Abstract
In the present investigation the acetone extracts of three brown marine macroalgae Dictyota dichotoma, Padaina pavonia and Sargassum vulgare were tested for antioxidant, antimicrobial and cytotoxic potential. The antioxidant activity was evaluated by free radical scavenging, superoxide anion radical scavenging and reducing power. P. pavonia extract showed more potent free radical scavenging activity (IC50 = 691.56 µg L−1) than D. dichotoma and S. vulgare extracts. Moreover, the tested extracts had effective reducing power and superoxide anion radical scavenging. The total content of phenol and flavonoid in extracts was examined using Folin–Ciocalteu reagent and aluminium chloride method and the obtained values were expressed as pyrocatechol equivalents, and as rutin equivalents, respectively. Further, the antimicrobial potential was determined by a microdilution method. Among the tested species, the extract of D. diichotoma showed the best antimicrobial activity with minimum inhibitory concentration values ranging from 0.156 to 2.5 mg L−1. Finally, the cytotoxic activity was tested using microculture tetrazolium test on the human colon carcinoma LS174 cells, human lung carcinoma A549 cells, malignant melanoma FemX cells and chronic myelogenous leukaemia K562 cells. The extract of D. dichotoma expressed stronger cytotoxic activity toward tested cell lines with IC50 values ranging from 9.76 to 50.96 µg L−1.

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References
N. Khaled, M. Hiba, C. Asma, Antioxidant and antifungal activities of Padina pavonica and Sargassum vulgare from the Lebanese Mediterranean Coast. Adv. Environ. Biol. 1, 42–48 (2012)
A. Ambreen, K. Hira, A. Ruqqia, V. Sultana, Evaluation of biochemical component and antimicrobial activity of some seaweeeds occurring at Karachi coast. Pak. J. Bot. 44, 1799–1803 (2012)
R. Bouhlal, C. Haslin, J.C. Chermann, S. Colliec-Jouault, C. Sinquin, G. Simon, S. Cerantola, H. Riadi, N. Bourgougnon, Antiviral activities of sulfated polysaccharides isolated from Sphaerococcus coronopifolius (Rhodophytha, Gigartinales) and Boergeseniella thuyoides (Rhodophyta,. Ceramiales). Mar. Drugs 9, 1187–1209 (2011)
S. Dayong, L. Jing, G. Shuju, H. Lijun, Antithrombotic effect of bromophenol, the alga-derived thrombin inhibitor. J. Biotechnol. 136, 577–588 (2008)
H.J. Na, P.D. Moon, H.J. Lee, H.R. Kim, H.J. Chae, T. Shin, Y. Seo, S.H. Hong, H.M. Kim, Regulatory effect of atopic allergic reaction by Carpopeltis affinis. J. Ethnopharmacol. 101, 43–48 (2005)
S.K. Kim, N.V. Thomas, X. Li, Anticancer compounds from marine macroalgae and their application as medicinal foods. Adv. Food Nutr. Res. 64, 213–224 (2011)
G.K. Devi, K. Manivannan, G. Thirumaran, F.A.A. Rajathi, P. Anantharaman, In vitro antioxidant activities of selected seaweeds from Southeast coast of India. Asian Pac. J. Trop. Med. 4, 205–211 (2011)
C.Y. Wang, T.C. Wu, S.L. Hsieh, Y.H. Tsai, C.W. Yeh, C.Y. Huang, Antioxidant activity and growth inhibition of human colon cancer cells by crude and purified fucoidan preparations extracted from Sargassum cristaefolium. J. Food Drug Anal. 23, 766–777 (2015)
O. Morton, B.E. Picton, Encyclopedia of Marine Life of Britain and Ireland (National Museums Northern Ireland, Holywood, 2010)
F.StP.D. Bunker, C.A. Maggs, J.A. Brodie, A.R. Bunker, Seasearch Guide to Seaweeds of Britain and Ireland (Marine Conservation Society, Ross-on-Wye, 2010)
W. Braune Meeresalgen, Ein Farbbildführer zu den verbreiteten benthischen Grün- Braun- und Rotalgen der Weltmeere (A.R.G. Gantner Verlag, Ruggell, 2008)
A. Tariq, J. Ara, V. Sultana, S. Ehteshamul-Haque, M. Athar, Antioxidant potential of seaweeds occurring at Karachi coast of Pakistan. J. Appl. Bot. Food Qual. 84, 207–212 (2011)
F.A. Agili, S.F. Mohamed, Polysaccharides from Padina pavonia: chemical structural and antioxidant activity. Aust. J. Basic Appl. Sci. 6, 277–283 (2012)
E.A.C. Guedes, T.G. da Silva, J.S. Aguiar, L.D. de Barros, L.M. Pinotti, A.E.G. Sant’Ana, Cytotoxic activity of marine algae against cancerous cells. Rev. Bras. Farmacogn. 23, 668–673 (2013)
T. Stanojković, K. Šavikin, G. Zdunić, Z. Kljajić, N. Grozdanić, J. Antić, In vitro antitumoral activities of Padina pavonia on human cervix and breast cancer cell lines. J. Med. Plants Res (2014). https://doi.org/10.5897/JMPR012.695
P.P.S. Rao, P. Sreenivasa Rao, S.M. Karmarkar, Antibacterial activity from Indian species of Sargassum. Bot. Mar. 31, 295–298 (1988)
E.S. El-Fatimy, A.A.M. Said, Antibacterial activity of methanolic extract of dominant marine alga (Padina pavonia) of Tolmeta Coasts. Libya. J. Am. Sci. 7, 745–751 (2011)
W.J. Yoon, Y.M. Ham, K.N. Kim, S.Y. Park, N.H. Lee, C.G. Hyun, W.J. Lee, Anti-inflammatory activity of brown algae Dictyota dichotoma in murine macrophage RAW 264.7 cells. J. Med. Plants Res. 3, 001–008 (2009)
M.O. Germoush, Antioxidant and anti-inflammatory effects of Padina pavonia and Turbenaria ornata in streptozotocin/nicotinamide diabetic rats. Life Sci. J. 10, 1265–1271 (2013)
C. Parthiban, C. Saranya, K. Girija, A. Hemalatha, M. Suresh, P. Anantharaman, Evaluation of in vitro antioxidant properties of selected seaweeds from Tuticorin coast. Int. J. Current Microbiol. App. Sci. 2, 64–73 (2013)
M.D. Deyab, T. Elkatony, F. Ward, Qualitative and quantitative analysis of phytochemical studies on brown Seaweed, Dictyota dichotoma. IJEDR 4, 674–678 (2016)
N. Ammar, R. Aydi Ben Abdallah, H. Jabnoun-Khiareddine, A. Nefzi, S. Rguez, M. Daami-Remadi, Sargassum vulgare extracts as an alternative to chemical fungicide for the management of fusarium dry rot in potato. J. Agric. Sci. Food Res. 8, 197 (2017)
G. Sudha, A. Balasundaram, Analysis of bioactive compounds in Padina pavonica using HPLC, UV-VIS and FTIR techniques. J. Pharmacogn. Phytochem. 7, 3192–3195 (2018)
L. Mhadhebi, A. Laroche, J. Robert, A. Bouraoui, Antioxidant, anti-inflammatory, and antiproliferative activities of organic fractions from the Mediterranean brown seaweed Cystoseira sedoides. Can. J. Physiol. Phamracol. 89, 911–921 (2011)
H.J. Dorman, O. Bachmayer, M. Kosar, R. Hiltunen, Antioxidant properties of aqueous extracts from selected Lamiaceae species grown in Turkey. J. Agric. Food Chem. 52, 762–770 (2004)
M. Oyaizu, Studies on products of browning reaction prepared from glucoseamine. Jpn. J. Nutr. 44, 307–314 (1986)
M. Nishimiki, N.A. Rao, K. Yagi, The occurrence of super-oxide anion in the reaction of reduced phenazine methosulfate and molecular oxygen. Biochem. Biophys. Res. Commun. 46, 849–853 (1972)
K. Slinkard, V.L. Slingleton, Total phenolic analyses: automation and comparison with manual method. Am. J. Enol. Vitic. 28, 49–55 (1997)
A. Meda, C.E. Lamien, M. Romito, J. Millogo, O.G. Nacoulma, Determination of the total phenolic, flavonoid and proline contents in Burkina Fasan honey, as well as their radical scavenging activity. Food Chem. 91, 571–577 (2005)
NCCLS (National Commitee for Clinical Laboratory Standards), Reference method for broth dilution antifungal susceptibility testing of conidium-forming filamentous fungi: proposed standard M38-P. NCCLS, Wayne, PA, USA (1998)
S.D. Sarker, L. Nahar, Y. Kumarasamy, Microtitre plate-based antibacterial assay incorporating resazurin as an indicator of cell growth, and its application in the in vitro antibacterial screening of phytochemicals. Methods 42, 321–324 (2007)
T. Mosmann, Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods 65, 55–63 (1983)
D. Balakrishnan, D. Kandasamy, P. Nithyanand, A review on antioxidant activity of marine organisms. Int. J. Chem. Technol. Res. 6, 3431–3436 (2014)
I.P. Fernando, M. Kim, K.T. Son, Y. Jeong, Y.J. Jeon, Antioxidant activity of marine algal polyphenolic compounds: a mechanistic approach. J. Med. Food 19, 615–628 (2016)
S.M.M. Shanab, E.A. Shalaby, E.A. El-Fayoumy, Enteromorpha compressa exhibits potent antioxidant activity. J. Biomed. Biotechnol. (2011). https://doi.org/10.1155/2011/726405
K. Sivakumar, S.V. Rajagopal, Radical scavenging activity of green algal species. J. Pharm. Res. 4, 723–725 (2011)
Z. Demirel, F.F. Yilmaz-Koz, N.U. Karabay-Yavasoglu, G. Ozdemir, A. Sukatar, Antimicrobial and antioxidant activeities of solvent extracts and the essential oil composition of Laurencia obtusa and Laurencia obtusa var. pyramidata. Rom. Biotechnol. Lett. 16, 5927–5936 (2011)
S.J. Heo, H.S. Cha, Antioxidant activities of chlorophyta and phaeophyta from Jeju Island. Algae 20, 251–260 (2005)
K.N.C. Murthy, A. Vanilha, J. Rajesha, M.M. Swamy, P.R. Swmya, G.A. Ravishankar, In vitro antioxidant activity of carotenoids from Dunaliella salina—a green microalga. Life Sci. 76, 1381–1390 (2005)
R. Uma, V. Sivasubramanian, S. Niranjali, Devaraj, Evaluation of in vitro antioxidant activities and antiproliferative activity of green microalgae, Desmococcus olivaceous and Chlorococcum humicola. Aust. J. Basic Appl. Sci. 2, 82–93 (2011)
H.H. Omar, H.M. Shiekh, N.M. Gumgumjee, M.M. El-Kazanm, A.M. El-Gendy, Antibacterial activity of extracts of marine algae from the Red Sea of Jeddah, Saudi Arabia. Afr. J. Biotechnol. 11, 13576–13585 (2012)
C. Ibtissam, R. Hassane, M.L. Jose, D.S.J. Francisco, G.V.J. Antonio, B. Hassan. K. Mohamed, Screening of antibacterial activity in marine green and brown macroalgae from the coast of Morocco. Afr. J. Biotechnol. 8, 1258–1262 (2009)
L. Jeyanthi Rebecca, V. Dhanalakshmi, T. Thomas, A comparison between the effects of three algal extracts against pathogenic bacteria. J. Chem. Pharm. Res. 4, 4859–4863 (2012)
J. Heijenoort, Formation of the glycan chains in the synthesis of bacterial peptidoglycan. Glycobiology 11, 25–36 (2001)
V. Farkaš, Structure and biosynthesis of fungal cell walls: methodological approaches. Folia Microbiol. 48, 469–478 (2003)
Y. Yang, E.J. Anderson, Antimicrobial activity of a porcine myeloperozidase against plant phatogenic bacteria and fungi. J. Appl. Microbiol. 86, 211–220 (1999)
V.K. Bajpai, Antimicrobial bioactive compounds from marine algae: a mini review. Indian J. Mar Sci. 45, 1076–1085 (2016)
N.E. Awad, M.A. Selim, H.M. Metawe, A.A. Matloub, Cytotoxic xenicane diterpenes from the brown alga Padina pavonia (L.) Gaill. Phytother. Res. 22, 1610–1613 (2008)
E. Hussain, L.J. Wang, B. Jiang, S. Riaz, G.Y. Butt, D.Y. Shi, A review of the components of brown seaweeds as potential candidates in cancer therapy. RSC Adv. 6, 12592–12610 (2016)
J. Chen, H. Li, Z. Zhao, X. Xia, B. Li, J. Zhang, X. Yan, Diterpenes from the marine algae of the genus Dictyota. Mar. Drugs. 16, 159 (2018)
L.A.R.D. Souza, C.M.P.G. Dore, A.J.G. Castro, T.C.G.D. Azevedo, M.T.B.D. Oliveira, M.D.F.V. Moura, N.M.B. Benevides, E.L. Leite, Galactans from the red seaweed Amansia multifida and their effects on inflammation, angiogenesis, coagulation and cell viability. Biomed. Prev. Nutr. 2, 154–162 (2012)
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This work was financed in part by the Ministry of Science, Technology, and Development of the Republic of Serbia and was carried out within the framework of Projects No. 173032 and 175011.
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Kosanić, M., Ranković, B. & Stanojković, T. Brown macroalgae from the Adriatic Sea as a promising source of bioactive nutrients. Food Measure 13, 330–338 (2019). https://doi.org/10.1007/s11694-018-9948-4
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DOI: https://doi.org/10.1007/s11694-018-9948-4