Abstract
Microalgae can stimulate antioxidant defense systems as adaptive responses to oxidative stress. Therefore, these organisms can be a potential source of natural antioxidants. In this work, forty-two strains of microalgae and cyanobacteria were selected within major groups held in the Coimbra Collection of Algae (ACOI). The antioxidant capacity of ethanolic extracts was determined by two spectrophotometric methods: the 2,2′-azinobis-(3-ethylbenzothiazoline-6-sulfonic acid (ABTS) assay and the 2,2-di(4-tert-octylphenyl)-1-picrylhydrazyl (DPPH) assay. Raspberry extract was used as a reference for comparison purposes. The ABTS assay showed an antioxidant capacity range of 16.61 ± 0.15 to 258.20 ± 0.65 mg Trolox (TE) (100 g)−1 fresh biomass (FW). High antioxidant capacity was observed in Eustigmatophyceae and Chlorophyta, with high results achieved for Vischeria helvetica ACOI 299, Characiopsis aquilonaris ACOI 2424, and Micrasterias radiosa var. elegantior ACOI 1568. The DPPH assay revealed that the eustigmatophytes Characiopsis sp. ACOI 2428, Characiopsis minima ACOI 2426, and V. helvetica ACOI 299, the cryptophyte Cryptomonas pyrenoidifera ACOI 1850, and the chlorophyte Mychonastes homosphaera ACOI 1850 had the highest scavenging activity. Cyanophytes revealed low antioxidant capacity, and mucilagineous strains of different taxa remained undetermined. The assessment of these strains and the broadening of a screening survey of the ACOI Culture Collection are expected to reveal very promising antioxidant-producing strains that may be applied in the field of human nutrition.
Similar content being viewed by others
References
Apak R, Gorinstein S, Böhm V, Schaich KM, Özyürek M, Güçlü K (2013) Methods of measurement and evaluation of natural antioxidant capacity/activity (IUPAC technical report). Pure Appl Chem 85:957–998
Aremu AO, Masondo NA, Stirk WA, Ördög V, Staden JV (2014) Influence of culture age on the phytochemical content and pharmacological activities of five Scenedesmus strains. J Appl Phycol 26:407–415
Benzie IFF (2000) Evolution of antioxidant defence mechanisms. Eur J Nutr 39:53–61
Birben E, Sahiner UM, Sackesen C, Erzurum S, Kalayci O (2012) Oxidative stress and antioxidant defense. World Allergy Organ J 5:9–19
Brand-Williams W, Cuvelier ME, Berset C (1995) Use of free radical method to evaluate antioxidant activity. LWT-Food Sci Technol 28:25–30
Carocho M, Ferreira ICFR (2013) A review on antioxidants, prooxidants and related controversy: natural and synthetic compounds, screening and analysis methodologies and future perspectives. Food Chem Toxicol 51:15–25
Çekiç Ç, Özgen M (2010) Comparison of antioxidant capacity and phytochemical properties of wild and cultivated red raspberry (Rubus idaeus L.). J Food Compos Anal 23:540–544
Cerón MC, García-Malea MC, Rivas J, Acien FG, Fernandez JM, Del Río E, Guerrero MG, 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 Biot 74:1112–1119
Chacón-Lee TL, González-Mariño GE (2010) Microalgae for “healthy” foods—possibilities and challenges. Compr Rev Food Sci F 9:655–675
Chaudhuri D, Ghate NB, Deb S, Panja S, Sarkar R, Rout J, Mandal N (2014) Assessment of the phytochemical constituents and antioxidant activity of a bloom forming microalgae Euglena tuba. Biol Res 47:1–11
Choochote W, Suklampoo L, Ochaikul D (2014) Evaluation of antioxidant capacities of green microalgae. J Appl Phycol 26:43–48
Custódio L, Justo T, Silvestre L, Barradas A, Duarte CV, Pereira H, Barreira L, Rauter AP, Alberício F, Varela J (2012) Microalgae of different phyla display antioxidant, metal chelating and acetylcholinesterase inhibitory activities. Food Chem 131:134–140
Damiani MC, Leonardi PI, Pieroni OI, Cáceres EJ (2006) Ultrastructure of the cyst wall of Haematococcus pluvialis (Chlorophyceae): wall development and behaviour during cyst germination. Phycologia 45:616–623
Floegel A, Kim D, Chung S, Koo S, Chun OK (2011) Comparison of ABTS/DPPH assays to measure antioxidant capacity in popular antioxidant-rich US foods. J Food Compos Anal 24:1043–1048
Goiris K, Muylaert K, Fraeye I, Foubert I, Brabanter JD, Cooman LD (2012) Antioxidant potential of microalgae in relation to their phenolic and carotenoid content. J Appl Phycol 24:1477–1486
Gouveia L, Oliveira AC (2009) Microalgae as a raw material for biofuels production. J Ind Microbiol Biotechnol 36:269–274
Guedes AC, Amaro HM, Malcata FX (2011) Microalgae as a source of high added-value compounds—a brief review of recent work. Biotechnol Prog 27:597–613
Guedes AC, Amaro HM, Gião MS, Malcata FX (2013a) Optimization of ABTS radical cation assay specifically for determination of antioxidant capacity of intracellular extracts of microalgae and cyanobacteria. Food Chem 138:638–643
Guedes AC, Gião MS, Seabra R, Ferreira ACS, Tamagnini P, Moradas-Ferreira P, Malcata FX (2013b) Evaluation of antioxidant activity of cell extracts from microalgae. Mar Drugs 11:1256–1270
Gülçin I, Topal F, Çakmakçl R, Bilsel M, Gören AC, Erdogan U (2011) Pomological features, nutritional quality, polyphenol content analysis, and antioxidant properties of domesticated and 3 wild ecotype forms of raspberries (Rubus idaeus L.). J Food Sci 76:585–593
Gutteridge JMC (1995) Lipid peroxidation and antioxidants as biomarkers of tissue damage. Clin Chem 41:1819–1828
Hajimahmoodi M, Faramarzi MA, Mohammadi N, Soltani N, Oveisi MR, Nafissi-Varcheh N (2010) Evaluation of antioxidant properties and total phenolic contents of some strains of microalgae. J Appl Phycol 22:43–50
Halliwell B (1994) Free radicals, antioxidants and human disease: curiosity, cause or consequence. Lancet 344:721–724
Halliwell B (2007) Biochemistry of oxidative stress. Biochem Soc Trans 35:1147–1150
Hu C, Lin J, Lu F, Chou F, Yang D (2008) Determination of carotenoids in Dunaliella salina cultivated in Taiwan and antioxidant capacity of the algal carotenoid extract. Food Chem 109:439–446
Huang D, Ou B, Prior RL (2005) The chemistry behind antioxidant capacity assays. J Agr Food Chem 53:1841–1856
Kalt W (2005) Effects of production and processing factors on major fruit and vegetable antioxidants. J Food Sci 70:11–19
Kim DO, Padilla-Zakour IO (2004) Jam processing effect on phenolics and antioxidant capacity in anthocyanin-rich fruits: cherry, plum, and raspberry. J Food Sci 69:395–400
Klein BC, Walter C, Lange HA, Buchholz R (2012) Microalgae as natural sources for antioxidative compounds. J Appl Phycol 24:1133–1139
Kobayashi M, Sakamoto Y (1999) Singlet oxygen quenching ability of astaxanthin esters from the green alga Haematococcus pluvialis. Biotechnol Lett 21:265–269
Li H, Cheng K, Wong C, Fan K, Chen F, Jiang Y (2007) Evaluation of antioxidant capacity and total phenolic content of different fractions of selected microalgae. Food Chem 102:771–776
Liu M, Li XQ, Weber C, Lee CY, Brown J, Liu RH (2002) Antioxidant and antiproliferative activities of raspberry. J Agr Food Chem 50:2926–2930
Maadane A, Merghoub N, Ainane T, Arroussi HE, Benhima R, Amzazi S, Bakri Y, Wahby I (2015) Antioxidant activity of some Moroccan marine microalgae: Pufa profile, carotenoids and phenolic content. J Biotechnol 215:13–19
Marxen K, Vanselow KH, Lippemeier S, Hintze R, Ruser A, Hansen U (2007) Determination of DPPH radical oxidation caused by methanolic extracts of some microalgal species by linear regression analysis of spectrophotometric measurements. Sensors 7:2080–2095
Mendes-Pinto MM, Raposo MFJ, Bowen J, Young AJ, Morais R (2001) Evaluation of different cell disruption processes on encysted cells of Haematococcus pluvialis: effects on astaxanthin recovery and implications for bioavailability. J Appl Phycol 13:19–24
Mishra K, Ojha H, Chaudhury NK (2012) Estimation of antiradical properties of antioxidants using DPPH• assay: a critical review and results. Food Chem 130:1036–1043
Müller L, Fröhlich K, Böhm V (2011) Comparative antioxidant activities of carotenoids measured by ferric reducing antioxidant power (FRAP), ABTS bleaching assay (αTEAC), DPPH assay and peroxyl radical scavenging. Food Chem 129:139–148
Natrah FMI, Yusoff FM, Shariff M, Abas F, Mariana NS (2007) Screening of Malaysian indigenous microalgae for antioxidant properties and nutritional value. J Appl Phycol 19:711–718
Ndhlala ER, Moyo M, Van Staden J (2010) Natural antioxidants: fascinating or mythical biomolecules? Molecules 15:6905–6930
Oroian M, Escriche I (2015) Antioxidants: characterization, natural sources, extraction and analysis. Food Res Int 47:10–36
Özgen M, Reese RN, Tulio AZ, Scheerens JC, Miller AR (2006) Modified 2,2-azino-bis-3-ethylbenzothiazoline-6-sulfonic acid (ABTS) method to measure antioxidant capacity of selected small fruits and comparison to ferric reducing antioxidant power (FRAP) and 2,2′-diphenyl-1-picrylhydrazyl (DPPH) methods. J Agr Food Chem 54:1151–1157
Pérez-Jiménez J, Arranz S, Tabernero M, Díaz-Rubio ME, Serrano J, Goňi I, Saura-Calixto F (2008) Updated methodology to determine antioxidant capacity in plant foods, oils and beverages: extraction, measurement and expression of results. Food Res Int 41:274–285
Pinchuk I, Shoval H, Dotan Y, Lichtenberg D (2012) Evaluation of antioxidants: scope, limitations and relevance of assays. Chem Phys Lipids 165:638–647
Prior RL, Wu X, Schaich K (2005) Standardized methods for the determination of antioxidant capacity and phenolics in foods and dietary supplements. J Agr Food Chem 53:4290–4302
Santos LMA, Santos MF (2004) The Coimbra Culture Collection of Algae (ACOI). Nova Hedwigia 79:39–47
Sariburun E, Şahin S, Demir C, Türkben C, Uylaşer V (2010) Phenolic content and antioxidant activity of raspberry and blackberry cultivars. J Food Sci 75:328–335
Šavikin K, Zdunić G, Janković T, Tasić S, Menković N, Stević T, Đorđević B (2009) Phenolic content and radical scavenging capacity of berries and related jams from certificated area in Serbia. Plant Food Hum Nutr 64:212–217
Shalaby EA (2015) Algae as a natural source of antioxidant active compounds. In: Dubey NK (ed) Plants as a source of natural antioxidants. CAB International, United Kingdom, pp. 129–147
Shalaby EA, Shanab SMM (2013) Comparison of DPPH and ABTS assays for determining antioxidant potential of water and methanol extracts of Spirulina platensis. Indian J Mar Sci 45:556–564
Souza VR, Pereira PAP, Silva TLT, Lima LCO, Pio R, Queiroz F (2014) Determination of the bioactive compounds, antioxidant activity and chemical composition of Brazilian blackberry, red raspberry, strawberry, blueberry and sweet cherry fruits. Food Chem 156:362–368
Srivastava AK, Bhargava P, Rai LC (2005) Salinity and copper-induced oxidative damage and changes in the antioxidative defence systems of Anabaena doliolum. World J Microb Biot 21:1291–1298
Takaichi S (2011) Carotenoids in algae: distributions, biosynthesis and functions. Mar Drugs 9:1101–1118
Zafrilla P, Ferreres F, Tomás-Barberán FA (2001) Effect of processing and storage on the antioxidant ellagic acid derivatives and flavonoids of red raspberry (Rubus idaeus) jams. J Agr Food Chem 49:3651–3655
Zakariah NA, Rahman NA, Hamzad F, Jahi TM, Ismail A (2015) Nannochloropsis oculata algae as biofuels: a review. In: Saha B (ed) Environmental science and sustainable development: international conference on environmental science and sustainable development. World Scientific Publishing, Singapore, pp. 217–222
Acknowledgments
We thank Prof. Dr. José Paulo Sousa for advice on statistical analysis of the data and Prof. Dr. Karen Fawley for the English review.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Funding
Raquel Amaral was supported by Portuguese Science and Technology Agency (FCT) through PhD funding SFRH/BD/73359/2010 under POPH/QREN financing program.
Conflict of interest
The authors declare that they have no conflict of interest.
Rights and permissions
About this article
Cite this article
Assunção, M.F.G., Amaral, R., Martins, C.B. et al. Screening microalgae as potential sources of antioxidants. J Appl Phycol 29, 865–877 (2017). https://doi.org/10.1007/s10811-016-0980-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10811-016-0980-7