Nutritional profile, bioactive compounds, and antioxidant activity of microalgal strain, Amphora sp., isolated from the Cape coastal waters, South Africa
DOI:
https://doi.org/10.5327/fst.76222Keywords:
diatom, marine microalgae, bioactive compounds, antioxidant activity, nutritional compositionAbstract
Microalgae represent a potential source of renewable nutrition, and there is growing global interest in algae-based dietary supplements. However, the selection of suitable and indigenous microalgae species is a fundamental requirement in developing value-added bioactive compounds in the food industry. The proximate composition, fatty acids, amino acids, and mineral profile, as well as bioactive compounds and antioxidant activity of an unexplored diatom strain, Amphora sp. WCA23.2, isolated from the Cape coastal waters, South Africa, were evaluated as a potential nutraceutical. The Amphora sp. WCA23.2 biomass had 44.2% ash, 28% carbohydrates, 15% protein, and 4% lipids. The fatty acid profile revealed that the diatom accumulates a significant amount of omega-7-monounsaturated fatty acid palmitoleic acid (24.50 mg/g), while the amino acid profile demonstrated that it contained all the nine essential amino acids. The antioxidant activities of the diatom extracts showed that the methanolic extract displayed the highest DPPH radical scavenging activity (1.90±0.11 mg GAE/g dry weight (DW)) and the lowest IC50 in all the antioxidant indices evaluated. These results suggest that Amphora sp. WCA23.2 biomass and its extracts can be utilized as a potential source of ingredients and nutraceuticals in food systems for humans.
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Ahmed, F., Fanning, K., Netzel, M., Turner, W., Li, Y., & Schenk, P. M. (2014). Profiling of carotenoids and antioxidant capacity of microalgae from subtropical coastal and brackish waters. Food Chemistry, 165, 300-306. https://doi.org/10.1016/j.foodchem.2014.05.107
Association of Analytical Chemists International (AOAC). (2005). Official methods of analysis of the Association of Analytical Chemists International. AOAC.
Bastos, C. R., Maia, I. B., Pereira, H., Navalho, J., & Varela, J. C. (2022). Optimisation of Biomass Production and Nutritional Value of Two Marine Diatoms (Bacillariophyceae), Skeletonema costatum and Chaetoceros calcitrans. Biology, 11(4), 594. https://doi.org/10.3390/biology11040594
Becker, E. W. (1994). Microalgae: biotechnology and microbiology (Vol. 10). Cambridge University Press.
Benzie, I. F. F., & Strain, J. J. (1996). The Ferric Reducing Ability of Plasma (FRAP) as a Measure of “Antioxidant Power”: The FRAP Assay. Analytical Biochemistry, 239(1), 70-76. https://doi.org/10.1006/abio.1996.0292
Bhattacharjya, R., Marella, T. K., Tiwari, A., Saxena, A., Singh, P. K., & Mishra, B. (2020). Bioprospecting of marine diatoms Thalassiosira, Skeletonema and Chaetoceros for lipids and other value-added products. Bioresource Technology, 318, 124073. https://doi.org/10.1016/j.biortech.2020.124073
Bidlingmeyer, B., Cohen, S., & Tarvin, T. (1984). The PICO-TAG method for amino acid determination. Journal of Chromatography, 33, 93-104.
Borowitzka, M. A. (2013). Species and strain selection. In M. A. Borowitzka & N. R. Moheimani (eds.), Algae for biofuels and energy (pp. 77-89). Springer.
Boukhris, S., Athmouni, K., Hamza-Mnif, I., Siala-Elleuch, R., Ayadi, H., Nasri, M., & Sellami-Kamoun, A. (2017). The potential of a brown microalga cultivated in high salt medium for the production of high-value compounds. BioMed Research International, 2017, 4018562. https://doi.org/10.1155/2017/4018562
Brand-Williams, W., Cuvelier, M.-E., & Berset, C. (1995). Use of a free radical method to evaluate antioxidant activity. LWT-Food science and Technology, 28(1), 25-30. https://doi.org/10.1016/S0023-6438(95)80008-5
Brown, M. R. (1991). The amino-acid and sugar composition of 16 species of microalgae used in mariculture. Journal of Experimental Marine Biology and Ecology, 145(1), 79-99. https://doi.org/10.1016/0022-0981(91)90007-J
Burja, A. M., Armenta, R. E., Radianingtyas, H., & Barrow, C. J. (2007). Evaluation of fatty acid extraction methods for Thraustochytrium sp. ONC-T18. Journal of Agricultural and Food Chemistry, 55(12), 4795-4801. https://doi.org/10.1021/jf070412s
Chandra, R., Das, P., Vishal, G., & Nagra, S. (2019). Factors affecting the induction of UV protectant and lipid productivity in Lyngbya for sequential biorefinery product recovery. Bioresource Technology, 278, 303-310. https://doi.org/10.1016/j.biortech.2019.01.084
Cheng, D., Li, D., Yuan, Y., Zhou, L., Li, X., Wu, T., Wang, L., Zhao, Q., Wei, W., & Sun, Y. (2017). Improving carbohydrate and starch accumulation in Chlorella sp. AE10 by a novel two-stage process with cell dilution. Biotechnology for Biofuels, 10(1), 75. https://doi.org/10.1186/s13068-017-0753-9
Chu, W.-L., Lim, Y.-W., Radhakrishnan, A. K., & Lim, P.-E. (2010). Protective effect of aqueous extract from Spirulina platensis against cell death induced by free radicals. BMC Complementary and Alternative Medicine, 10, 53. https://doi.org/10.1186/1472-6882-10-53
Cui, Y., Thomas-Hall, S. R., Chua, E. T., & Schenk, P. M. (2021). Development of a Phaeodactylum tricornutum biorefinery to sustainably produce omega-3 fatty acids and protein. Journal of Cleaner Production, 300, 126839. https://doi.org/10.1016/j.jclepro.2021.126839
Darwish, R., Gedi, M. A., Akepach, P., Assaye, H., Zaky, A. S., & Gray, D. A. (2020). Chlamydomonas reinhardtii is a potential food supplement with the capacity to outperform Chlorella and Spirulina. Applied Sciences, 10(19), 6736. https://doi.org/10.3390/app10196736
Debnath, C., Bandyopadhyay, T. K., Bhunia, B., Mishra, U., Narayanasamy, S., & Muthuraj, M. (2021). Microalgae: Sustainable resource of carbohydrates in third-generation biofuel production. Renewable and Sustainable Energy Reviews, 150, 111464. https://doi.org/10.1016/j.rser.2021.111464
Fox, J. M., & Zimba, P. V. (2018). Minerals and Trace Elements in Microalgae. In I. A. Levine & J. Fleurence (Eds.), Microalgae in Health and Disease Prevention (pp. 177-193). Academic Press. https://doi.org/10.1016/B978-0-12-811405-6.00008-6
Gebhardt, S. E. (2002). Nutritive value of foods. US Department of Agriculture, Agricultural Research Service.
Gillingham, L. G., Harris-Janz, S., & Jones, P. J. (2011). Dietary monounsaturated fatty acids are protective against metabolic syndrome and cardiovascular disease risk factors. Lipids, 46(3), 209-228. https://doi.org/10.1007/s11745-010-3524-y
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. https://doi.org/10.1007/s10811-012-9804-6
Gügi, B., Le Costaouec, T., Burel, C., Lerouge, P., Helbert, W., & Bardor, M. (2015). Diatom-specific oligosaccharide and polysaccharide structures help to unravel biosynthetic capabilities in diatoms. Marine Drugs, 13(9), 5993-6018. https://doi.org/10.3390/md13095993
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. https://doi.org/10.1007/s10811-009-9424-y
Hemalatha, A., Girija, K., Parthiban, C., Saranya, C., & Anantharaman, P. (2013). Antioxidant properties and total phenolic content of a marine diatom, Navicula clavata and green microalgae, Chlorella marina and Dunaliella salina. Advanced Applied Science Research, 4(5), 151-157.
Hossain, M. F., Ratnayake, R. R., Meerajini, K., & Wasantha Kumara, K. (2016). Antioxidant properties in some selected cyanobacteria isolated from fresh water bodies of Sri Lanka. Food Science & Nutrition, 4(5), 753-758. https://doi.org/10.1002/fsn3.340
Kent, M., Welladsen, H. M., Mangott, A., & Li, Y. (2015). Nutritional evaluation of Australian microalgae as potential human health supplements. PloS One, 10(2), e0118985. https://doi.org/10.1371/journal.pone.0118985
Lafarga, T. (2019). Effect of microalgal biomass incorporation into foods: Nutritional and sensorial attributes of the end products. Algal Research, 41, 101566. https://doi.org/10.1016/j.algal.2019.101566
Lee, S.-H., Karawita, R., Affan, A., Lee, J.-B., Lee, K.-W., Lee, B.-J., Kim, D.-W., & Jeon, Y.-J. (2009). Potential of Benthic Diatoms Achnanthes longipes, Amphora coffeaeformisand Navicula sp.(Bacillariophyceae) as Antioxidant Sources. Algae, 24(1), 47-55. https://doi.org/10.4490/algae.2009.24.1.047
Lichtenthaler, H. K. (1987). Chlorophylls and carotenoids, the pigments of photosynthetic biomembranes. In R. Douce, L. Packer (Eds.), Methods in Enzymology (pp. 350-382). Academic Press. https://doi.org/10.1016/0076-6879(87)48036-1
Maltsev, Y., & Maltseva, K. (2021). Fatty acids of microalgae: Diversity and applications. Reviews in Environmental Science and Bio/Technology, 20(2), 515-547. https://link.springer.com/article/10.1007/s11157-021-09571-3
Mata, T. M., Martins, A. A., Oliveira, O., Oliveira, S., Mendes, A. M., & Caetano, N. S. (2016). Lipid content and productivity of Arthrospira platensis and Chlorella vulgaris under mixotrophic conditions and salinity stress. Chemical Engineering Transactions, 49, 187-192. https://doi.org/10.3303/CET1649032
Mekkawy, I. A., Mahmoud, U. M., Moneeb, R. H., & Sayed, A. E.-D. H. (2020). Significance assessment of Amphora coffeaeformis in arsenic-induced hemato-biochemical alterations of African catfish (Clarias gariepinus). Frontiers in Marine Science, 7, 191. https://doi.org/10.3389/fmars.2020.00191
Muys, M., Sui, Y., Schwaiger, B., Lesueur, C., Vandenheuvel, D., Vermeir, P., & Vlaeminck, S. E. (2019). High variability in nutritional value and safety of commercially available Chlorella and Spirulina biomass indicates the need for smart production strategies. Bioresource Technology, 275, 247-257. https://doi.org/10.1016/j.biortech.2018.12.059
Niccolai, A., Bigagli, E., Biondi, N., Rodolfi, L., Cinci, L., Luceri, C., & Tredici, M. R. (2017). In vitro toxicity of microalgal and cyanobacterial strains of interest as food source. Journal of Applied Phycology, 29(1), 199-209. https://doi.org/10.1007/s10811-016-0924-2
Obata, T., Fernie, A. R., & Nunes-Nesi, A. (2013). The central carbon and energy metabolism of marine diatoms. Metabolites, 3(2), 325-346. https://doi.org/10.3390/metabo3020325
Prieto, P., Pineda, M., & Aguilar, M. (1999). Spectrophotometric quantitation of antioxidant capacity through the formation of a phosphomolybdenum complex: specific application to the determination of vitamin E. Analytical Biochemistry, 269(2), 337-341. https://doi.org/10.1006/abio.1999.4019
Qazi, M. W., Sousa, I. G., Nunes, M. C., & Raymundo, A. (2022). Improving the nutritional, structural, and sensory properties of gluten-free bread with different species of microalgae. Foods, 11(3), 397. https://doi.org/10.3390/foods11030397
Ranganathan, J., Waite, R., Searchinger, T., & Hanson, C. (2018). How to sustainably feed 10 billion people by 2050, in 21 charts. World Resources Institute.
Rasheed, R., Saadaoui, I., Bounnit, T., Cherif, M., Al Ghazal, G., & Al Jabri, H. (2020). Sustainable food production and nutraceutical applications from Qatar desert chlorella sp. (chlorophyceae). Animals, 10(8), 1413. https://doi.org/10.3390/ani10081413
Re, R., Pellegrini, N., Proteggente, A., Pannala, A., Yang, M., & Rice-Evans, C. (1999). Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radical Biology and Medicine, 26(9-10), 1231-1237. https://doi.org/10.1016/s0891-5849(98)00315-3
Sansone, C., & Brunet, C. (2019). Promises and challenges of microalgal antioxidant production. Antioxidants, 8(7), 199. https://doi.org/10.3390/antiox8070199
Saxena, A., Marella, T. K., Singh, P. K., & Tiwari, A. (2021). Indoor mass cultivation of marine diatoms for biodiesel production using induction plasma synthesized nanosilica. Bioresource Technology, 332, 125098. https://doi.org/10.1016/j.biortech.2021.125098
Tilman, D., Balzer, C., Hill, J., & Befort, B. L. (2011). Global food demand and the sustainable intensification of agriculture. Proceedings of the National Academy of Sciences, 108(50), 20260-20264.
West Suitor, C., & Murphy, S. P. (2013). Nutrition Guidelines to Maintain Health. In A. M. Coulston, C. J. Boushey, & M. G. Ferruzzi (eds.), Nutrition in the Prevention and Treatment of Disease (3ª Edition) (pp. 231-247). Academic Press. https://doi.org/10.1016/B978-0-12-391884-0.00013-5
Wong, J. F., Hong, H. J., Foo, S. C., Yap, M. K. K., & Tan, J. W. (2022). A review on current and future advancements for commercialized microalgae species. Food Science and Human Wellness, 11(5), 1156-1170. https://doi.org/10.1016/j.fshw.2022.04.007
World Health Organization (WHO) (2007). Protein and amino acid requirements in human nutrition. Report of a Joint WHO/FAO/UNU Expert Consultation. WHO Technical Report Series 935. WHO.
Wu, Y., Li, R., & Hildebrand, D. F. (2012). Biosynthesis and metabolic engineering of palmitoleate production, an important contributor to human health and sustainable industry. Progress in Lipid Research, 51(4), 340-349. https://doi.org/10.1016/j.plipres.2012.05.001
Zhou, L., Li, K., Duan, X., Hill, D., Barrow, C., Dunshea, F., Martin, G., & Suleria, H. (2022). Bioactive compounds in microalgae and their potential health benefits. Food Bioscience, 49, 101932. https://doi.org/10.1016/j.fbio.2022.101932
Zhou, X., Bao, X., Zhou, J., Xin, F., Zhang, W., Qian, X., Dong, W., Jiang, M., & Ochsenreither, K. (2021). Evaluating the effect of cultivation conditions on palmitoleic acid‐rich lipid production by Scheffersomyces segobiensis DSM 27193. Biofuels, Bioproducts and Biorefining, 15(6), 1859-1870. https://doi.org/10.1002/bbb.2286