Betül Aydın, Burcu Ak Çimen, Leyla Açık, Selin Sayın

Evaluation of Antimicrobial Effects of Four Selected Marine Macroalgae from Iskenderun Bay

In the present study, the seaweeds belong to Phaeophyaceae (Cystoseira elegans Sauvageau 1912, Cystoseira amentacea (C.Agardh) Bory 1832, Padina crassa Yamada 1931) and Florideophyceae (Corallina elongata J.Ellis & Solander 1786) collected from nearby Iskenderun-Turkey of Mediterranean Sea were detected for their antimicrobial activities against seven bacterial strains (Escherichia coli ATCC 35218, Bacillus cereus NRRL B-371, Staphylococcus aureus ATCC 25923, Pseudomonas aeruginosa ATCC 27853, Klebsiella pneumoniae ATCC 13883, Salmonella typhimurium ATCC 14028, Proteus vulgaris RSKK 96029). The antimicrobial activities were expressed as minimum inhibitory concentrations (MICs) and minimum bactericidal concentrations (MBCs). According to the results obtained from MICs and MBCs values of the extracts on pathogenic microorganisms were between 0.78 to 50 mg/mL. The lowest MICs and MBCs values were recorded for C. elegans extract against B. cereus with a MIC value of 0.78 mg/mL. These results suggest that secondary metabolites of brown and red algae are important sources that could be used as broad spectrum of biological and pharmaceutical activities

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Abourriche A, Charrouf M, Bennamara A, Berrada M, Chaib N, Boudouma M, Francisco C. 1999. Investigation of bioactivity of extracts from Moroccan solitary tunicate Cynthia savignyi. Journal of Ethnopharmacology, 1999. 68: 47-53. doi: https://doi.org/10.1016/S0378-8741(99)00033-1
Adrien A, Dufour D, Baudouin S, Maugard T, Bridiau N. 2017. Evaluation of the anticoagulant potential of polysaccharide- rich fractions extracted from macroalgae. Natural Product Research, 31: 2126–2136. doi: https://doi.org/10.1080/ .2017.1278595
Al-Zahrani A, Al-Haj N, Omer H, Al-Judaibi A. 2014. Impact of Extracts of Marine Macroalgae on Multidrug-Resistant Bacteria. Journal of Microbiology Research, 4: 18-24. doi: https://doi.org/10.5923/s.microbiology.201401.03
Arguelles EDLR, Monsalud RG, Sapin AB. 2019. Chemical composition and in vitro antioxidant and antibacterial activities of Sargassum vulgare C. Agardh from Lobo, Batangas, Philippines. Journal of International Society for Southeast Asian Agricultural Sciences. 25(1): 112-122.
Arguelles EDLR. 2021. Evaluation of Antioxidant Capacity, Tyrosinase Inhibition, and Antibacterial Activities of Brown Seaweed, Sargassum ilicifolium (Turner) C. Agardh 1820 for Cosmeceutical Application. Journal of Fisheries and Environment, 45(1): 64-77.
Banaigs B, Francisco C, Gonzalez E, Fenical W. 1983. Diterpenoid metabolites from the marine alga Cystoseira elegans. Tetrahedon, 39: 629-638. doi: https://doi.org/10.1016/S0040-4020(01)91838-1
Bansemir A, Blume M, Schroder S, Lindequist U. 2006. Screening of cultivated seaweeds for antibacterial activity against fish pathogenic bacteria. Aquaculture, 252: 79-84. doi: https://doi.org/10.1016/j.aquaculture.2005.11.051
Battu GR, Ethadi S, Prayaga Murthy P, Praneeth VS, Rao M. 2011. In vitro antibacterial activity and preliminary phytochemical screening of three algae from Visakhapatnam Coast, Andhra Pradesh India. International Journal of Pharmacy and Pharmaceutical Sciences, 3(4): 399-401.
Bhadury P, Wright CP. 2004. Exploitation of marine algae: biogenic compounds for potential antifouling application. Planta, 219: 561-578. doi: https://doi.org/10.1007/s00425- 004-1307-5
Bhowmick S, Mazumdar A, Moulick A, Adam V. 2020. Algal metabolites: An inevitable substitute for antibiotics. Biotechnology Advances, 43: 107571. doi: https://doi.org/10.1016/j.biotechadv.2020.107571
Biris-Dorhoi ES, Michiu D, Pop CR, Rotar AM, Tofana M, Pop OL, Socaci SA, Farcas AC. 2020. Macroalgae—A Sustainable Source of Chemical Compounds with Biological Activities. Nutrients, 12: 3085. doi: https://doi.org/10.3390/nu12103085
Blunt JW, Copp BR, Hu WP, Munro MHG, Northcote PT, Prinsep, MR. 2007. Marine natural products. Natural Product Reports, 24: 31–86. doi: https://doi.org/10.1039/B603047P
Bourgougnon N, Stiger-Pouvreau V. 2012. Chemodiversity and bioactivity within red and brown macroalgae along the French coasts, metropole and overseas departements and territories. 58-105 pp. In: Kim, S-K. (Eds.), Handbook of Marine Macroalgae. JohnWiley & Sons, Ltd., 567 p
Bory de Saint-Vincent JBGM. 1832. Hydrophytes. In: Expédition scientifique de Morée. Section des sciences physiques. Tome III. 2e partie. Botanique, pp. 1-367 [368]. (Bory de Saint-Vincent, J.B.G.M Eds), pp. 316-337. Paris & Strabourg: Chez F. G. Levrault, imprimeur-libraire, rue de la Harpe, n. 81; même maison, rue des Juifs, n. 33 (Strasbourg, imprimerie de Levrault).
Braña AF, Fiedler HP, Nava H, González V, Sarmiento-Vizcaíno A, Molina A, Acuña JL, García LA, Blanco G. 2015. Two Streptomyces Species Producing Antibiotic, Antitumor, and Anti-Inflammatory Compounds Are Widespread Among Intertidal Macroalgae and Deep-Sea Coral Reef Invertebrates from the Central Cantabrian Sea. Microbial Ecology, 69: 512– 524. doi: https://doi.org/10.1007/s00248-014-0508-0
Cabral EM, Oliveira M, Mondala JRM, Curtin J, Tiwari BK, Garcia- Vaquero M. 2021. Antimicrobials from Seaweeds for Food Applications. Marine Drugs, 19(4): 211. doi: https://doi.org/10.3390/md19040211.
Chew YL, Lim YY, Omar M, Khoo KS. 2008. Antioxidant activity of three edible seaweeds from two areas in South East Asia. LWT-Food Science and Technology, 41(6): 1067-1072. doi: https://doi.org/10.1016/j.lwt.2007.06.013
Chiheb I, Riadi H, Martine -Lopez J, Dominguez-Seglar JF, Gomez Vidal JA, Bouziane H, Kadiri M. 2009. Screening of antibacterial activity in marine green and brown macroalgae from the coast of Morocco. African Journal of Biotechnology, 8(7): 1258-1562.
Cox S, Abu-Ghannam N, Gupta S. 2010. An assessment of the antioxidant and antimicrobial activity of six species of edible Irish seaweeds. International Food Research Journal, 17: 205– 220.
CLSI. 2018. Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria That Grow Aerobically-11th edition. CLSI standard M07. In. Wayne, PA: Clinical and Laboratory Standards Institute.
Cornish ML, Garbary DJ. 2010. Antioxidants from macroalgae: potential applications in human health and nutrition. Algae, 25(4): 155-171. doi: https://doi.org/10.4490/algae.2010.25. 4.155
Dahms HU, Dobretsov S. 2017. Antifouling Compounds from Marine Macroalgae. Marine Drugs, 15(9): 265. doi: https://doi.org/10.3390/md15090265
Demirel Z, Yilmaz-Koz FF, Karabay-Yavasoglu U, Ozdemir G, Sukatar A. 2009. Antimicrobial and Antioxidant Activity of Brown Algae from the Aegean Sea. Journal of the Serbian Chemical Society, 74: 619-628. doi: https://doi.org/10.2298/ JSC0906619D
Divya CV, Devika V, Asha KRT, Bharat G. 2011. Antimicrobial Screening of the Brown Algae Sargassum cinereum. Journal of Pharmacy Research, 4(2): 420-421.
Dulger B, Hacıoglu N, Erdugan H, Aysel H. 2009. Antimicrobial Activity of Some Brown Algae from Turkey. Asian Journal of Chemistry, 21(5): 4113-4117.
Eliuz E, Börekçi N, Ayas D. 2019. The Antimicrobial Activity of Enteromorpha sp. Methanolic Extract and Gelatin Film Solution Against on Some Pathogens. Marine Science and Technology Bulletin, 8(2): 58-63. doi: https://doi.org/ 10.33714/masteb.640614
Ellis J, Solander D. 1786. The natural history of many curious and uncommon zoophytes, pp. [i]-xii, [1]-208, 63 pls. London: Printed for Benjamin White and Son, at Horace's Head, Fleet- Street and Peter Elmsly, in the Strand.
El Shafay SM, Ali SS, El-Sheekh MM. 2016. Antimicrobial activity of some seaweed’s species from red sea, against multidrug resistant bacteria. The Egyptian Journal of Aquatic Research, 42: 65–74. doi: https://doi.org/10.1016/j.ejar. 2015.11.006
El-Sheekh MM, Mousa ASH, Farghl AAM. 2020. Antibacterial efficacy and phytochemical characterization of some marine brown algal extracts from the red sea, Egypt. Romanian Biotechnological Letters; 25(1): 1160-1169. doi: https://doi.org/10.25083/rbl/25.1/1160.1169
Ertürk Ö, Taş B. 2011. Antibacterial and Antifungal Effects of Some Marine Algae. Kafkas Ü niversitesi Veteriner Fakültesi Dergisi, 17: 121-124.
Ghannadi A, Plubrukarn A, Zandi K, Sartavi K, Yegdaneh A. 2013. Screening for antimalarial and acetylcholinesterase inhibitory activities of some Iranian seaweeds. Research in pharmaceutical sciences, 8(2): 113–118. PMID: 24019820; PMCID: PMC3764674
Glombitza KW. 1979. Antibiotics from algae. Hoppe I.L.A., Ed., Marine Algae in Pharmaceutical Science, Waiter de Gruyter, Berlin, New York, 303f.
Gouveia V, Seca AML, Barreto MC, Pinto DCGA. 2013. Di- and sesquiterpenoids from Cystoseira genus: Structure, intra- molecular transformations and biological activity. Mini Reviews in Medicinal Chemistry, 13: 1150–1159. doi: https://doi.org/10.2174/1389557511313080003
Gümüş B, Ü nlüsayın M, Gümüş E. 2018. A review on antimicrobial properties of marine macroalgae extracts. Ege Journal of Fisheries and Aquatic Sciences, 35(3): 343-351. doi: https://doi.org/10.12714/egejfas.2018.35.3.15
Guner A, Koksal C, Erel SB, Kayalar H, Nalbantsoy A, Sukatar A, Karabay Yavasoglu, NU. 2015. Antimicrobial and antioxidant activities with acute toxicity, cytotoxicity and mutagenicity of Cystoseira compressa (Esper) Gerloff & Nizamuddin from the coast of Urla (İzmir, Turkey). Cytotechnology, 67: 135–143. doi: https://doi.org/10.1007/s10616-013-9668-x
Guner A, Nalbantsoy A, Sukatar A, Karabay Yavaşoğlu, NÜ. 2019. Apoptosis-inducing activities of Halopteris scoparia L. Sauvageau (Brown algae) on cancer cells and its biosafety and antioxidant properties. Cytotechnology, 71: 687–704. doi: https://doi.org/10.1007/s10616-019-00314-5
Guven KC, Coban B, Ozdemir O. 2020. Pharmacology of marine macroalgae. Encyclopedia of Marine Biotechnology, 1: 585– 615. doi: https://doi.org/10.1002/9781119143802.ch20
Hans N, Malik A, Naik S. 2021. Antiviral activity of sulfated polysaccharides from marine algae and its application in combatin g COVID-19: Mini review. Bioresource Technology Reports, 13: 100623. doi: https://doi.org/ 10.1016/j.biteb.2020.100623
Jaswir I, Monsur HA. 2011. Anti-inflammatory compounds of macro algae origin: A review. Journal of Medicinal Plants Research, 5: 7146–7154. doi: https://doi.org/10.5897/ JMPRX11.018
Jegan S, Raj A, Chandrasekaran M, Vencatesalu V. 2019. Anti- MRSA activity of Padina tetrastromatica, Padina gymnospora from guft of mannar biosphere. World Scientific News, 115: 15–26.
Jing-Wen M, Wei-ci T. 1984. Screening for antimicrobial activities in marine algae from the Qingdao coast, China. Hydrobiologia, 116:517–520. doi: https://doi.org/10.1007/ BF00027736
Kamenarska Z, Serkedjieva J, Najdenski H, Stefanov K, Tsvetkova I, Dimitrova-Konaklieva S. et al. 2009.
Antibacterial, antiviral, and cytotoxic activities of some red and brown seaweeds from the Black Sea. Botanica Marina, 52(1): 80–86. doi: https://doi.org/10.1515/BOT.2009.030
Kazlowska K, Hsu T, Hou CC, Yang WC, Tsai GJ. 2010. Anti- inflammatory properties of phenolic compounds and crude extract from Porphyra dentate. Journal of Ethnopharmacology, 128(1): 123–130. doi: https://doi.org/10.1016/j.jep.2009.12.037
Kuda T, Nishizawa M, Toshima D, Matsushima K, Yoshida S, Takahashi H, Kimura B, Yamagishi T. 2021. Antioxidant and anti-norovirus properties of aqueous acetic acid macromolecular extracts of edible brown macroalgae. LWT, 141: 110942. doi: https://doi.org/10.1016/j.lwt.2021.110942
Manivannan K, Karthikai devi G, Anantharaman P, Balasubramanian T. 2011. Antimicrobial potential of selected brown seaweeds from vedalai coastal waters, Gucf of Mannar. Asian Pacific Journal of Tropical Biomedicine, 1(2): 114-120. doi: https://doi.org/10.1016/S2221-1691(11)60007- 5
Martins RM, Nedel F, Guimarães VBS, da Silva AF, Colepicolo P, Pereira CMP, Lund RG. 2018. Macroalgae extracts from Antarctica have antimicrobial and anticancer potential. Frontiers in Microbiology, 9:412. doi: https://doi.org/ 10.3389/fmicb.2018.00412
Mayer AMS, Rodríguez AD, Berlinck RGS, Fusetani N. 2011. Marine pharmacology in 2007–8: Marine compounds with antibacterial, anticoagulant, antifungal, anti-inflammatory, antimalarial, antiprotozoal, antituberculosis, and antiviral activities; affecting the immune and nervous system, and other miscellaneous mechanisms of action. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 153(2): 191–222. doi: https://doi.org/ 10.1016/j.cbpc.2010.08.008
Matanjun P, Mohamed S, Mustapha NM, Muhammad K, Ming CH. 2008. Antioxidant activities and phenolics content of eight species of seaweeds from north Borneo. Journal of Applied Phycology, 20(4): 367–373. doi: https://doi.org/ 10.1007/s10811-007-9264-6
Mickymaray S, Alturaiki W, Al-Aboody MS, Mariappan P, Rajenderan V, Alsagaby SA, Kalyanasundram U, Alarfajj AA. 2018. Anti-bacterial efficacy of bacteriocin produced by marine Bacillus subtilis against clinically important extended spectrum beta-lactamase strains and methicillin-resistant Staphylococcus aureus. International Journal of Medical Research & Health Sciences, 7(2): 75–83.
Mirzadeh M, Arianejad MR, Khedmat L. 2020. Antioxidant, antiradical, and antimicrobial activities of polysaccharides obtained by microwave-assisted extraction method: A review. Carbohydrate Polymers, 229: 11542. doi: https://doi.org/10.1016/j.carbpol.2019.115421
Mohamed S, Hashim SN, Rahman HA. 2012. Seaweeds: A sustainable functional food for complementary and alternative therapy. Trends in Food Science & Technology, 23(2): 83-96. doi: https://doi.org/10.1016/j.tifs.2011.09.001
Moshfegh A, Salehzadeh A, Sadat Shandiz SA. Shafaghi M, Naeemi AS, Salehi S. 2019. Phytochemical Analysis, Antioxidant, Anticancer and Antibacterial Properties of the Caspian Sea Red Macroalgae, Laurencia caspica. Iranian Journal of Science and Technology, Transactions A: Science, 43(1): 49-56. doi: https://doi.org/10.1007/s40995-017-0388-5
Musale AG, Raja KK, Ajit S, Dasgupta S. 2020. Marine Algae as a Natural Source for Antiviral Compounds. AIJR Preprints Series: Coronavirus. doi: https://doi.org/10.21467/ preprints.38
Nagayama K, Iwamura Y, Shibata T, Hirayama I, Nakamura T. 2002. Bactericidal activity of phlorotannins from the brown alga Ecklonia kurome. Journal of Antimicrobial Chemotherapy, 50(6): 889–893. doi: https://doi.org/ 10.1093/jac/dkf222
Negara BFSP, Oktoviani, Nugraheni E, Kusuma AB, Kontesa R, Putra ED, Siallagan D, Herliany NE, Purnama D. 2020. The Utilization of Seaweeds as An Inexpensive Source of New Drugs Agent. IOP Conf. Series: Earth and Environmental Science ,593(1): 012033. doi: https://doi.org/10.1088/1755- 1315/593/1/012033
Osman MEH, Abushady AM, Elshobary ME. 2010. In vitro screening of antimicrobial activity of extracts of some macroalgae collected from Abu-Qir Bay Alexandria, Egypt. African Journal of Biotechnology, 9(42): 7203-7208.
Oumaskour K, Boujaber N, Etahiri S, Assobhei O. 2012. Screening of antibacterial and antifungal activities in green and brown algae from the coast of Sidi Bouzid (El Jadida, Morocco). African Journal of Biotechnology, 11(104): 16831-16837.
Oumaskour K, Boujaber N, Etahiri S, Assobhei O. 2013. Anti- inflammatory and antimicrobial activities of twenty-three marine red algae from The Coast of Sidi Bouzid (El Jadida- Morocco). International Journal of Pharmacy and Pharmaceutical Sciences, 5: 145-149.
Parsaeiemhr A, Lutzu GA. 2016. Algae as a novel source of antimicrobial compounds:Current and future perspective. In: Antibiotic Resistance. Mechanisms and New Antimicrobial Approaches - 1st edition, Eds: K. Kon, M. Rai. Academic Press.
Paul VJ, Puglisi MP. 2004. Chemical mediation of interactions among marine organisms. Natural Product Reports, 21(1): 189-209. doi: https://doi.org/10.1039/B302334F
Pérez MJ, Falqué E, Domínguez H. 2016. Antimicrobial Action of Compounds from Marine Seaweed. Marine drugs, 14(3): 52. doi: https://doi.org/10.3390/md14030052
Rhimou B, Hassane R, Jose M, Nathalie B. 2010. The antibacterial potential of the seaweeds (Rhodophyceae) of the Strait of Gibraltar and the Mediterranean Coast of Morocco. African Journal of Biotechnology, 9(38): 6365-6372.
Rizvi MA, Shammel M. 2004. Studies on the bioactivity and Elementology of marine algae from the Coast of Karachi, Pakistan. Phytotherapy Research: An International Journal Devoted to Pharmacological and Toxicological Evaluation of Natural Product Derivatives, 18(11): 865-872. doi: https://doi.org/10.1002/ptr.1441
Salem WM, Galal H, Nasr El-Deen F. 2011. Screening for antibacterial activities in some marine algae from the red sea (Hurghada, Egypt). African Journal of Microbiology Research, 5(15): 2160-2167. doi: https://doi.org/10.5897/ AJMR11.390
Salvador N, Garreta AG, Lavelli L, Ribera MA. 2007. Antimicrobial activity of Iberian macroalgae. Scientia Marina, 71(1): 101–113. doi: http://dx.doi.org/10.3989/ scimar.2007.71n1101
Sauvageau C. 1912. A propos des Cystoseira de Banyuls et Guéthary. Bulletin de la Station biologique d'Arcachon, 14: 133-556.
Seca AML, Pinto D. 2018. Overview on the Antihypertensive and Anti-Obesity Effects of Secondary Metabolites from Seaweeds. Marine Drugs, 16(7): 237. doi: https://doi.org/10.3390/md16070237
Silva A, Silva SA, Carpena M, Garcia-Oliveira P, Gullón P, Barroso MF, Prieto MA, Simal-Gandara J. 2020. Macroalgae as a source of valuable antimicrobial compounds: Extraction and applications. Antibiotics, 9(10): 642. doi: https://doi.org/10.3390/antibiotics9100642
Smith JE, Hunter CL, Smith CM. 2002. Distribution and reproductive characteristics of nonindigenous and invasive marine algae in the Hawaiian Islands. Pacific Science, 56(3): 299–315. doi: https://doi.org/10.1353/psc.2002.0030
Smit AJ. 2004. Medicinal and pharmaceutical uses of seaweed natural products: A review. Journal of Applied Phycology, 16(4): 245-262. doi: https://doi.org/10.1023/B:JAPH. 0000047783.36600.ef
Tambekar DH, Patil RV, Pawar AL. 2011. Studies on Methanotrophs from Lonar Lake. Journal of Research in Biology. 3: 230-236.
Tuney I, Cadirci BH, Unal D, Sukatar A. 2006. Antimicrobial activities of the extracts of marine algae from the coast of Urla (Izmir Turkey). Turkish Journal of Biology, 30(3): 171 -175.
Wang C, Lu Y. Cao, S. 2020. Antimicrobial compounds from marine actinomycetes. Archives of Pharmacal Research, 43: 677–704. doi: https://doi.org/10.1007/s12272-020-01251-0
Watson SB, Cruz-Rivera E. 2003. Algal chemical ecology: an introduction to the special issue. Phycologia, 42(4): 319-323. doi: https://doi.org/10.2216/i0031-8884-42-4-319.1
Yamada Y. 1931. Notes on some Japanese algae II. Journal of the Faculty of Science, Hokkaido Imperial University 1: 65-76, 3 figs, plates XVI-XX.
Yegdaneh A, Putchakarn S, Yuenyongsawad S, Ghannadi A, Plubrukarn A. 2013. 3-oxoabolene and 1-oxocurcuphenol, aromatic bisabolanes from the sponge Myrmekioderma sp. Natural Product Communications, 8(10): 1355–1357. doi: https://doi.org/10.1177/1934578X130080100
Yegdaneh A, Ghannadi A, Dayani L. 2016. Chemical constituents and biological activities of two Iranian Cystoseira species. Research in Pharmaceutical Sciences, 11(4): 311-317. doi: https://doi.org/10.4103/1735-5362.189 307.
Yuan YV, Carrington MF, Walsh NA. 2005. Extracts from dulse (Palmaria palmata) are effective antioxidants and inhibitors of cell proliferation in vitro. Food and Chemical Toxicology, 43(7): 1073-1081. doi: https://doi.org/10.1016/j.fct. 2005.02.012
Zouaoui B, Ghalem BR. 2017. The Phenolic Contents and Antimicrobial Activities of Some Marine Algae from the Mediterranean Sea (Algeria). Russian Journal of Marine Biology, 43(6): 491–495. doi: https://doi.org/10. 1134/S1063074017060128