Journal of Applied Phycology

, Volume 29, Issue 2, pp 865–877 | Cite as

Screening microalgae as potential sources of antioxidants

  • Mariana F. G. AssunçãoEmail author
  • Raquel Amaral
  • Clara B. Martins
  • Joana D. Ferreira
  • Sandrine Ressurreição
  • Sandra Dias Santos
  • Jorge M. T. B. Varejão
  • Lília M. A. Santos


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.


Microalgae Eustigmatophyceae Antioxidant Radical scavenger ABTS DPPH 



We thank Prof. Dr. José Paulo Sousa for advice on statistical analysis of the data and Prof. Dr. Karen Fawley for the English review.


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.


  1. 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 85:957–998CrossRefGoogle Scholar
  2. 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 26:407–415CrossRefGoogle Scholar
  3. Benzie IFF (2000) Evolution of antioxidant defence mechanisms. Eur J Nutr 39:53–61CrossRefPubMedGoogle Scholar
  4. Birben E, Sahiner UM, Sackesen C, Erzurum S, Kalayci O (2012) Oxidative stress and antioxidant defense. World Allergy Organ J 5:9–19CrossRefPubMedPubMedCentralGoogle Scholar
  5. Brand-Williams W, Cuvelier ME, Berset C (1995) Use of free radical method to evaluate antioxidant activity. LWT-Food Sci Technol 28:25–30CrossRefGoogle Scholar
  6. 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 51:15–25CrossRefPubMedGoogle Scholar
  7. 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 23:540–544CrossRefGoogle Scholar
  8. 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 74:1112–1119CrossRefGoogle Scholar
  9. Chacón-Lee TL, González-Mariño GE (2010) Microalgae for “healthy” foods—possibilities and challenges. Compr Rev Food Sci F 9:655–675CrossRefGoogle Scholar
  10. 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 47:1–11CrossRefGoogle Scholar
  11. Choochote W, Suklampoo L, Ochaikul D (2014) Evaluation of antioxidant capacities of green microalgae. J Appl Phycol 26:43–48CrossRefGoogle Scholar
  12. 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 131:134–140CrossRefGoogle Scholar
  13. 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 45:616–623CrossRefGoogle Scholar
  14. 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 24:1043–1048CrossRefGoogle Scholar
  15. 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 24:1477–1486CrossRefGoogle Scholar
  16. Gouveia L, Oliveira AC (2009) Microalgae as a raw material for biofuels production. J Ind Microbiol Biotechnol 36:269–274CrossRefPubMedGoogle Scholar
  17. Guedes AC, Amaro HM, Malcata FX (2011) Microalgae as a source of high added-value compounds—a brief review of recent work. Biotechnol Prog 27:597–613CrossRefPubMedGoogle Scholar
  18. 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 138:638–643CrossRefPubMedGoogle Scholar
  19. 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 11:1256–1270CrossRefPubMedPubMedCentralGoogle Scholar
  20. 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 76:585–593CrossRefGoogle Scholar
  21. Gutteridge JMC (1995) Lipid peroxidation and antioxidants as biomarkers of tissue damage. Clin Chem 41:1819–1828PubMedGoogle Scholar
  22. 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 22:43–50CrossRefGoogle Scholar
  23. Halliwell B (1994) Free radicals, antioxidants and human disease: curiosity, cause or consequence. Lancet 344:721–724CrossRefPubMedGoogle Scholar
  24. Halliwell B (2007) Biochemistry of oxidative stress. Biochem Soc Trans 35:1147–1150Google Scholar
  25. 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 109:439–446CrossRefPubMedGoogle Scholar
  26. Huang D, Ou B, Prior RL (2005) The chemistry behind antioxidant capacity assays. J Agr Food Chem 53:1841–1856CrossRefGoogle Scholar
  27. Kalt W (2005) Effects of production and processing factors on major fruit and vegetable antioxidants. J Food Sci 70:11–19CrossRefGoogle Scholar
  28. 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 69:395–400CrossRefGoogle Scholar
  29. Klein BC, Walter C, Lange HA, Buchholz R (2012) Microalgae as natural sources for antioxidative compounds. J Appl Phycol 24:1133–1139CrossRefGoogle Scholar
  30. Kobayashi M, Sakamoto Y (1999) Singlet oxygen quenching ability of astaxanthin esters from the green alga Haematococcus pluvialis. Biotechnol Lett 21:265–269CrossRefGoogle Scholar
  31. 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 102:771–776CrossRefGoogle Scholar
  32. Liu M, Li XQ, Weber C, Lee CY, Brown J, Liu RH (2002) Antioxidant and antiproliferative activities of raspberry. J Agr Food Chem 50:2926–2930CrossRefGoogle Scholar
  33. 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 215:13–19CrossRefPubMedGoogle Scholar
  34. 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 7:2080–2095CrossRefPubMedCentralGoogle Scholar
  35. 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 13:19–24CrossRefGoogle Scholar
  36. Mishra K, Ojha H, Chaudhury NK (2012) Estimation of antiradical properties of antioxidants using DPPH• assay: a critical review and results. Food Chem 130:1036–1043CrossRefGoogle Scholar
  37. 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 129:139–148CrossRefGoogle Scholar
  38. 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 19:711–718CrossRefGoogle Scholar
  39. Ndhlala ER, Moyo M, Van Staden J (2010) Natural antioxidants: fascinating or mythical biomolecules? Molecules 15:6905–6930CrossRefPubMedGoogle Scholar
  40. Oroian M, Escriche I (2015) Antioxidants: characterization, natural sources, extraction and analysis. Food Res Int 47:10–36CrossRefGoogle Scholar
  41. 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 54:1151–1157CrossRefGoogle Scholar
  42. 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 41:274–285CrossRefGoogle Scholar
  43. Pinchuk I, Shoval H, Dotan Y, Lichtenberg D (2012) Evaluation of antioxidants: scope, limitations and relevance of assays. Chem Phys Lipids 165:638–647CrossRefPubMedGoogle Scholar
  44. 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 53:4290–4302CrossRefGoogle Scholar
  45. Santos LMA, Santos MF (2004) The Coimbra Culture Collection of Algae (ACOI). Nova Hedwigia 79:39–47CrossRefGoogle Scholar
  46. Sariburun E, Şahin S, Demir C, Türkben C, Uylaşer V (2010) Phenolic content and antioxidant activity of raspberry and blackberry cultivars. J Food Sci 75:328–335CrossRefGoogle Scholar
  47. 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 64:212–217CrossRefGoogle Scholar
  48. 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. 129–147Google Scholar
  49. 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 45:556–564Google Scholar
  50. 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 156:362–368CrossRefPubMedGoogle Scholar
  51. 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 21:1291–1298CrossRefGoogle Scholar
  52. Takaichi S (2011) Carotenoids in algae: distributions, biosynthesis and functions. Mar Drugs 9:1101–1118CrossRefPubMedPubMedCentralGoogle Scholar
  53. 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 49:3651–3655CrossRefGoogle Scholar
  54. 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. 217–222Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  • Mariana F. G. Assunção
    • 1
    Email author
  • Raquel Amaral
    • 1
  • Clara B. Martins
    • 1
  • Joana D. Ferreira
    • 1
  • Sandrine Ressurreição
    • 2
  • Sandra Dias Santos
    • 2
  • Jorge M. T. B. Varejão
    • 2
  • Lília M. A. Santos
    • 1
  1. 1.Coimbra Collection of Algae (ACOI), Department of Life SciencesUniversity of CoimbraCoimbraPortugal
  2. 2.Research Center for Natural Resources, Environmental and Society (CERNAS), ESACPolytechnic Institute of CoimbraCoimbraPortugal

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