Skip to main content
SpringerLink
Log in

Antioxidant activity and phenolic profile in filamentous cyanobacteria: the impact of nitrogen

  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

In the present study, ethanolic extracts of ten cyanobacterial strains cultivated under different nitrogen conditions were assessed for the phenolic content and antioxidant activity. The amount of detected phenolic compounds ranged from 14.86 to 701.69 μg g−1 dry weight (dw) and HPLC-MS/MS analysis revealed gallic acid, chlorogenic acid, quinic acid, catechin, epicatechin, kaempferol, rutin and apiin. Only catechin, among the detected phenolics, was present in all the tested strains, while quinic acid was the most dominant compound in all the tested Nostoc strains. The results also indicated the possibility of increasing the phenolic content in cyanobacterial biomass by manipulating nitrogen conditions, such as in the case of quinic acid in Nostoc 2S7B from 70.83 to 594.43 μg g−1 dw. The highest radical scavenging activity in DPPH assay expressed Nostoc LC1B with IC50 value of 0.04 ± 0.01 mg mL−1, while Nostoc 2S3B with IC50 = 9.47 ± 3.61 mg mL−1 was the least potent. Furthermore, the reducing power determined by FRAP assay ranged from 8.36 ± 0.08 to 21.01 ± 1.66 mg AAE g−1, and it was significantly different among the tested genera. The Arthrospira strains exhibited the highest activity, which in the case of Arthrospira S1 was approximately twofold higher in comparison to those in nitrogen-fixing strains. In addition to this, statistical analysis has indicated that detected phenolics were not major contributor to antioxidant capacities of tested cyanobacteria. However, this study highlights cyanobacteria of the genera Nostoc, Anabaena, and Arthrospira as producers of antioxidants and phenolics with pharmacological and health-beneficial effects, i.e., quinic acid and catechin in particular.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Abd El-Aty AM, Mohamed AA, Samhan FA (2014) In vitro antioxidant and antibacterial activities of two fresh water cyanobacterial species, Oscillatoria agardhii and Anabaena sphaerica. J Appl Pharm Sci 4:69–75

    Google Scholar 

  • Abd El-Baky HH, El Baz FK, El-Baroty GS (2009) Production of phenolic compounds from Spirulina maxima microalgae and its protective effects. Afr J Biotechnol 8:7059–7067

    CAS  Google Scholar 

  • Agyei D, Danquah MK, Sarethy IP, Pan S (2015) Antioxidative peptides derived from food proteins. In: Rani V, Yadav U (eds) Free radicals in human health and disease. Springer, New Delhi, pp 417–430

    Google Scholar 

  • Al-Hazzani AA, Alshatwi AA (2011) Catechin hydrate inhibits proliferation and mediates apoptosis of SiHa human cervical cancer cells. Food Chem Toxicol 49:3281–3286

    Article  PubMed  CAS  Google Scholar 

  • Al-Rashed SA, Ibrahim MM, El-Gaaly GA, Al-Shehri S, Mostafa A (2016) Evaluation of radical scavenging system in two microalgae in response to interactive stresses of UV-B radiation and nitrogen starvation. Saudi J Biol Sci 23:706–712

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Babaoğlu Aydaş S, Ozturk S, Aslım B (2013) Phenylalanine ammonia lyase (PAL) enzyme activity and antioxidant properties of some cyanobacteria isolates. Food Chem 136:164–169

    Article  PubMed  CAS  Google Scholar 

  • Babić O, Kovač D, Rašeta M, Šibul F, Svirčev Z, Simeunović J (2016) Evaluation of antioxidant activity and phenolic profile of filamentous terrestrial cyanobacterial strains isolated from forest ecosystem. J Appl Phycol 28:2333–2342

    Article  CAS  Google Scholar 

  • Belay A (2013) Biology and industrial production of Arthrospira (Spirulina). In: Richmond A, Hu Q (eds) Handbook of microalgal culture: applied phycology and biotechnology. Blackwell, Oxford, pp 339–358

    Chapter  Google Scholar 

  • Benzie IFF, Strain JJ (1996) The ferric reducing ability of plasma (FRAP) as a measure of antioxidant power: the FRAP assay. Anal Biochem 239:70–76

    Article  PubMed  CAS  Google Scholar 

  • Cepoi L, Rudi L, Miscu V, Cojocari A, Chiriac T, Sadovnic D (2009) Antioxidative activity of ethanol extracts from Spirulina platensis and Nostoc linckia measured by various methods. Analele Universităţii din Oradea, Fascicula Biologie 16:43–48

    Google Scholar 

  • Chen AY, Chen YC (2013) A review of the dietary flavonoid, kaempferol on human health and cancer chemoprevention. Food Chem 138:2099–2107

    Article  PubMed  CAS  Google Scholar 

  • Colla LM, Reinehr CO, Reichert C, Costa JAV (2007) Production of biomass and nutraceutical compounds by Spirulina platensis under different temperature and nitrogen regimes. Bioresour Technol 98:1489–1493

    Article  PubMed  CAS  Google Scholar 

  • Čiž M, Čížová H, Denev P, Kratchanova M, Slavov A, Lojek A (2010) Different methods for control and comparison of the antioxidant properties of vegetables. Food Control 21:518–523

    Article  CAS  Google Scholar 

  • Espin JC, Soler-Rivas C, Wichers HJ (2000) Characterization of the total free radical scavenger capacity of vegetable oils and oil fractions using 2,2-diphenyl-1-picrylhydrazyl radical. J Agric Food Chem 48:648–656

    Article  PubMed  CAS  Google Scholar 

  • Freile-Pelegrín Y, Robledo D (2013) Bioactive phenolic compounds from algae. In: Hernández-Ledesma B, Herrero M (eds) Bioactive compounds from marine foods: plant and animal sources. John Wiley & Sons, Chichester, pp 113–129

    Chapter  Google Scholar 

  • 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. J Appl Phycol 24:1477–1486

    Article  CAS  Google Scholar 

  • Guedes AC, Amaro HM, Barbosa CR, Pereira RD, Malcata FX (2011) Fatty acid composition of several wild microalgae and cyanobacteria, with a focus on eicosapentaenoic, docosahexaenoic and α-linolenic acids for eventual dietary uses. Food Res Int 44:2721–2729

    Article  CAS  Google Scholar 

  • Guedes AC, Gião MS, Seabra R, Ferreira AC, Tamagnini P, Moradas-Ferreira P, Malcata FX (2013) Evaluation of the antioxidant activity of cell extracts from microalgae. Mar Drugs 11:1256–1270

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Ijaz S, Hasnain S (2016) Antioxidant potential of indigenous cyanobacterial strains in relation with their phenolic and flavonoid contents. Nat Prod Res 30:1297–1300

    Article  PubMed  CAS  Google Scholar 

  • Jerez-Martel I, García-Poza S, Rodríguez-Martel G, Rico M, Afonso-Olivares C, Gómez-Pinchetti J (2017) Phenolic profile and antioxidant activity of crude extracts from microalgae and cyanobacteria strains. J Food Qual 4:1–8

    Article  CAS  Google Scholar 

  • Kepekçi RA, Saygideger SD (2012) Enhancement of phenolic compound production in Spirulina platensis by two-step batch mode cultivation. J Appl Phycol 24:897–905

    Article  CAS  Google Scholar 

  • Lefort EC, Blay J (2013) Apigenin and its impact on gastrointestinal cancers. Mol Nutr Food Res 57:126–144

    Article  PubMed  CAS  Google Scholar 

  • Li H-B, Cheng K-W, Wong C-C, Fan K-W, Chen F, Jiang Y (2007) Evaluation of antioxidant capacity and total phenolic content of different fractions of selected microalgae. Food Chem 102:771–776

    Article  CAS  Google Scholar 

  • Li P, Jia J, Zhang D, Xie J, Xu X, Wei D (2014) In vitro and in vivo antioxidant activities of a flavonoid isolated from celery (Apium graveolens L. var. dulce). Food Funct 5:50–56

    Article  PubMed  CAS  Google Scholar 

  • Ma R, Lu F, Bi Y, Hu Z (2015) Effects of light intensity and quality on phycobiliprotein accumulation in the cyanobacterium Nostoc sphaeroides Kützing. Biotechnol Lett 37:1663–1669

    Article  PubMed  CAS  Google Scholar 

  • Machu L, Misurcova L, Ambrozova JV, Orsavova J, Mlcek J, Sochor J, Jurikova T (2015) Phenolic content and antioxidant capacity in algal food products. Molecules 20:1118–1133

    Article  PubMed  CAS  Google Scholar 

  • Milovanović I, Mišan A, Simeunović J, Kovač D, Jambrec D, Mandić A (2015) Determination of volatile organic compounds in selected strains of cyanobacteria. J Chem. https://doi.org/10.1155/2015/969542

  • Miranda MS, Cintra RG, Barros SBM, Mancini-Filho J (1998) Antioxidant activity of the microalga Spirulina maxima. Braz J Med Biol Res 31:1075–1079

    Article  PubMed  CAS  Google Scholar 

  • Mukund S, Sivasubramanian V, Palanisamy M, Chinnu K (2014) In vitro antioxidant and anti-proliferative activity of Phormidium fragile. J Algal Biomass Utln 5:49–57

    Google Scholar 

  • 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 assay. Food Chem 129:139–148

    Article  CAS  Google Scholar 

  • Nunnery JK, Mevers E, Gerwick WH (2010) Biologically active secondary metabolites from marine cyanobacteria. Curr Opin Biotechnol 21:787–793

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ogawa T, Terui G (1970) Studies on the growth of Spirulina platensis: (I) On the pure culture of Spirulina platensis. J Ferment Tech 48:361–367

    Google Scholar 

  • Onofrejová L, Vašíčková J, Klejdus B, Stratil P, Mišurcová L, Kráčmar S, Kopecký J, Vacek J (2010) Bioactive phenols in algae: the application of pressurized-liquid and solid-phase extraction techniques. J Pharm Biomed 51:464–470

    Article  CAS  Google Scholar 

  • Orčić D, Francišković M, Bekvalac K, Svirčev E, Beara I, Lesjak M, Mimica-Dukić N (2014) Quantitative determination of plant phenolics in Urtica dioica extracts by high-performance liquid chromatography coupled with tandem mass spectrometric detection. Food Chem 143:48–53

    Article  PubMed  CAS  Google Scholar 

  • Pero RW, Lund H (2009) In vivo treatment of humans with quinic acid enhances DNA repair and reduces the influence of lifestyle factors on risk to disease. Int J Biotechnol Biochem 5:293–305

    Google Scholar 

  • Ramalho SA, Gualberto NC, Santos Leite Neta MT, Batista RA, Araújo SM, Moreira J, Narain N (2014) Catechin and epicatechin contents in wines obtained from Brazilian exotic tropical fruits. Food Nutr Sci 5:449–457

    CAS  Google Scholar 

  • Rippka R, Deruelles J, Waterbury JB, Herdman M, Stanier RY (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111:1–61

    Google Scholar 

  • Rodriguez-Garcia I, Guil-Guerrero JL (2008) Evaluation of the antioxidant activity of three microalgal species for use as dietary supplements and in the preservation of foods. Food Chem 108:1023–1026

    Article  PubMed  CAS  Google Scholar 

  • Rop O, Mlcek J, Jurikova T, Neugebauerova J, Vabkova J (2012) Edible flowers—a new promising source of mineral elements in human nutrition. Molecules 17:6672–6683

    Article  PubMed  CAS  Google Scholar 

  • Safafar H, van Wagenen J, Møller P, Jacobsen C (2015) Carotenoids, phenolic compounds and tocopherols contribute to the antioxidative properties of some microalgae species grown on industrial wastewater. Mar Drugs 13:7339–7356

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sakač MB, Sedej IJ, Mandić AI, Mišan AČ (2015) Antioksidativna svojstva brašna od heljde –doprinos funkcionalnosti pekarskih, testeničarskih i brašneno-konditorskih proizvoda. Hemijska industrija 69:469–483

    Article  Google Scholar 

  • 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 Geomarine Sci 42:556–564

    Google Scholar 

  • Sharathchandra K, Rajashekhar M (2013) Antioxidant activity in the four species of cyanobacteria isolated from a sulfur spring in the western ghats of Karnataka. Int J Pharm Bio Sci 4:275–285

    Google Scholar 

  • Simeunović J, Bešlin K, Svirčev Z, Kovač D, Babić O (2013) Impact of nitrogen and drought on phycobiliprotein content in terrestrial cyanobacterial strains. J Appl Phycol 25:597–607

    Article  CAS  Google Scholar 

  • Suhail S, Biswas D, Farooqui A, Arif JM, Zeeshan M (2011) Antibacterial and free radical scavenging potential of some cyanobacterial strains and their growth characteristics. J Chem Pharm Res 3:472–478

    Google Scholar 

  • Tanwar B, Modgil R (2012) Flavonoids: dietary occurrence and health benefits. Spatula DD 2:59–68

    Article  Google Scholar 

  • Vaz JA, Heleno SA, Martins A, Almeida GM, Vasconcelos MH, Ferreira IC (2010) Wild mushrooms Clitocybe alexandri and Lepista inversa: in vitro antioxidant activity and growth inhibition of human tumour cell lines. Food Chem Toxicol 48:2881–2884

    Article  PubMed  CAS  Google Scholar 

  • Yu H, Jia S, Dai Y (2009) Growth characteristics of the cyanobacterium Nostoc flagelliforme in photoautotrophic, mixotrophic and heterotrophic cultivation. J Appl Phycol 21:127–133

    Article  CAS  Google Scholar 

Download references

Funding

This study has been supported by the funding of the Ministry of Education, Science and Technological Development, Republic of Serbia (project number: TR 31029) which is greatly acknowledged.

Author information

Authors and Affiliations

  1. Faculty of Sciences, Department of Biology and Ecology, University of Novi Sad, Trg Dositeja Obradovića 3, Novi Sad, 21000, Serbia

    Dajana Blagojević, Olivera Babić, Ljiljana Janjušević & Jelica Simeunović

  2. Faculty of Sciences, Department of Chemistry, Biochemistry and Environmental Protection, University of Novi Sad, Trg Dositeja Obradovića 3, Novi Sad, 21000, Serbia

    Milena Rašeta & Filip Šibul

Authors
  1. Dajana Blagojević
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Olivera Babić
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Milena Rašeta
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Filip Šibul
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ljiljana Janjušević
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jelica Simeunović
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jelica Simeunović.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Blagojević, D., Babić, O., Rašeta, M. et al. Antioxidant activity and phenolic profile in filamentous cyanobacteria: the impact of nitrogen. J Appl Phycol 30, 2337–2346 (2018). https://doi.org/10.1007/s10811-018-1476-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-018-1476-4

Keywords

Search

Navigation