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ISSN : 1229-1153(Print)
ISSN : 2465-9223(Online)
Journal of Food Hygiene and Safety Vol.33 No.3 pp.151-156
DOI : https://doi.org/10.13103/JFHS.2018.33.3.151

Marine Algae and Their Potential Application as Antimicrobial Agents

Grace N.A. Charway1,2, Padmini Yenumula3, Young-Mog Kim1,3.4*
1Inland and Aquaculture Division, Fisheries Commission, Ministry of Fisheries and Aquaculture Development, AccraBox GP 630, Ghana
2KOICA-PKNU International Graduate Program of Fisheries Science, Pukyong National University, Busan, Korea
3Department of Food Science and Technology, Pukyong National University, Busan, Korea
4Marine-Integrated Bionics Research Center, Pukyong National University, Busan, Korea
Correspondence to: Young-Mog Kim, Department of Food Science and Technology, Pukyong National University, Busan 48547, Korea Tel: 82-51-629-5832 E-mail: ymkim@pknu.ac.kr
April 17, 2018 May 9, 2018 May 25, 2018

Abstract


The world is becoming overwhelmed with widespread diseases as antibiotic resistance increases at an alarming rate. Hence, there is a demanding need for the discovery and development of new antimicrobial drugs. The ocean is gifted with many organisms like phytoplankton, algae, sponges, cnidarians, bryozoans, mollusk, tunicates and echinoderms, which are known to produce a wide variety of bioactive secondary metabolites with pharmacological properties. Many new therapeutic drugs have emerged from marine invertebrates, although the large algal community is yet to be explored. The bioactivity possessing secondary metabolites of marine algae include polyphenols, phlorotannins, alkaloids, halogenated compounds, sulfated polysaccharides, agar, carrageenan, proteoglycans, alginate, laminaran, rhamnan sulfate, galactosylglycerol, and fucoidan. These metabolites have been found to have great antimicrobial activities against many human aliments. Studies show that the algal community represents about 9% of biomedical compounds obtained from the sea. This review looks at the evolution of drugs from the ocean, with a special emphasis on the antimicrobial activities of marine algae.



초록


    Many chemotherapeutic agents have been discovered from a wide variety of chemical classes such as terpenoids, polyketides, acetogenins, peptides, and alkaloids. These agents have been discovered from the marine environment making it a worldwide focus in the effort for the discovery of novel natural products. Reports show that more than 12,000 novel chemicals have been discovered from marine organisms and majority of these chemical compounds have been identified from marine invertebrates such as sponges predominate1,2). Marine algae represent a small fraction of these discoveries. However, recent trends in drug research from natural sources have indicated that marine algae are a promising source of novel biochemically active compounds, especially for antiprotozoal, antibiotic, anti-cancer, and antiviral activities3). Table 1 shows various biological activities of marine algae and its metabolites4-17).

    Marine macroalgae can be classified as red algae (rhodophyta), brown algae (phaeophyta) or green algae (chlorophyta) depending on their nutrient and chemical composition. Red and brown algae commonly referred to as seaweeds for human food sources also serve as an important source of bioactive natural substance18). These red and brown algae are extensively used in Asian diet for centuries due to their natural nutritional value such as carotenoids, dietary fibers, proteins, essential fatty acids, and also huge presence of vitamins and minerals18). Apart from their nutritional value, many coastal inhabitants in Asia prepare algae extracts for the treatment of disorders and ailments such as wounds, fever and stomach aches, and for the prevention of arrhythmia19).

    Bio stimulating properties of seaweed are shown to have antimicrobial activities such as antibiotics, laxatives, anticoagulants, anti-ulcer products and suspending agents in radiological preparations, thus making seaweeds a potential source of natural antioxidants. Bioactive metabolites such as sulphated polysaccharides, a macromolecule of seaweed and phlorotannins have also exhibited active response to the treatment of most bacterial and viral diseases and also have anticoagulant activities. Marine algae have consequently become an important source of pharmacologically active metabolites in the discovery of novel drugs.

    Antibacterial activity of marine algae

    The development of new antibiotics has become a high priority for many biomedical researches due to the high resistance to current antibacterial agents to the treatment of infectious disease and food borne pathogens. Many studies on compounds such as terpenoids, phlorotannins, acrylic acid, phenolic, steroids, halogenated ketones and alkanes, and cyclic polysulphide present in marine algae have been reported as promising bactericidal agents20). The presence of these compounds suggests a number of alternative mechanisms for antimicrobial action. Among the tested algae the extracts of Scenedesmus obliquus showed a strong inhibition against Gram-positive (Staphylococcus aureus) and Gramnegative bacteria (Salmonella spp., Escherichia coli, and Pseudomonas aeruginosa)21). Phlorotannins extracted from Marine brown algae (Ecklonia cava, E. kurome, E. stolonifera, Eiseniaaborea, Eiseniabicyclis, Ishigeokamurae, and Pelvetiasiliquosa) have also been reported to show an antibacterial activity against S. aureus, methicillin resistant S. aureus (MRSA), Salmonella spp., and E. coli22).

    Polyphenols, carotenoids, amino acids, and catechinsare extracted from Marine algae Gracilariopsislongissima have an antibacterial activity against Vibrio spp.23). Demirel et al.24) also reported that hydrocarbons, terpenes, phenols, sulfur-containing compound, and aldehydes extracted from the brown algae Colpomeniasinuosa, Dictyota dichotoma, Dictyota dichotoma var. implexa, Petaloniafascia, and Scytosiphon lomentar have an antibacterial activity against Bacillus subtilis and S. aureus. Phytochemicals such as saponins, tannins, carotenoids, flavonoids, alkaloids, and glycosides extracted from the green algae Chlorococcumhumicola have an antibacterial activity against E. coli, S. aureus, Salmonella Typhimurium, P. aeruginosa and Vibriocholerae25). Phytol, fucosterol, neophytadiene or palmitic, palmitoleic and oleic acids from the brown algae Himanthalia elongate have an antibacterial activity against E. coli and S. aureus26). Lipophilic compounds (pyrrole-2-carboxylic acid, pentadecanoic acid, and octadecanoic acid) from the red algae Asparagopsis taxiformis, Laurenciaceylanica, Laurenciabrandenii, and Hypneavalentiae have an antibacterial activity against pathogenic Vibrio strains27).

    Similarly, Etahiri et al.28) reported that Sphaerococcuscoronopifolius, a cosmopolitan red alga, contains diterpene and bromosphaerone, and shows an antibacterial activity against S. aureus with an MIC of 0.047 μg/mL. It has been also reported that a marine fungus isolated from the surface of the brown alga Rosenvingea sp. cultured with a unicellular marine bacterium to yield pestalone has a potent antibiotic activity against MRSA with an MIC of 0.037 μg/ mL and vancomycin-resistant Enterococcus faecium with an MIC of 0.078 μg/mL29). 95% ethanol extract from whole dried Gracilariacervicornis algae was active against S. aureus at a concentration of 5.0 mg/mL and ethanol extracts from Gracilariadomigensis and G. sjoestedii showed antibacterial activity against E. coli and S. aureus30,31). The phlorotannin, dieckol, extracted from the brown marine algae has shown a potent antimicrobial activity against MRSA in the range of 125-250 μg/mL32). Eom et al.33) also reported that fermentation broth of Eiseniabicyclis with Candida utilis YM-1 exhibited enhanced antimicrobial activity against MRSA and food-borne pathogenic bacteria. In addition, 2,3,5,6-tetrabromo-1-methylindole, a bromoindole isolated from the red algae Laurenciabrongniartii possess an antibacterial activity against B. subtilis and Saccharomyces cerevisiae and themethanol extract of fresh Gracilariacorticata was also active against B. subtilis, B. megaterium, S. aureus, and Streptococcus viridians12,31). Plaza et al.26) reported the antimicrobial activity of algae Himanthalia elongate and microalgae Synechocystis spp. against E. coli and S. aureus.

    Antifungal activity of marine algae

    Fungal infections have become common and many researchers are focusing on novel drugs for treating these infections. The algae community has become a promising lead in the discovery and development of novel drugs for fungal infections. The antifungal activity of seaweed extracts can be explained by the presence of phenolic compounds and their impact on spore germination. Some algal extracts have also shown to inhibit fungal enzyme activity due to the presence of bioactive metabolites. Ethanol extracts from Gracilariadebilis, G. domingensis, and G. sjoestedii were active against Candida albicans shown by agar plate method31). Also, the ethanol extract of G. domigensis was active against Mycobacterium smegmatis and Neurospora crassa12). Alarif et al.34) also reported that isolauraldehyde isolated from the organic extract of the red alga Laurencia obtuse had significant antifungal activity against C. albicans with MIC of 70 mg/mL, and showed medium activity against Aspergillus fumigatus and Aspergillus flavus with a MIC of 100 and 1,000 mg/mL, respectively. Dieckol purified from E. cava has fungicidal activity against Trichophyton rubrum associated with dermatophytic nail infections in humans35).

    Antiprotozoal activity

    Diseases caused by protozoan parasites lead to high rates of mortality and morbidity worldwide. The traditional use of algae for antiparasitic treatment has gained the attention of several research groups around the world, and marine secondary metabolites are now being evaluated as drug leads for the treatment of neglected diseases such as leishmaniasis, Chagas disease, and human African trypanosomiasis. To date, no marine natural products or any derivatives have entered pre-clinical assessment for trypanosomatid diseases, but numerous antiprotozoal therapeutic extracts or fractions and a few compounds from several seaweed species have been studied for potential lead compound isolation, medicinal applications or for modifications. Compounds such as terpenes, acetogenins, polyphenols, and alkaloids from algae are noted to have antiprotozoal activity with the halogenated terpenoids and acetogenins from the genera Bifurcaria, Laurencia, Dictyota, and Canestrocarpus showing a leishmanicidal and trypanocidal activity36-40).

    The red algae Mastocarpusstellatus which shares phylogenetic origins with Plasmodium falciparum, showed the best antiplasmodial activity41). Gallé et al.42) also reported that organic extracts of 20 species of French seaweed showed antiprotozoal activity against Trypanosoma brucei, the parasite responsible for sleeping sickness. These extracts have previously shown potent antiprotozoal activities in vitro against P. falciparum and Leishmaniadonovani. Süzgeç-Selçuk et al.43) showed that methanolic extracts of algae belonging to Chlorophyta (Caulerparacemosa and Codium bursa), Phaeophyta (Cystoseirabarbata and Cystoseiracrinata) and Rhodophyta (Corallinagranifera, Janiarubens, Ceramiumrubrum, Gracilariaverrucosa, Dasyapedicellata, and Gelidiumcrinale) were active against T. bruceirhodesiense. Further studies also showed that the nhexane and dichloromethane fractions of Bostrychiatenella (Rhodophyta) from the Sao Paulo Coast, Brazil, showed activity against Trypanosoma cruzitrypomastigotes and Leishmania amazonensispromastigotes44).

    Studies showed that Dictyotapfaffii and Canistrocarpuscervicornis, brown alga have an antileishmanial activity and that the diterpene [8,10,18-trihydroxy-2,6-dolabelladiene( 5)] obtained from Dictyotapfaffii, exhibited a leishmanicidal activity against intracellular amastigotes (IC50= 44 μM) and anti-human immunodeficiency virus (HIV)-1 activity. HIV-1 is known to exacerbate the Leishmania load in macrophage infection. Therefore, the leishmanicidal and anti-HIV-1 activities of dolabelladienetriol (5) make it a promising candidate for leishmaniasis chemotherapy, either in isolated cases or in cases associated with HIV-137,39).

    Antiviral activity of marine algae

    Viral diseases, caused by pathogenic virus infections, are still one of the leading causes of death in humans worldwide. Although many antiviral agents have been developed and are used for treatment of viral infections, emergence of drug resistance, side effects, and the necessity for extensive clinical use are the main reasons for failure of antiviral therapy45). Therefore, the development of new antiviral agents with diverse kinds of antiviral actions is required. The search for new antiviral agents focuses on not only synthetic compounds but also natural products such as plants, insects, animal organs, and their components45). Recently, a great deal of interest has been expressed regarding marine algae as potential antiviral agents. This contribution focuses on anti-herpes virus therapeutic agents derived from marine algae which are considered as novel functional ingredients in anti-herpes virus therapy. Sulfated polymannuroguluronate (SPMG) a polysaccharide with an average molecular weight of 8.0 kDa isolated from brown algae, recently entered Phase II clinical trial in China as the first anti-acquired immune deficiency syndrome (AIDS) drug candidate and was initially reported to bind to 28 amino acids located in the HIV viral glycoprotein gp120 V3 loop46).

    Witvrouw and De Clercq47) have reported that fucoidans and sulfated polysaccharides (SPs) extracted from some marine brown seaweeds show an antiviral activity against infectious diseases, such as HIV, herpes simplex virus types (HSV-1 and HSV-2) and cytomegalovirus. It has been also reported that some seaweed-derived SPs such as carrageenans, fucoidans, and sulfated rhamnogalactans have inhibitory effects on the entry of enveloped viruses including herpes and HIV into cells48-51). Ono et al.52) and Talarico et al.53) have also reported that the SPs of some seaweed extract from Undariapinnatifida, Splachnidiumrugosum, Gigartinaatropurpurea, and Plocamiumcartilagineum have an antiviral activity against HSV-I and HSV-II. Beress et al.54) have demonstrated that seaweed-derived SPs could be used as vaginal antiviral formulations without disturbing essential functions of the vaginal epithelial cells and normal bacterial flora.

    Summary

    Marine environments provide a rich and an invaluable source of new natural products of chemically diverse compounds that have a promising lead in the development of novel, potential, and useful therapeutic agents. Many marine algae have been reported to exhibit antimicrobial effects against several pathogens and human infections thus making them the focus for the discovery of novel drugs, however more Studies need to be done on the bioactivity of marine natural products especially marine algae as these group of marine natural products have exhibited great potential for novel drugs.

    Acknowledgements

    This research was funded by the Marine Biotechnology Program (20150220) funded by the Ministry of Oceans and Fisheries, Republic of Korea.

    Figure

    Table

    Marine algae active compounds and their biological activities

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