. Biochemical Society Transactions, 11, 591-592.
Lim, G. H., Singhal, R., Kachroo, A., & Kachroo, P. (2017). Fatty acid–and lipid-mediated signaling in plant defense. Annual Review of Phytopathology55(1), 505-536.
Liu, J., Mao, X., Zhou, W., & Guarnieri, M. T. (2016). Simultaneous production of triacylglycerol and high-value carotenoids by the astaxanthin-producing oleaginous green microalga Chlorella zofingiensisBioresource Technology214, 319-327.
Marles, R. J., Barrett, M. L., Barnes, J., Chavez, M. L., Gardiner, P., Ko, R., ... & Griffiths, J. (2011). United States pharmacopeia safety evaluation of SpirulinaCritical Reviews in Food Science and Nutrition51(7), 593-604.
Mohammadi Alasti, F., Fadei Noghani, V., & Khosravi Darani, K. (2015). Influence of different concentrations of Spirulina platensis on some physicochemical and sensory properties of probiotic spinach yoghurt. Food Industry Research, 26(2), 127-143. (in persian)
Niu, X. D., Li, G. R., Kang, Z. H., Huang, J. L., & Wang, G. X. (2012). Photosynthetic characteristics and antioxidant enzyme system in high-chlorophyll rice Gc mutant. Russian Journal of Plant Physiology59, 691-695.
Paliwal, C., Mitra, M., Bhayani, K., Bharadwaj, S. V., Ghosh, T., Dubey, S., & Mishra, S. (2017). Abiotic stresses as tools for metabolites in microalgae. Bioresource Technology244, 1216-1226.
Pancha, I., Chokshi, K., Maurya, R., Trivedi, K., Patidar, S. K., Ghosh, A., & Mishra, S. (2015). Salinity induced oxidative stress enhanced biofuel production potential of microalgae Scenedesmus sp. CCNM 1077. Bioresource Technology189, 341-348.
Pandolfini, T., Gabbrielli, R., & Comparini, C. (1992). Nickel toxicity and peroxidase activity in seedlings of Triticum aestivum L. Plant Cell and Environment, 15, 719-725.
Patel, A. K., Albarico, F. P. J. B., Perumal, P. K., Vadrale, A. P., Nian, C. T., Chau, H. T. B., ... & Singhania, R. R. (2022). Algae as an emerging source of bioactive pigments. Bioresource Technology351, 126910.
Pietryczuk, A., Biziewska, I., Imierska, M., & Czerpak, R. (2014). Influence of traumatic acid on growth and metabolism of Chlorella vulgaris under conditions of salt stress. Plant Growth Regulation73, 103-110.
Qian, H., Xu, J., Lu, T., Zhang, Q., Qu, Q., Yang, Z., & Pan, X. (2018). Responses of unicellular alga Chlorella pyrenoidosa to allelochemical linoleic acid. Science of the Total Environment625, 1415-1422.
Rahim, A., Çakir, C., Ozturk, M., Şahin, B., Soulaimani, A., Sibaoueih, M., ... & El Amiri, B. (2021). Chemical characterization and nutritional value of Spirulina platensis cultivated in natural conditions of Chichaoua region (Morocco). South African Journal of Botany141, 235-242.
Ran, W., Wang, H., Liu, Y., Qi, M., Xiang, Q., Yao, C., ... & Lan, X. (2019). Storage of starch and lipids in microalgae: Biosynthesis and manipulation by nutrients. Bioresource Technology291, 121894.
Randrianarison, G., & Ashraf, M. A. (2017). Microalgae: a potential plant for energy production. Geology, Ecology, and Landscapes1(2), 104-120.
Rosario, J. C., & Josephine, R. M. (2015). Mineral profile of edible algae Spirulina platensisInternational Journal of Current Microbiology and Applied Sciences4(1), 478-483.
Sagharyan, M., & Sharifi, M. (2024). Metabolic and physiological changes induced by exogenous phenylalanine in Linum album Cells. Journal of Plant Growth Regulation, 43, 2785-2801.
Sagharyan, M., Sharifi, M., & Samari, E. (2023). Methyl jasmonate redirects the dynamics of carbohydrates and amino acids toward the lignans accumulation in Linum album cells. Plant Physiology and Biochemistry198, 107677.
Shinde, S., Villamor, J. G., Lin, W., Sharma, S., & Verslues, P. E. (2016). Proline coordination with fatty acid synthesis and redox metabolism of chloroplast and mitochondria. Plant Physiology172(2), 1074-1088.
Sagharyan, M., Sharifi, M., Samari, E., & Karimi, F. (2024). Changes in MicroRNAs expression mediate molecular mechanism underlying the effect of MeJA on the biosynthesis of podophyllotoxin in Linum album cells. Scientific Reports14(1), 30738.
Saxena, I., Srikanth, S., & Chen, Z. (2016). Cross talk between H2O2 and interacting signal molecules under plant stress response. Frontiers in Plant Science7, 570.
Solovchenko, A. E. (2013). Physiology and adaptive significance of secondary carotenogenesis in green microalgae. Russian Journal of Plant Physiology60, 1-13.
Tashackori, H., Sharifi, M., Ahmadian Chashmi, N., Behmanesh, M., Safaie, N., & Sagharyan, M. (2021). Physiological, biochemical, and molecular responses of Linum album to digested cell wall of Piriformospora indica. Physiology and Molecular Biology of Plants27, 2695-2708.
Trotta, T., Porro, C., Cianciulli, A., & Panaro, M. A. (2022). Beneficial effects of spirulina consumption on brain health. Nutrients14(3), 676.
Ugya, A. Y., Imam, T. S., Li, A., Ma, J., & Hua, X. (2020). Antioxidant response mechanism of freshwater microalgae species to reactive oxygen species production: a mini review. Chemistry and Ecology, 36(2), 174-193.
Upchurch, R. G. (2008). Fatty acid unsaturation, mobilization, and regulation in the response of plants to stress. Biotechnology Letters30, 967-977.
Wang, C., Wang, R., Hu, L., Xi, M., Wang, M., Ma, Y., ... & Gao, P. (2023). Metabolites and metabolic pathways associated with allelochemical effects of linoleic acid on Karenia mikimotoiJournal of Hazardous Materials447, 130815.
Wang, X. Q., Li, L. N., Chang, W. R., Zhang, J. P., Gui, L. L., Guo, B. J., & Liang, D. C. (2001). Structure of C-phycocyanin from Spirulina platensis at 2.2 Å resolution: a novel monoclinic crystal form for phycobiliproteins in phycobilisomes. Acta Crystallographica Section D: Biological Crystallography57(6), 784-792.
Xu, S., Yang, S. Q., Yang, Y. J., Xu, J. Z., Shi, J. Q., & Wu, Z. X. (2017). Influence of linoleic acid on growth, oxidative stress and photosynthesis of the cyanobacterium Cylindrospermopsis raciborskiiNew Zealand Journal of Marine and Freshwater Research51(2), 223-236.
Zarrouk, C. (1966). Contribution a l'etude d'une Cyanophycee. Influence de divers facteurs physiques et chimiques sur la croissance et la photosynthese de Spirulina mixima Geitler. (Doctoral dissertation, University of Paris, France).
Zeeshan, M., & Prasad, S. M. (2009). Differential response of growth, photosynthesis, antioxidant enzymes and lipid peroxidation to UV-B radiation in three cyanobacteria. South African Journal of Botany75(3), 466-474.
Zhao, J. (2015). Phospholipase D and phosphatidic acid in plant defence response: from protein–protein and lipid–protein interactions to hormone signalling. Journal of Experimental Botany66(7), 1721-1736.