Cover Image

Investigating the antioxidant potential of Streptomyces sp. MUSC 11 from mangrove soil in Malaysia

Hefa Mangzira Kemung, Loh Teng-Hern Tan, Kok-Gan Chan, Hooi-Leng Ser, Jodi Woan-Fei Law, Learn-Han Lee, Bey-Hing Goh Abstract - 312 PDF - 38


Streptomyces are a distinguished group of gram-positive bacteria mostly acknowledged for their immense contribution to life-saving drugs and lines of compounds with diverse bioactivities. To date, there remains limited studies on Streptomyces with biological activities residing in underexplored ecosystems such as the mangrove forests. For this purpose, the present work aimed at investigating the biological activity of Streptomyces sp. MUSC 11 collected from soil sample in mangrove forests, situated in the State of Pahang, Peninsular of Malaysia. The cultured strain resembled phenotypic and genotypic traits of genus Streptomyces. Investigations of the methanolic extract from Streptomyces sp. MUSC 11 revealed antioxidant activities in form of scavenging free radicals ABTS, DPPH, chelating iron and reducing ferric iron. Besides the antioxidant tests, antioxidant results corresponded well to the presence of phenolic content. In summary, Streptomyces derived from extreme and understudied ecosystem such as the mangrove forests are potential sources of biologically active and therapeutically useful compounds.

Full Text:



Giri C, Ochieng E, Tieszen LL, et al. Status and distribution of mangrove forests of the world using earth observation satellite data. Global Ecol Biogeogr 2011; 20(1): 154–159.

Pramanik A, Sengupta S, and Bhattacharyya M. Microbial Diversity and Community Analysis of the Sundarbans Mangrove, a World Heritage Site, in Microbial Diversity in the Genomic Era 2019; Elsevier: p. 65–76.

Lee L-H, Zainal N, Azman A-S, et al. Diversity and antimicrobial activities of actinobacteria isolated from tropical mangrove sediments in Malaysia. Sci World J 2014; 2014.

Chan W-K, Tan LTH, Chan K-G, et al. Nerolidol: A sesquiterpene alcohol with multi-faceted pharmacological and biological activities. Mol 2016; 21(5): 529.

Tan LTH, Lee LH, Yin WF, et al., Traditional uses, phytochemistry, and bioactivities of Cananga odorata (Ylang-Ylang). Evidence-Based Complementary Altern Med 2015; 2015.

Tang C, Hoo PC-X, Tan LT-H, et al. Golden needle mushroom: A culinary medicine with evidenced-based biological activities and health promoting properties. Front Pharmacol 2016; 7: 474.

Yong YL, Tan LT-H, Ming LC, et al. The effectiveness and safety of topical capsaicin in postherpetic neuralgia: A systematic review and meta-analysis. Front Pharmacol 2017; 7: 538.

Chan C-K, Tan LT-H, Andy SN, et al. Anti-neuroinflammatory activity of Elephantopus scaber L. via activation of Nrf2/HO-1 signaling and inhibition of p38 MAPK pathway in LPS-induced microglia BV-2 cells. Front Pharmacol 2017; 8: 397.

Tan LT-H, Chan K-G, Pusparajah P, et al. Targeting membrane lipid a potential cancer cure? Front Pharmacol 2017; 8: 12.

Ma DS, Tan LT-H, Chan K-G, et al. Resveratrol—potential antibacterial agent against foodborne pathogens. Front Pharmacol 2018; 9: 102.

Tan LTH, Low LE, Tang SY, et al. A reliable and affordable 3D tumor spheroid model for natural product drug discovery: A case study of curcumin. Prog Drug Discov Biomed Sci 2019; 2(1).

Goh JXH, Tan LT-H, Goh JK, et al. Nobiletin and Derivatives: Functional Compounds from Citrus Fruit Peel for Colon Cancer Chemoprevention. Cancers, 2019; 11(6): 867.

Tay KC, Tan LTH, Chan CK, et al. Formononetin: A review of its anticancer potentials and mechanisms. Front Pharmacol 2019; 10: 820.

Paul DJ, Laure NB, Guru SK, et al. Antiproliferative and antimicrobial activities of alkylbenzoquinone derivatives from Ardisia kivuensis. Pharm Biol 2014.

Ser H-L, Tan W-S, Cheng H-J, et al. Draft genome of starch degrading actinobacterium, Microbacterium mangrovi MUSC 115T isolated from intertidal sediments. Prog Drug Discov Biomed Sci 2018; 1(1).

Ser H-L, Tan W-S, Cheng H-J, et al. Draft genome of amylolytic actinobacterium, Sinomonas humi MUSC 117T isolated from intertidal soil. Mar Genomics 2015; 24: 209–210.

Ancheeva E, Daletos G, and Proksch P. Lead compounds from mangrove-associated microorganisms. Mar Drugs 2018; 16(9): 319.

Patridge E, Gareiss P, Kinch MS, et al. An analysis of FDA approved drugs: Natural products and their derivatives. Drug Discov Today 2016; 21(2): 204–207.

Hu H, Lin H-P, Xie Q, et al. Streptomyces qinglanensis sp. nov., isolated from mangrove sediment. Int J Syst Evol Microbiol 2012; 62(3): 596–600.

Xu J, Wang Y, Xie S-J, et al. Streptomyces xiamenensis sp. nov., isolated from mangrove sediment. Int J Syst Evol Microbiol 2009; 59(3): 472–476.

Huang H, Liu M, Zhong W, et al. Streptomyces caeni sp. nov., isolated from mangrove mud. Int J Syst Evol Microbiol 2018; 68(10):


Wang Y, Huang H, Yuan W, et al. Streptomyces mangrovi sp. nov., an actinomycete from mangrove soil. Int J Syst Evol Microbiol 2015; 65(9): 3086–3090.

World Health Organization. 20th Essential Medicines List (2017). 2019 [cited 2019 14/6/2019]; Available from: https://www.who. int/medicines/news/2017/20th_essential_med-list/en/.

Waksman SA and Henrici AT. The nomenclature and classification of the actinomycetes. J Bacteriol 1943; 46(4): 337.

Zainal N, Ser H-L, Yin W-F, et al. Streptomyces humi sp. nov., an actinobacterium isolated from soil of a mangrove forest. Antonie van Leeuwenhoek 2016; 109(3): 467–474.

Schatz A, Bugle E, and Waksman SA. Streptomycin, a Substance Exhibiting Antibiotic Activity Against Gram-Positive and Gram-Negative Bacteria. Proc Soc Exp Biol Med 1944; 55(1): 66–69.

Umezawa H, Maeda K, Takeuchi T, et al. New antibiotics, bleomycin A and B. The J Antibiot 1966; 19(5): 200–209.

Raja A, LaBonte J, Lebbos J, et al. Daptomycin. 2003, Nature Publishing Group.

Muramatsu H and Nagai K. Streptomyces tsukubensis sp. nov., a producer of the immunosuppressant tacrolimus. J Antibiot 2013; 66(4): 251.

Kemung HM, Tan LT-H, Khan TM, et al. Streptomyces as a prominent resource of future anti-MRSA drugs. Front Microbiol 2018; 9.

L.P.S.N. Genus Streptomyces. 2019 [cited 2019 2/4/2019]; Available from:

Law JW-F, Tan K-X, Wong SH, et al. Taxonomic and characterization methods of Streptomyces: a review. Prog Microbes Mol Biol 2018; 1(1).

Berdy J. Bioactive microbial metabolites. J Antibiot 2005. 58(1): 1.

Tan LT-H, Chan K-G, Lee L-H, et al. Streptomyces bacteria as potential probiotics in aquaculture. Front Microbiol 2016; 7: 79.

Bérdy J. Thoughts and facts about antibiotics: Where we are now and where we are heading. J Antibiot 2012; 65(8): 385.

Tan LTH, Mahendra CK, Yow YY, et al. Streptomyces sp. MUM273b: A mangrove-derived potential source for antioxidant and UVB radiation protectants. MicrobiologyOpen 2019; 14: e859.

Ser H-L, Tan W-S, Yin W-F, et al. Whole genome sequence of Streptomyces humi strain MUSC 119T isolated from intertidal soil. Progr Drug Discov Biomed Sci 2019; 2(1).

Ser H-L, Tan W-S, Mutalib N-SA, et al. Genome sequence of Streptomyces gilvigriseus MUSC 26T isolated from mangrove forest. Braz J Microbiol 2018; 49(2): 207–209.

Spalding M, World Atlas Of Mangroves 2010; Routledge.

Law JW-F, Ser H-L, Duangjai A, et al. Streptomyces colonosanans sp. nov., a novel actinobacterium isolated from Malaysia mangrove soil exhibiting antioxidative activity and cytotoxic potential against human colon cancer cell lines. Front Microbiol 2017; 8: 877.

Ser H-L, Palanisamy UD, Yin W-F, et al. Streptomyces malaysiense sp. nov.: A novel Malaysian mangrove soil actinobacterium with antioxidative activity and cytotoxic potential against human cancer cell lines. Sci Rep 2016; 6: 24247.

Ser H-L, Tan LT-H, Palanisamy UD, et al. Streptomyces antioxidans

sp. nov., a novel mangrove soil actinobacterium with antioxidative and neuroprotective potentials. Front Microbiol 2016; 7: 899.

Lee L-H, Zainal N, Azman A-S, et al. Streptomyces pluripotens sp. nov., a bacteriocin-producing streptomycete that inhibits meticillin resistant Staphylococcus aureus. Inter J Syst Evol Microbiol 2014; 64(9): 3297–3306.

Ser H-L, Tan W-S, Ab Mutalib N-S, et al. Genome sequence of Streptomyces pluripotens MUSC 135T exhibiting antibacterial and antioxidant activity. Mar Genomics 2015; 24: 281–283.

Ser H-L, Ab Mutalib N-S, Yin W-F, et al. Genome sequence of Streptomyces antioxidans MUSC 164T isolated from mangrove forest. Prog Microbes Mol Biol 2018; 1(1).

Law JW-F, Pusparajah P, Ab Mutalib N-S, et al. A review on mangrove actinobacterial diversity: The roles of streptomyces and novel species discovery. Prog Microbes Mol Biol 2019; 1(1).

Ser H-L, Chan K-G, Tan W-S, et al. Complete genome of mangrove-derived anti-MRSA streptomycete, Streptomyces pluripotens MUSC 135T. Prog Microbes Mol Biol 2018; 1(1).

Tan LT-H, Ser H-L, Yin W-F, et al., Investigation of antioxidative and anticancer potentials of Streptomyces sp. MUM256 isolated from Malaysia mangrove soil. Front Microbiol 2015; 6: 1316.

Shepherd MD, Kharel MK, Bosserman MA, et al. Laboratory maintenance of Streptomyces species. Curr Protoc Microbiol 2010; 10E-1.

Hong K, Gao A-H, Xie Q-Y, et al. Actinomycetes for marine drug discovery isolated from mangrove soils and plants in China. Mar Drugs 2009; 7(1): 24–44.

Thompson JD, Gibson TJ, Plewniak F, et al. The CLUSTAL_X windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 1997; 25(24): 4876– 4882.

Kim O-S, Cho Y-J, Lee K, et al. Introducing EzTaxon-e: A prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. Int J Syst Evol Microbiol 2012; 62(3): 716–721.

Tamura K, Stecher G, Peterson D, et al. MEGA6: Molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 2013; 30(12): 2725–2729.

Saitou N and Nei M. The neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol Biol Evol 1987; 4(4): 406–425.

Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 1980; 16(2): 111–120.

Felsenstein J. Confidence limits on phylogenies: An approach using the bootstrap. Evol 1985; 39(4): 783–791.

Shirling ET and Gottlieb D. Methods for characterization of Streptomyces species1. Int J Syst Evol Microbiol 1966; 16(3): 313–340.

Atlas RM. Alphabetical listing of media. Handbook of microbiological media. CRC Press, Inc., Boca Raton, Fla, 1993; 455-462.

Mac Faddin JF. Biochemical tests for identification of medical bacteria. Williams & Wilkins Co; 1976.

Atlas RM. Handbook of microbiological media. CRC press; 2010.

Küster E and Williams ST. Selection of media for isolation of streptomycetes. Nature 1964; 202(4935): 928.

Kelly KL. Color-name charts illustrated with centroid colors. Inter Society Color Council-National Bureau of Standards, Chicago; 1964.

Lee L-H, Zainal N, Azman A-S, et al., Mumia flava gen. nov., sp. nov., an actinobacterium of the family Nocardioidaceae. Int J Syst Evol Microbiol 2014; 64(5): 1461–1467.

Carrillo PG, Mardaraz C, Pitta-Alvarez SI, et al. Isolation and selection of biosurfactant-producing bacteria. World J Microbiol Biotechnol 1996; 12(1): 82–84.

Meena B, Rajan LA, Vinithkumar NV, et al. Novel marine actinobacteria from emerald Andaman & Nicobar Islands: A prospective source for industrial and pharmaceutical byproducts. BMC Microbiol 2013; 13(1): 145.

Tan LT-H, Chan K-G, Khan TM, et al. Streptomyces sp. MUM212 as a source of antioxidants with radical scavenging and metal chelating properties. Front Pharmacol 2017; 8: 276.

Adjimani JP and Asare P. Antioxidant and free radical scavenging activity of iron chelators. Toxicol Rep 2015; 2: 721–728.

Tan LT-H, Chan K-G, Pusparajah P, et al. Mangrove derived Streptomyces sp. MUM265 as a potential source of antioxidant and anticolon-cancer agents. BMC Microbiol 2019; 19(1): 38.

Tomm HA, Ucciferri L, and Ross AC. Advances in microbial culturing conditions to activate silent biosynthetic gene clusters for novel metabolite production. J Ind Microbiol Biotechnol 2019; 1–20.

Ser H-L, Tan LT-H, Law JW-F, et al. Focused review: Cytotoxic and antioxidant potentials of mangrove-derived Streptomyces. Front Microbiol 2017; 8: 2065.

Alongi DM. Bacterial productivity and microbial biomass in tropical mangrove sediments. Microbial Ecol 1988; 15(1): 59–79.

Saricaoglu S, Isik K, Veyisoglu A, et al. Streptomyces burgazadensis sp. nov., isolated from soil. Int J Syst Evol Microbiol 2014; 64(12): 4043–4048.

He L, Li W, Huang Y, et al. Streptomyces jietaisiensis sp. nov., isolated from soil in northern China. Int J Syst Evol Microbiol 2005; 55(5): 1939–1944.

Pereira PHF, Macrae A, Reinert F, et al. Streptomyces odonnellii sp. nov., a proteolytic streptomycete isolated from soil under cerrado (savanna) vegetation cover. Int J Syst Evol Microbiol 2017; 67(12): 5211–5215.

Wu H, Liu B, Ou X, et al. Streptomyces thermoalkaliphilus sp. nov., an alkaline cellulase producing thermophilic actinomycete isolated from tropical rainforest soil. Antonie van Leeuwenhoek 2018; 111(3): 413–422.

Luo X-x, Kai L, Wang Y, et al. Streptomyces luteus sp. nov., an actinomycete isolated from soil. Int J Syst Evol Microbiol 2017; 67(3): 543–547.

Nachtigall J, Kulik A, Helaly S, et al. Atacamycins A–C, 22 membered antitumor macrolactones produced by Streptomyces sp. C38. J Antibiot 2011; 64(12): 775.

Tan LT-H, Chan K-G, Chan CK, et al. Antioxidative potential of a Streptomyces sp. MUM292 isolated from mangrove soil. BioMed Res Int 2018; 2018.

Law JW-F, Ser H-L, Ab Mutalib N-S, et al. Streptomyces monashensis sp. nov., a novel mangrove soil actinobacterium from East Malaysia with antioxidative potential. Sci Rep 2019; 9(1): 3056.

Nelson DL, Lehninger AL, and Cox MM. Lehninger principles of biochemistry. Macmillan; 2008.

Yasuda M, Ohzeki Y, Shimizu S, et al. Stimulation of in vitro angiogenesis by hydrogen peroxide and the relation with ETS-1 in

endothelial cells. Life Sci 1998; 64(4): 249–258.

Niethammer P, Grabher C, Look AT, et al. A tissue-scale gradient of hydrogen peroxide mediates rapid wound detection in zebrafish. Nature 2009; 459(7249): 996.

Fajardo AF, Sobchak C, Shifrin Y, et al. Hydrogen peroxide promotes gastric motility in the newborn rat. Pediatr Res 2018; 84(5):

Ighodaro O and Akinloye O. First line defence antioxidants superoxide dismutase (SOD), catalase (CAT) and glutathione peroxidase (GPX): Their fundamental role in the entire antioxidant defence grid. Alexandria J Med 2018; 54(4): 287–293.

Ghosh N, Das A, Chaffee S, et al. Reactive Oxygen Species, Oxidative Damage and Cell Death, in Immunity and Inflammation in Health and Disease. Elsevier; 2018; p. 45–55.

Henriksen EJ. Role of Oxidative Stress in the Pathogenesis of Insulin Resistance and Type 2 Diabetes, in Bioactive Food as Dietary Interventions for Diabetes. Elsevier; 2019; p. 3–17.

Bose A and Beal MF. Mitochondrial dysfunction and oxidative stress in induced pluripotent stem cell models of Parkinson’s disease. Eur J Neurosci 2019; 49(4): 525–532.

Kashyap D, Tuli HS, Sak K, et al. Role of reactive oxygen species in cancer progression. Curr Pharmacol Rep 2019; 1–8.

Förstermann U, Xia N, and Li H. Roles of vascular oxidative stress and nitric oxide in the pathogenesis of atherosclerosis. Circ Res 2017; 120(4): 713–735.

Oikawa S, Nishino K, Oikawa S, et al. Oxidative DNA damage and apoptosis induced by metabolites of butylated hydroxytoluene. Biochem Pharmacol 1998; 56(3): 361–370.

Kahl R and Kappus H. Toxicology of the synthetic antioxidants BHA and BHT in comparison with the natural antioxidant vitamin E. Zeitschrift Fur Lebensmittel-Untersuchung Und-Forschung 1993; 196(4): 329–338.

Resende LM, Franca AS, and Oliveira LS. Buriti (Mauritia flexuosa L. f.) fruit by-products flours: Evaluation as source of dietary fibers and natural antioxidants. Food Chem 2019; 270: 53–60.

Samotyja U. Potato peel as a sustainable resource of natural anti oxidants for the food industry. Potato Research 2019; 1–17.

Cefali LC, Franco JG, Nicolini GF, et al. In vitro antioxidant activity and solar protection factor of blackberry and raspberry extracts in topical formulation. J Cosmet Dermatol 2019; 18(2): 539–544.

Tan JBL and Lim YY. Critical analysis of current methods for assessing the in vitro antioxidant and antibacterial activity of plant extracts. Food Chem 2015; 172: 814–822.

Benzie IF and Strain JJ. The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: The FRAP assay. Anal Biochem 1996; 239(1): 70–76.

Loschen G, Azzi A, Richter C, et al. Superoxide radicals as precursors of mitochondrial hydrogen peroxide. FEBS Lett 1974; 42(1): 68–72.

FentonH J. Oxidationoftartaricacidinpresenceof iron. J Chem Soci, Trans 1894; 65: 899–910.

Dholakiya RN, Kumar R, Mishra A, et al. Antibacterial and antioxidant activities of novel actinobacteria strain isolated from Gulf of Khambhat, Gujarat. Front Microbiol 2017; 8: 2420.

Ser H-L, Yin W-F, Chan K-G, et al. Antioxidant and cytotoxic potentials of Streptomyces gilvigriseus MUSC 26T isolated from mangrove soil in Malaysia. Prog Microbes Mol Biol 2018; 1(1).

Kadhim MJ, Mohammed GJ, and Hussein H. Analysis of bioactive metabolites from Candida albicans using (GC-MS) and evaluation of antibacterial activity. Int J Pharm Clin Res 2016; 8(7): 655–670.

Kadhim M. In vitro antifungal potential of Acinetobacter baumannii and determination of its chemical composition by gas chromatographymass spectrometry. Der Pharma Chem 2016; 8(19): 657–665.

Liu X, Dong M, Chen X, et al. Antioxidant activity and phenolics of an endophytic Xylaria sp. from Ginkgo biloba. Food Chem 2007; 105(2): 548–554.

Thirumurugan D and Vijayakumar R. A potent fish pathogenic bacterial killer Streptomyces sp. isolated from the soils of east coast region, South India. J Coastal Life Med 2013; 1(3): 175–180.

Hameed IH, Hamza LF, and Kamal SA. Analysis of bioactive chemical compounds of Aspergillus niger by using gas chromatography-mass spectrometry and fourier-transform infrared spectroscopy. J Pharmacogn Phytother 2015; 7(8): 132–163.

Al-Jassaci M, Mohammed G, and Hameed I. Secondary metabolites analysis of Saccharomyces cerievisiae and evaluation of antibacterial activity. Int J Pharm Clin Res 2016; 8(5): 304–315.

Altaee N, Kadhim MJ, and Hameed IH. Detection of volatile compounds produced by Pseudomonas aeruginosa isolated from UTI patients by gas chromatography-mass spectrometry. Int J Curr Pharm Rev Res 2017; 7(6): 8–24.

Azman A-S, Othman I, Fang C-M, et al. Antibacterial, anticancer and neuroprotective activities of rare Actinobacteria from mangrove forest soils. Indian J Microbiol 2017; 57(2): 177–187.

Mathew S, Abraham TE, and Zakaria ZA. Reactivity of phenolic compounds towards free radicals under in vitro conditions. J Food Sci Technol 2015; 52(9): 5790–5798.

Bendary E, Francis R, Ali H, et al. Antioxidant and structure activity relationships (SARs) of some phenolic and anilines compounds. Ann Agri Sci 2013; 58(2): 173–181.

Kawahara T, Izumikawa M, Otoguro M, et al. JBIR-94 and JBIR- 125, antioxidative phenolic compounds from Streptomyces sp. R56-07. J Nat Prod 2012; 75(1): 107–110.

Haneishi T, Arai M, Kitano N, et al. Aspiculamycin, a new cytosine nucleoside antibiotic. J Antibiot 1974; 27(5): 339–342.

Wiwanitkit V, Interest in paromomycin for the treatment of visceral leishmaniasis (kala-azar). Ther Clin Risk Manage 2012; 8: 323.


  • There are currently no refbacks.

Copyright (c) 2019 Hefa Mangzira Kemung, Loh Teng-Hern Tan, Kok-Gan Chan, Hooi-Leng Ser, Jodi Woan-Fei Law, Learn-Han Lee, Bey-Hing Goh

Creative Commons License
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.