Abstract
Many types of macroalgae contain a wide range of bioactive compounds that have antioxidant potential. However, in contrast to terrestrial plants, only a few studies have reported the antioxidant activity of seaweeds. Therefore, extracts from 26 marine macroalgae species from the south and southeast coasts of Brazil were evaluated for their antioxidant activity, using the 2,2-diphenyl-2-picrylhydrazyl hydrate (DPPH) method and β-carotene/linoleic acid assay, and their total phenolic contents, through Folin–Ciocalteu method. Padina gymnospora, Sargassum vulgare, and Osmundaria obtusiloba presented the highest values of total phenolic content. Using β-carotene bleaching assay, Colpomenia sinuosa, Dictyota sp., Dichotomaria marginata, Ganonema farinosum, and Spyridia clavata presented up to 65 % of antioxidant activity. Some of the extracts showed more than 60 % of inhibition of DPPH in the lowest concentration (0.01 mg/mL), including Amansia sp., Bostrychia tenella, Cryptonemia seminervis, Hypnea musciformis, Plocamium brasiliense (1), and S. clavata. Both Amansia sp., and C. seminervis presented the most relevant antioxidant potential, with percentage of inhibition greater than 70 % in the three tested concentrations. These two species were then analyzed by nuclear magnetic resonance spectroscopy (NMR) and were selected for guided fractionation bioassay. They both presented lipid compounds, fatty acids, esters of fatty acids, triglycerides, and sterols as major components. The fractionation of extracts revealed that the organic fractions were responsible for the antioxidant activity. The results obtained through this work indicate that the analyzed seaweeds are a promising source of compounds with high antioxidant potential.
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Alves MGCF, Dore CMP, Castro AJG, Nascimento MS, Cruz AKM, Soriano EM, Benevides NMB, Leite EL (2011) Antioxidant, cytotoxic and hemolytic effects of sulfated galactans from edible red alga Hypnea musciformis. J Appl Phycol 24:1217–1227
Bitencourt FS, Figueiredo JG, Mota MR, Bezerra CC, Silvestre PP, Vale MR, Nascimento KS, Sampaio AH, Nagano CS, Saker-Sampaio S, Farias WR, Cavada BS, Assreuy AM, de Alencar NM (2008) Antinociceptive and anti-inflammatory effects of a mucin-binding agglutinin isolated from the red marine alga Hypnea cervicornis. Naunyn Schmiedebergs Arch Pharmacol 377:139–48
Cano A, Hernández-Ruíz J, García-Cánovas F, Acosta M, Arnao MB (1998) An end-point method for estimation of the total antioxidant activity in plant material. Phytochem Anal 9:196–202
Cechinel Filho V, Yunes RA (1998) Estudo químico de plantas medicinais orientado para a análise biológica. Obtenção, determinação e modificação estrutural de compostos bioativos. In: Yunes RA, Calixto JB (eds) Plantas medicinais sob a ótica da química medicinal moderna, 1st edn. Argos, Chapecó, pp 97–104
Costa LS, Fidelis GP, Cordeiro SL, Oliveira RM, Sabry DA, Câmara RB, Nobre LT, Costa MS, Almeida-Lima J, Farias EH, Leite EL, Rocha HA (2010) Biological activities of sulfated polyssacharides from tropical seaweeds. Biomed Pharmacother 64:21–28
Duarte ME, Noseda DG, Noseda MD, Tulio S, Pujol CA, Damonte EB (2001) Inhibitory effect of sulfated galactans from the marine alga Bostrychia montagnei on herpes simplex virus replication in vitro. Phytomedicine 8:53–8
Ferreira WJ, Amaro R, Cavalcanti DN, de Rezende CM, da Silva VA, Barbosa JE, Paixão IC, Teixeira VL (2010) Anti-herpetic activities of chemical components from the Brazilian red alga Plocamium brasiliense. Nat Prod Commun 5:1167–1170
Fitzgerald C, Gallagher E, Tasdemir D, Hayes M (2011) J Agric Food Chem 59:6829–6836
Jang-Kyoung H, Lee-Bong H, Choi-Byoung W, Lee-Hyi S, Shin-Jong H (2005) Chromenes from the brown alga Sargassum siliquastrum. J Nat Prod 68:719–23
Karagözler A, Erdag B, Emek Y, Uygun D (2008) Antioxidant activity and proline content of leaf extracts from Dorystoechas hastata. Food Chem 111:400–407
Kelman D, Posner EK, McDermi KJ, Tabandera NK, Wright PR, Wright AD (2012) Antioxidant activity of Hawaiian marine algae. Mar Drugs 10:403–416
Kohen R, Nyska A (2002) Oxidation of biological systems: oxidative stress phenomena, antioxidants, redox reactions, and methods for their quantification. Toxicol Pathol 31:620–650
Kuda T, Ikemori T (2009) Minerals, polysaccharides and antioxidant properties of aqueous solutions obtained from macroalgal beach-casts in the Noto Peninsula, Ishikawa, Japan. Food Chem 112:575–581
Langebartels C, Wohlgemuth H, Kschieschan S, Grün S, Sandermann H (2002) Oxidative burst and cell death in ozone-exposed plants. Plant Physiol Biochem 40:567–575
Liu M, Hansen PE, Lin X (2011) Bromophenols in marine algae and their bioactivities. Mar Drugs 9:1273–1292
Marco GJ (1968) A rapid method for evaluation of antioxidants. J Am Oil Chem Soc 45:594–598
Matanjun P, Mohamed S, Mustapha NM, Muhammad K, Ming CH (2008) Antioxidant activities and phenolics content of eight species of seaweeds from north Borneo. J Appl Phycol 20:367–373
Matsukawa R, Dubinsky Z, Kishimoto E, Masaki K, Masuda Y, Takeuchi T, Chihaara M, Yamamoto Y, Niki E, Karube I (1997) A comparison of screening methods for antioxidant activity in seaweeds. J Appl Phycol 9:29–35
Miller HE (1971) A simplified method for the evaluation of antioxidants. J Am Oil Chem Soc 48:91
Molyneux P (2004) The use of the stable free radical diphenylpicrylhydrazyl (DPPH) for estimating antioxidant activity. Songklanakarin J Sci Technol 26:211–219
Nahas R, Abatis D, Anagnostopoulou MA, Kefalas P, Vagias C, Roussis V (2007) Radical-scavenging activity of Aegean Sea marine algae. Food Chem 102:577–581
Neushul M (1990) Antiviral carbohydrates from marine red algae. Hydrobiologia 204/205:99–104
Neves SA, Freitas ALP, Sousa BW, Rocha MLA, Correia MVO, Sampaio DA, Viana GSB (2007) Antinociceptive properties in mice of a lectin isolated from the marine alga Amansia multifida Lamouroux. Braz J Med Biol Res 40:127–134
Nishida TA (1996) A method for screening potential antioxidant activity. J Biotech 51:149–155
Peng J, Yuan J, Wu C, Wang J (2011) Fucoxanthin, a marine carotenoid present in brown seaweeds and diatoms: metabolism and bioactivities relevant to human health. Mar Drugs 9:1806–1828
Reische DW, Lillard DA, Eitenmiller RR (2002) Antioxidants. In: Akoh CC, Min DB (eds) Food lipids. Marcel Dekker, New York, pp 489–516
Rocha FD, Pereira RC, Kaplan MAC, Teixeira VL (2007) Produtos naturais de algas marinhas e seu potencial antioxidante. Rev Bras Farmacogn 17:631–639
Ruberto G, Baratta MT, Biondi DM, Amico V (2001) Antioxidant activity of extracts of the marine algal genus Cystoseira in a micellar model system. J Appl Phycol 13:403–407
Sachindra N, Sato E, Maeda H, Hosokawa M, Niwano Y, Kohno M (2007) Radical scavenging and singlet oxygen quenching activity of marine carotenoid fucoxanthin and its metabolites. J Agric Food Chem 55:8516–8522
Shanab SM, Shalaby EA, El-Fayoumy (2011) Enteromorpha compressa exhibits potent antioxidant activity. J Biomed Biotech 2011:1–11
Sharma YK, Davis KR (1997) The effects of ozone on antioxidant responses in plants. Free Radical Biol Med 23:480–488
Shibata T, Ishimaru K, Kawaguchi S, Yoshikawa H, Hama Y (2008) Antioxidant activities of phlorotannins isolated from Japanese Laminariaceae. J Appl Phycol 20:705–711
Sousa MB, Pires KMS, Alencar DB, Sampaio AH, Saker-Sampaio S (2008) α- and β-carotene, and α-tocopherol in fresh seaweeds. Ciênc Tecnol Aliment 28:953–958
Subbiah M, Sundaresan B (2012) Antitumor activity of Chondrococcus hornemanni and Spyridia fusiformis on Dalton's lymphoma ascites in mice. Bangladesh J Pharmacol 7.
Sultana B, Anwar F, Przybylski R (2007) Antioxidant activity of phenolic components present in barks of Azadirachta indica, Terminalia arjuna, Acacia nilotica, and Eugenia jambolana Lam. trees. Food Chem 104:1106–14
Tait A, Ganzerli S, Di Bella M (1996) Synthesis and free radical scavenging activity of 4-(2H-1,2,4-benzothiadiazine-1,1-dioxide-3-yl)-2,6-bis(1,1-dimethylethyl)phenols. Tetrahedron 52:1287–1296
Takamatsu S, Hodges TW, Rajbhandari I, Gerwick WH, Hamann MT, Nagle DG (2003) Marine natural products as novel antioxidant prototypes. J Nat Prod 66:605–608
Talarico LB, Zibetti RG, Faria PC, Scolaro LA, Duarte ME, Noseda MD, Pujol CA, Damonte EB (2004) Anti-herpes simplex virus activity of sulfated galactans from the red seaweeds Gymnogongrus griffithsiae and Cryptonemia crenulata. Int J Biol Macromol 34:63–71
Targett NM, Arnold TM (1998) Predicting the effects of brown algal phlorotannins on marine herbivores in tropical and temperate oceans. J Phycol 34:195–205
Thomas NV, Kim S (2011) Potential pharmacological applications of polyphenolic derivatives from marine brown algae. Inv Toxic Pharmacology 32:325–335
Tovar CZ, Ballantine DL (2000) Multiple antimicrobial activities of the marine alga Spyridia filamentosa (Ceramiaceae, Rhodophyta). Bot Mar 43:233–238
Vatan O, Celikler S, Yildiz G (2011) In vitro antigenotoxic and anti-oxidative capacity of Hypnea musciformis (Wulfen) Lamour. Extract in human lymphocytes. Afr J Biotechnol 10:484–490
Wu XJ, Hansen C (2008) Antioxidant capacity, phenolic content, polysaccharide content of Lentinus edodes grown in whey permeate based submerged culture. J Food Sci 73:M1–M8
Yan XJ, Nagata T, Fan X (1998) Antioxidative activities in some seaweeds. Plant Food Hum Nutr 52:253–262
Yan X, Chuda Y, Suzuki M, Nagata T (1999) Fucoxanthin as the major antioxidant in Hijikia fusiformis, a common edible seaweed. Biosci Biotech Biochem 63:605–607
Zhang W, Duan X, Huang H, Zhang Y, Wang B (2007) Evaluation of 28 marine algae from the Qingdao coast for antioxidative capacity and determination of antioxidant efficiency and total phenolic content of fractions and subfractions derived from Symphyocladia latiuscula (Rhodomelaceae). J Appl Phycol 19:97–108
Zubia M, Deslandes E (2008) Alginate, mannitol, phenolic compounds and biological activities of two range-extending brown algae, Sargassum mangarevense and Turbinaria ornata (Phaeophyta: Fucales), from Thaiti (French Polynesia). J Appl Phycol 6:1033–1043
Zubia M, Robledo D, Freile-Pelegrin Y (2007) Antioxidant activities in tropical marine macroalgae from the Yucatan Peninsula, Mexico. J Appl Phycol 19:449–458
Zubia M, Fabre MS, Kerjean V, Le Lann K, Stiger-Pouvreau V, Fauchon M, Deslandes E (2009) Antioxidant and antitumoural activities of some Phaeophyta from Brittany coasts. Food Chem 116:693–701
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The authors thank CAPES, CNPq and FAPERJ for financial support.
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Martins, C.D.L., Ramlov, F., Nocchi Carneiro, N.P. et al. Antioxidant properties and total phenolic contents of some tropical seaweeds of the Brazilian coast. J Appl Phycol 25, 1179–1187 (2013). https://doi.org/10.1007/s10811-012-9918-x
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DOI: https://doi.org/10.1007/s10811-012-9918-x