Browse > Article
http://dx.doi.org/10.47853/FAS.2022.e38

Antibacterial activity and toxicity of Halymenia durvillei red seaweed from Kayangan island, South Sulawesi, Indonesia  

Kasmiati, Kasmiati (Faculty of Marine Science and Fisheries, Hasanuddin University)
Nurunnisa, Andi Tenri (Faculty of Marine Science and Fisheries, Hasanuddin University)
Amran, Amran (Faculty of Marine Science and Fisheries, Hasanuddin University)
Resya, Muhammad Ikhwan (Faculty of Marine Science and Fisheries, Hasanuddin University)
Rahmi, Mufti Hatur (Faculty of Marine Science and Fisheries, Hasanuddin University)
Publication Information
Fisheries and Aquatic Sciences / v.25, no.8, 2022 , pp. 417-428 More about this Journal
Abstract
This study aimed to determine the antibacterial activity and toxicity of methanol and hexane extracts of Halymenia durvillei red seaweed which were found abundantly in Kayangan island, South Sulawesi. The antibacterial activity of the crude extract was tested against five gram-negative bacteria, namely Escherichia coli, Salmonella typhi, Pseudomonas aeruginosa, Aeromonas hydrophila, and Vibrio harveyi at a dose of 200 g/disk. Extract toxicity was tested on Artemia salina larvae at concentrations of 1,000, 500, 250, 125, 62.5, and 31.25 ㎍/mL. The results showed that the methanol and hexane extracts of H. durvillei had the highest activity against S. thypi and A. hydrophila, respectively, with inhibition zones of 26.2 mm and 21.0 mm. On the other hand, the two extracts did not show activity against E. coli and P. aeruginosa, respectively. The toxicity of the methanol extract of H. durvillei was twice as high as that of the hexane extract with half-maximal inhibitory concentration of 98.24 and 184.21 ㎍/mL, respectively. Thus, the methanol and hexane extracts of red seaweed H. durvillei have the potential as new antibacterial agents respectively against the pathogenic bacteria S. typhi and A. hydrophila, but also have the opportunity to be developed into antitumor herbal compounds.
Keywords
Seaweed; Halymenia durvillei; Antibacterial activity; Toxicity activity;
Citations & Related Records
Times Cited By KSCI : 3  (Citation Analysis)
연도 인용수 순위
1 Jannah M, Hanapi A, Fasya AG. Toxicity and phytochemical tests of methanol, chloroform and n-hexane extract of the brown algae Sargassum vulgare from Kapong Beach, Pamekasan Madura. Alchemy. 2014;3:194-203.
2 Kang JY, Chun BS, Lee MC, Choi JS, Choi IS, Hong YK. Anti-inflammatory activity and chemical composition of essential oil extracted with supercritical CO2 from the brown seaweed Undaria pinnatifida. J Essent Oil-Bear Plants. 2016;19:46-51.   DOI
3 Kasmiati K, Yoshioka Y, Okamoto T, Ojika M. New crambescidin-type alkaloids from the Indonesian marine sponge Clathria bulbotoxa. Mar Drugs. 2018;16:84.
4 Kazlowska K, Hsu T, Hou CC, Yang WC, Tsai GJ. Anti-inflammatory properties of phenolic compounds and crude extract from Porphyra dentata. J Ethnopharmacol. 2010;128:123-30.   DOI
5 Khatulistiani TS, Noviendri D, Munifah I, Melanie S. Bioactivities of red seaweed extracts from Banten, Indonesia. IOP Conf Ser Earth Environ Sci. 2020;404:012065.
6 Kim YD, Choi JS. Larvicidal effects of Korean seaweed extracts on brine shrimp Artemia salina. J Anim Plant Sci. 2017;27:1039-46.
7 Kini S, Divyashree M, Mani MK, Mamatha BS. Algae and cyanobacteria as a source of novel bioactive compounds for biomedical applications. In: Singh P, Kumar A, Singh VK, Shrivistava A, editors. Advances in cyanobacterial biology. Cambridge: Academic Press; 2020. p. 173-94.
8 Lin X, Yang M, Li H, Wang C, Peng XX. Decreased expression of LamB and Odp1 complex is crucial for antibiotic resistance in Escherichia coli. J Proteomics. 2014;98:244-53.   DOI
9 De Corato U, Salimbeni R, De Pretis A, Avella N, Patruno G. Antifungal activity of crude extracts from brown and red seaweeds by a supercritical carbon dioxide technique against fruit postharvest fungal diseases. Postharvest Biol Technol. 2017;131:16-30.   DOI
10 Deepak P, Balamuralikrishnan B, Park S, Sowmiya R, Balasubramani G, Aiswarya D, et al. Phytochemical profiling of marine red alga, Halymenia palmata and its bio-control effects against dengue vector, Aedes aegypti. S Afr J Bot. 2019;121:257-66.   DOI
11 El Shafay SM, Ali SS, El-Sheekh MM. Antimicrobial activity of some seaweeds species from red sea, against multidrug resistant bacteria. Egypt J Aquat Res. 2016;42:65-74.   DOI
12 Gorniak I, Bartoszewski R, Kroliczewski J. Comprehensive review of antimicrobial activities of plant flavonoids. Phytochem Rev. 2018;18:241-72.
13 Gunasekaran S, Thirumalairaj VK, Shanmugasokan LS, Pitchai S, Yesudas R, Chacko A. Screening of in vitro cytotoxic activity of brown seaweeds against Hepatocellular carcinoma. J Appl Pharm Sci. 2017;7:51-5.
14 Gutierrez-Rodriguez AG, Juarez-Portilla C, Olivares-Banuelos T, Zepeda RC. Anticancer activity of seaweeds. Drug Discov Today. 2018;23:434-47.   DOI
15 Hamrun N, Nabilah T, Hasyim R, Ruslin M, Dammar I, Arianto MAA. Toxicity test of bioactive red alga extract Eucheuma spinosum on shrimp Artemia salina Leach. Sys Rev Pharm. 2020;11:672-6.
16 Hamza AH, Al-Bishri W, Omar HH, Danial EN. Potential antimicrobial, antioxidant and anityrosenase activities achieved by selected species of marine macroalgae. J Pure Appl Microbiol. 2014;8:257-65.
17 Horta A, Pinteus S, Alves C, Fino N, Silva J, Fernandez S, et al. Antioxidant and antimicrobial potential of the Bifurcaria bifurcata epiphytic bacteria. Mar Drugs. 2014;12:1676-89.   DOI
18 Hussain A, Satti L, Hanif F, Zehra NM, Nadeem S, Bangash TM, et al. Typhoidal Salmonella strains in Pakistan: an impending threat of extensively drug-resistant Salmonella Typhi. Eur J Clin Microbiol Infect Dis. 2019;38:2145-9.   DOI
19 Ismail A, Ktari L, Romdhane YBR, Aoun B, Sadok S, Boudabous A, et al. Antimicrobial fatty acids from green alga Ulva rigida (Chlorophyta). BioMed Res Int. 2018;2018:3069595.
20 Ismail A, Ktari L, Ahmed M, Bolhuis H, Boudabbous A, Stal LJ, et al. Antimicrobial activities of bacteria associated with the brown alga Padina pavonica. Front Microbiol. 2016;7:1072.
21 Hampton HG, Watson BNJ, Fineran PC. The arms race between bacteria and their phage foes. Nature. 2020;577:327-36.   DOI
22 Malik SAA, Bazire A, Gamboa-Munoz A, Bedoux G, Robledo D, Garcia-Maldonado JQ, et al. Screening of surface-associated bacteria from the Mexican red alga Halymenia floresii for quorum sensing activity. Microbiology. 2020;89:778-88.   DOI
23 Nagappan T, Vairappan CS. Nutritional and bioactive properties of three edible species of green algae, genus Caulerpa (Caulerpaceae). J Appl Phycol. 2014;26:1019-27.   DOI
24 Nurhayati APD, Abdulgani N, Febrianto R. Toxicity of Eucheuma alvarezii extract against Artemia salina as a preliminary study on anticancer potential. Akta Kimindo. 2006;2:41-6.
25 Peng B, Wang C, Li H, Su Y, Ye J, Yang M, et al. Outer membrane proteins form specific patterns in antibiotic-resistant Edwardsiella tarda. Front Microbiol. 2017;8:69.
26 Puspita M, Setyawidati NAR, Stiger-Pouvreau V, Vandanjon L, Widowati I, Radjasa OK, et al. Indonesian Sargassum species bioprospecting: potential applications of bioactive compounds and challenge for sustainable development. Adv Bot Res. 2020;95:113-61.   DOI
27 Riyanto EI, Widowati I, Sabdono A. Screening on antibacterial activity of Sargassum polycystum extract against Vibrio harveyi and Micrococcus luteus in Panjang island, Jepara. J Mar Res. 2014;3.
28 Weyermann J, Lochmann D, Zimmer A. A practical note on the use of cytotoxicity assays. Int J Pharm. 2005;288:369-76.   DOI
29 Sanger G, Rarung LK, Damongilala LJ, Kaseger BE, Montolalu LADY. Phytochemical constituents and antidiabetic activity of edible marine red seaweed (Halymenia durvilae). IOP Conf Ser Earth Environ Sci. 2019;278:012069.
30 Silva A, Silva SA, Lourenco-Lopes C, Jimenez-Lopez C, Carpena M, Gullon P, et al. Antibacterial use of macroalgae compounds against foodborne pathogens. Antibiotics. 2020;9:712.
31 Wijesinghe WAJP, Athukorala Y, Jeon YJ. Effect of anticoagulative sulfated polysaccharide purified from enzyme-assistant extract of a brown seaweed Ecklonia cava on wistar rats. Carbohydr Polym. 2011;86:917-21.   DOI
32 Yap WF, Tay V, Tan SH, Yow YY, Chew J. Decoding antioxidant and antibacterial potentials of Malaysian green seaweeds: Caulerpa racemosa and Caulerpa lentillifera. Antibiotics. 2019;8:152.
33 Anjali KP, Sangeetha BM, Devi G, Raghunathan R, Dutta S. Bioprospecting of seaweeds (Ulva lactuca and Stoechospermum marginatum): the compound characterization and functional applications in medicine-a comparative study. J Photochem Photobiol B Biol. 2019;200:111622.
34 Baptista RC, Horita CN, Sant'Ana AS. Natural products with preservative properties for enhancing the microbiological safety and extending the shelf-life of seafood: a review. Food Res Int. 2020;127:108762.
35 Bauer AW, Kirby WMM, Sherris JC, Turck M. Antibiotic susceptibility testing by a standardized single disk method. Am J Clin Pathol. 1966;45:493-6.   DOI
36 Bhadury P, Wright PC. Exploitation of marine algae: biogenic compounds for potential antifouling applications. Planta. 2004;219:561-78.
37 Christobel GJ, Lipton AP, Aishwarya MS, Sarika AR, Udayakumar A. Antibacterial activity of aqueous extract from selected macroalgae of southwest coast of India. Seaweed Res Utiln. 2011;33:67-75.
38 Bolanos JM, Baleta FN, Cairel JD. Antimicrobial properties of Sargassum spp. (Phaeophyceae) against selected aquaculture pathogens. Int J Curr Microbiol Appl Sci. 2017;6:1024-37.   DOI
39 Brown EM, Allsopp PJ, Magee PJ, Gill CIR, Nitecki S, Strain CR, et al. Seaweed and human health. Nutr Rev. 2014;72:205-16.   DOI
40 Casciaro B, Mangiardi L, Cappiello F, Romeo I, Loffredo MR, Iazzetti A, et al. Naturally-occurring alkaloids of plant origin as potential antimicrobials against antibiotic-resistant infections. Molecules. 2020;25:3619.
41 Corsetto PA, Montorfano G, Zava S, Colombo I, Ingadottir B, Jonsdottir R, et al. Characterization of antioxidant potential of seaweed extracts for enrichment of convenience food. Antioxidants. 2020;9:249.
42 De Alencar DB, Da Silva SR, Pires-Cavalcante KMS, De Lima RL, Pereira Junior FN, De Sousa MB, et al. Antioxidant potential and cytotoxic activity of two red seaweed species, Amansia multifida and Meristiella echinocarpa, from the coast of northeastern Brazil. An Acad Bras Cienc. 2014;86:251-63.   DOI
43 Abu-Ghannam N, Rajauria G. Antimicrobial activity of compounds isolated from algae. In: Dominguez H, editor. Functional ingredients from algae for foods and nutraceuticals. Cambridge: Woodhead; 2013. p. 287-306.
44 Agbaje-Daniels F, Babalola A, Akintayo I, Adeleye A, Beukes D. Evaluation of antibacterial activity of Bryopsis pennata and Chaetomorpha antennina against multidrug resistant Morganella morganii and Salmonella species isolated from healthy individuals. J Pharm Res Int. 2017;8:1-7.
45 Alghazeer R, Whida F, Abduelrhman E, Gammoudi F, Naili M. In vitro antibacterial activity of alkaloid extracts from green, red and brown macroalgae from western coast of Libya. Afr J Biotechnol. 2013;12:7086-91.
46 Aguila-Ramirez RN, Arenas-Gonzalez A, Hernandez-Guerrero CJ, Gonzalez-Acosta B, Borges-Souza JM, Veron B, et al. Antimicrobial and antifouling activities achieved by extracts of seaweeds from Gulf of California, Mexico. Hidrobiologica. 2012;22:8-15.
47 Akram J, Khan AS, Khan HA, Gilani SA, Akram SJ, Ahmad FJ, et al. Extensively drug-resistant (XDR) typhoid: evolution, prevention, and its management. BioMed Res Int. 2020;2020:6432580.
48 Akremi N, Cappoen D, Anthonissen R, Verschaeve L, Bouraoui A. Phytochemical and in vitro antimicrobial and genotoxic activity in the brown algae Dictyopteris membranacea. S Afr J Bot. 2017;108:308-14.   DOI
49 Al-Saif SSA, Abdel-Raouf N, El-Wazanani HA, Aref IA. Antibacterial substances from marine algae isolated from Jeddah coast of Red sea, Saudi Arabia. Saudi J Biol Sci. 2014;21:57-64.   DOI
50 Amorim RNS, Rodrigues JAG, Holanda ML, Quindere ALG, de Paula RCM, Melo VMM, et al. Antimicrobial effect of a crude sulfated polysaccharide from the red seaweed Gracilaria ornata. Braz Arch Biol Technol. 2012;55:171-81.   DOI
51 Vinosha M, Palanisamy S, Muthukrishnan R, Selvam S, Kannapiran E, You SG, et al. Biogenic synthesis of gold nanoparticles from Halymenia dilatata for pharmaceutical applications: antioxidant, anti-cancer and antibacterial activities. Process Biochem. 2019;85:219-29.   DOI
52 Fraga-Corral M, Garcia-Oliveira P, Pereira AG, Lourenco-Lopes C, Jimenez-Lopez C, Prieto MA, et al. Technological application of tannin-based extracts. Molecules. 2020;25:614.
53 Generalic Mekinic I, Skroza D, Simat V, Hamed I, Cagalj M, Perkovic ZP. Phenolic content of brown algae (Pheophyceae) species: extraction, identification, and quantification. Biomolecules. 2019;9:244.
54 Vinosha M, Palanisamy S, Anjali R, Li C, Yelithao K, Marudhupandi T, et al. Sulfated galactan from Halymenia dilatata enhance the antioxidant properties and prevents Aeromonas hydrophila infection in tilapia fish: in vitro and in vivo study. Int J Biol Macromol. 2020;158:569-79.   DOI
55 Wong W, Al Rawahi H, Patel S, Yau Y, Eshaghi A, Zittermann S, et al. The first Canadian pediatric case of extensively drug-resistant Salmonella Typhi originating from an outbreak in Pakistan and its implication for empiric antimicrobial choices. IDCases. 2019;15:e00492.
56 Zamani E, Shokrzadeh M, Fallah M, Shaki F. A review of acrylamide toxicity and its mechanism. Pharm Biomed Res. 2017;3:1-7.
57 Sah R, Donovan S, Seth-Smith HMB, Bloemberg G, Wuthrich D, Stephan R, et al. A novel lineage of ceftriaxone-resistant Salmonella Typhi from India that is closely related to XRD S. Typhi found in Pakistan. Clin Infect Dis. 2020;71:1327-30.   DOI
58 Singh RP, Reddy CRK. Seaweed-microbial interactions: key functions of seaweed-associated bacteria. FEMS Microbiol Ecol. 2014;88:213-30.   DOI
59 Sanjeewa KAA, Jeon YJ. Edible brown seawees: a review. J Food Bioact. 2018;2:37-50.
60 Sharo NM, Ningsih R, Hanapi A, Nasichuddin A. Toxicity test and identification of red algae extract compounds against Artemia salina Leach shrimp larvae. Alchemy. 2013;2:170-77.
61 Sirakov I, Velichkova K, Rusenova N, Dinev T. In vitro test of inhibition effect of extracts from three seaweed species distributed at Black Sea on different pathogens potentially dangerous for aquaponics. Rom Biotechnol Lett. 2019;24:176-83.   DOI
62 Sujuliyani, Thaib EA, Indriati N, Liananda M. Antibacterial activity of the symbiotic bacteria of green algae Caulerpa racemosa from Pulau Lima Indonesia. IOP Conf Ser Earth Environ Sci. 2019;278:012075.
63 Thanigaivel S, Vidhya Hindu S, Vijayakumar S, Mukherjee A, Chandrasekaran N, Thomas J. Differential solvent extraction of two seaweeds and their efficacy in controlling Aeromonas salmonicida infection in Oreochromis mossambicus: a novel therapeutic approach. Aquaculture. 2015;443:56-64.   DOI
64 Cheung RCF, Wong JH, Pan WL, Chan YS, Yin CM, Dan XL, et al. Antifungal and antiviral products of marine organisms. Appl Microbiol Biotechnol. 2014;98:3475-94.   DOI
65 Nazarudin MF, Paramisparam A, Khalid NA, Albaz MN, Shahidan MS, Yasin ISM, et al. Metabolic variations in seaweed, Sargassum polycystum samples subjected to different drying methods via 1H NMR-based metabolomics and their bioactivity in diverse solvent extracts. Arab J Chem. 2020;13:7652-64.   DOI
66 Perez MJ, Falque E, Dominguez H. Antimicrobial action of compounds from marine seaweed. Mar Drugs. 2016;14:52.
67 Rozi R, Mukti AT, Samara SH, Santanumurti MB. The effect of chitosan in feed on growth, survival rate and feed utilization efficiency of Nile tilapia (Oreochromis niloticus). J Perikanan Univ Gadjah Mada. 2018;20:2502-5066.
68 Perez-Santaescolastica C, Munekata PES, Feng X, Liu Y, Bastianello Campagnol PC, Lorenzo JM. Active edible coatings and films with Mediterranean herbs to improve food shelflife. Crit Rev Food Sci Nutr. 2022;62:2391-403.   DOI
69 Puspitasari E, Rozirwan, Hendri M. Toxicity test using brine shrimp lethality test (BSLT) method on mangrove extract (Avicennia marina, Rhizophora mucronata, Sonneratia alba and Xylocarpus granatum) from Banyuasin, South Sumatera. J Biol Trop. 2018;18.
70 Reed TAN, Krang S, Miliya T, Townell N, Letchford J, Bun S, et al. Antimicrobial resistance in Cambodia: a review. Int J Infect Dis. 2019;85:98-107.   DOI