Biological activity of sponge-associated fungi from Karimunjawa Islands, Indonesia against pathogenic Streptococcus pneumoniae




Abstract. Cristianawati O, Sabdaningsih A, Becking LE, Khoeri MM, Nuryadi H, Sabdono A, Trianto A, Radjasa OK. 2019. Biological activity of sponge-associated fungi from Karimunjawa Islands, Indonesia against pathogenic Streptococcus pneumoniae. Biodiversitas 20: 2143-2150. Threats of drug-resistant Streptococcus pneumoniae and the urgent need for new antibiotics require prompt and sustained action for discovering bioactive compounds. This study aimed to isolate sponge-associated fungi as a candidate for sources of drugs. The sponge-associated fungi were screened against the MDR S. pneumoniae. The Deoxyribonucleic Acid (DNA) of fungal isolates that showed the most active was generated by using universal primers ITS1 and ITS4. While the sponge host was identified based on the molecular and by slide section. Out of twenty-nine fungal isolates from 13 marine sponges, S.06.2 isolate produced secondary metabolite that inhibiting the growth of MDR S. pneumoniae. Molecular identification based on the ITS region revealed that the active fungal isolate was closely related to Curvularia lunata, with a 99% similarity. The C. lunata S.06.2 was isolated from sponge Cinachyrella australiensis. Thus, C. lunata S.06.2_ LC315806 can serve as a fruitful strategy for the discovery of novel antibiotics for the treatment of MDR S. pneumoniae.


A Brakhage A, Spröte , Al-Abdallah Q, Gehrke A, Plattner H and Tüncher A. 2004. Regulation of Penicillin Biosynthesis in Filamentous Fungi.
Blunt JW, Copp BR, Munro MH, Northcote PT and Prinsep MR. 2010. Marine natural products. Nat Prod Rep 27(2), 165-237.
Bolanos J, De Leon LF, Ochoa E, Darias J, Raja HA, Shearer CA, Miller AN, Vanderheyden P, Porras-Alfaro A and Caballero-George C. 2015. Phylogenetic Diversity of Sponge-Associated Fungi from the Caribbean and the Pacific of Panama and Their In Vitro Effect on Angiotensin and Endothelin Receptors. Mar Biotechnol (NY) 17(5), 533-564.
Buttachon S, May Zin WW, Dethoup T, Gales L, Pereira JA, Silva AM and Kijjoa A. 2016. Secondary Metabolites from the Culture of the Marine Sponge-Associated Fungi Talaromyces tratensis and Sporidesmium circinophorum. Planta Med 82(9-10), 888-896.
Cárdenas P, Rapp HT, Schander C and Tenda OS. 2010. Molecular taxonomy and phylogeny of the Geodiidae (Porifera, Demospongiae, Astrophorida) – combining phylogenetic and Linnaean classification. Zoologica Scripta 39(1), 89-106.
Carter HJ. 1886. Descriptions of Sponges from the Neighbourhood of Port Phillip Heads, South Australia continued. Annals and Magazine of Natural History.
CDC. Ceters for Diseases Control. 2017.
Cherazard R, Epstein M, Doan TL, Salim T, Bharti S and Smith MA. 2017. Antimicrobial Resistant Streptococcus pneumoniae: Prevalence, Mechanisms, and Clinical Implications. Am J Ther 24(3), e361-e369.
Chombard C, Boury-Esnault N and Tillier S. 1998. Reassessment of Homology of Morphological Characters in Tetractinellid Sponges Based on Molecular Data. Systematic Biology 47(3), 351-366.
Cleary D, Becking L, de Voogd N, Pires A, Polónia A.M, Egas C and Gomes N. 2013. Habitat- and host-related variation in sponge bacterial symbiont communities in Indonesian waters.
Corral P, Esposito F., Tedesco P, Falco A, Tortorella E, Tartaglione L, Festa C, D'Auria MV, Gnavi G, Varese GC and de Pascale D. 2018. Identification of a Sorbicillinoid-Producing Aspergillus Strain with Antimicrobial Activity Against Staphylococcus aureus: a New Polyextremophilic Marine Fungus from Barents Sea. Mar Biotechnol (NY).
Cristianawati O, Radjasa OK, Sabdono A, Trianto A, Sabdaningsih A, Sibero MT and Nuryadi H. 2017. Exploration of Fungal Association From Hard Coral Against Pathogen MDR Staphylococcus haemolyticus. IOP Conference Series: Earth and Environmental Science 55(1), 012027.
Ding Y, An F, Zh X., Yu H, Hao L and Lu Y. 2019. Curdepsidones B(-)G, Six Depsidones with Anti-Inflammatory Activities from the Marine-Derived Fungus Curvularia sp. IFB-Z10. Mar Drugs 17(5).
Ditjen P2P KK. 2018. Health Statistics 2017.
DKP-Jateng DKPJT. 2014. Profil Kesehatan Provinsi Jawa Tengah Tahun 2014.
Dunne EM, Mura C, Sudigdoadi S, Fadlyana E, Tarigan R, Indriyani SAK, Pell CL, Watts E, Satzke C, Hinds J, Dewi NE, Yani FF, Rusmil K. Mulholland K. and Kartasasmita C. 2018. Carriage of Streptococcus pneumoniae, Haemophilus influenzae, Moraxella catarrhalis, and Staphylococcus aureus in Indonesian children: A cross-sectional study. PLoS One 13(4), e0195098.
Erpenbeck D, Voigt O, M Al-Aidaroos A, Berumen M, Büttner G, Catania D, Naguib Guirguis A. Paulay G, Schätzle S and Wörheide G. 2016, Molecular biodiversity of Red Sea demosponges.
Farida H, Severin JA, Gasem MH, Keute M, Wahyono H, van den Broek P, Hermans PW and Verbrugh HA. 2014. Nasopharyngeal carriage of Streptococcus pneumonia in pneumonia-prone age groups in Semarang, Java Island, Indonesia. PLoS One 9(1), e87431.
Folme O, Black M, Wr H, Lutz R and Vrijenhoek R. 1994. DNA primers for amplification of mitochondrial Cytochrome C oxidase subunit I from diverse metazoan invertebrates.
Greve H, Schupp PJ, Eguereva E, Kehraus S, Kelter G, Maier A, Fiebig HH and Konig GM. 2008. Apralactone A and a New Stereochemical Class of Curvularins from the Marine-Derived Fungus Curvularia sp. European J Org Chem 2008(30).
Hajaj B, Yesilkaya H, Shafeeq S, Zhi X, Benisty R, Tchalah S, Kuipers OP and Porat N. 2017. CodY Regulates Thiol Peroxidase Expression as Part of the Pneumococcal Defense Mechanism against H2O2 Stress. Front Cell Infect Microbiol 7, 210.
Ha WB, Lu YH, Zhang H, Zhang GF, Mei YN, Jiang N, Lei X, Song C, Ng SW and Ta RX. 2014. Curvulamine, a new antibacterial alkaloid incorporating two undescribed units from a Curvularia species. Org Lett 16(20), 5366-5369.
Hu J, Su X, Huang Z, Wagner L, Carlson B, Yan J, Tang S, Li , Boulton ML and Yuan Z. 2016. Streptococcus pneumoniae and Haemophilus influenzae type b carriage in Chinese children aged 12-18 months in Shanghai, China: a cross-sectional study. BMC Infect Dis 16, 149.
Imhoff JF. 2016. Natural Products from Marine Fungi--Still an Underrepresented Resource. Mar Drugs 14(1), 19.
Indraningrat AA, Smidt H and Sipkema D. 2016. Bioprospecting Sponge-Associated Microbes for Antimicrobial Compounds. Mar Drugs 14(5).
Kadioglu A, Weiser JN, Paton JC and Andrew PW. 2008. The role of Streptococcus pneumoniae virulence factors in host respiratory colonization and disease. Nat Rev Microbiol 6(4), 288-301.
Khoeri M, Radjasa OK, Sabdono A and Sudoyo H. 2011. Bioprospecting of Bacterial Symbiont of Tunicate Didemnum molle from Sambangan, Karimunjawa Islands.
Kimura M.1981.A Simple Method for Estimating Evolutionary Rate of Base Substitutions Through Comparative Studies of Nucleotide Sequences.
Kobayashi J and Ishibash M. 1993. Bioactive metabolites of symbiotic marine microorganisms. Chemical Reviews 93(5), 1753-1769.
Lafay B, Smith AB and Christen R. 1995. A Combined Morphological and Molecular Approach to the Phylogeny of Asteroids (Asteroidea: Echinodermata). Systematic Biology 44(2), 190-208.
Lang G, Wiese J, Schmaljohan R and Imhoff J. 2007. New pentaenes from the sponge-derived marine fungus Penicillium rugulosum: structure determination and biosynthetic studies.
Le HL, Lecointre G and Perasso R. 1993. A 28S rRNA-based phylogeny of the gnathostomes: first steps in the analysis of conflict and congruence with morphologically based cladograms. Mol Phylogenet Evol 2(1), 31-51.
Lestari ES, Severin JA and Verbrugh HA. 2012. Antimicrobial resistance among pathogenic bacteria in Southeast Asia. Southeast Asian J Trop Med Public Health 43(2), 385-422.
Liu WH, Ding Y, Ji X, An FL and Lu YH. 2019. Curvulaide A, a bicyclic polyketide with anti-anaerobic bacteria activity from marine-derived Curvularia sp. J Antibiot (Tokyo) 72(2), 111-113.
Mayer AM, Rodriguez AD, Taglialatela-Scafati O and Fusetani N. 2013. Marine pharmacology in 2009-2011: marine compounds with antibacterial, antidiabetic, antifungal, anti-inflammatory, antiprotozoal, antituberculosis, and antiviral activities; affecting the immune and nervous systems, and other miscellaneous mechanisms of action. Mar Drugs 11(7), 2510-2573.
Mirza S, Wilson L, Benjamin WH, Jr, Novak J, Barnes S, Hollingshead SK and Briles DE. 2011. Serine protease PrtA from Streptococcus pneumoniae plays a role in the killing of S. pneumoniae by apolactoferrin. Infect Immun 79(6), 2440-2450.
Mondol MA, Farthouse J, Islam MT, Schuffler A and Laatsch H. 2017. Metabolites from the Endophytic Fungus Curvularia sp. M12 Act as Motility Inhibitors against Phytophthora capsici Zoospores. J Nat Prod 80(2), 347-355.
Nurhayati APD, Pratiwi R, Wahyuono S, Istriyati I and de Voogd N. 2015. The Anticancer Activity of Marine Sponge Cinachyrella sp. (Family Tetillidae).
O'Brien KL, Wolfson LJ, Watt JP, Henkle E, Deloria-Knoll M, McCall N, Lee E, Mulholland K, Levine OS and Cherian T. 2009. Burden of disease caused by Streptococcus pneumoniae in children younger than 5 years: global estimates. Lancet 374(9693), 893-902.
Qiu WY, Yao YF, Zhu YF, Zhang YM, Zhou P, Jin YQ and Zhang B. 2005. Fungal spectrum identified by a new slide culture and in vitro drug susceptibility using Etest in fungal keratitis. Curr Eye Res 30(12), 1113-1120.
Radjasa OK, Khoeri MM, Chelzie C, Darusallam Trimasanto H and Sudoyo H. 2013. Bacterial symbionts of reef invertebrates: Screening for anti-pathogenic bacteria activity.
Raghukumar C. 2008. Marine fungal biotechnology: An ecological perspective.
Rahaweman AC, Pamungkas J, Madduppa H, Thoms C and Tarman K. 2016. Screening of Endophytic Fungi from Chlorophyta and Phaeophyta for Antibacterial Activity. IOP Conference Series: Earth and Environmental Science 31(1), 012026.
Sabdaningsih A, Cristianawati O, Sibero MT, Nuryadi H, Radjasa OK, Sabdono A and Trianto A. 2017. Screening Antibacterial Agent from Crude Extract of Marine-Derived Fungi Associated with Soft Corals against MDR- Staphylococcus haemolyticus. IOP Conference Series: Earth and Environmental Science 55(1), 012026.
Safari D, Harimurti K, Khoeri MM, Waslia L, Mudaliana S, A'Yun H Q, Angeline R and Subekti D. 2015. Staphylococcus aureus and Streptococcus pneumoniae Prevalence among Eldery Adults in Jakarta, Indonesia. Southeast Asian J Trop Med Public Health 46(3), 465-471.
Saleem M, Shaiq Ali M, Hussain S, Jabbar A, Ashraf M and Sup Lee Y. 2007. ChemInform Abstract: Marine Natural Products of Fungal Origin.
Sibero MT, Sabdaningsih A, Cristianawati O, Nuryadi H, Radjasa OK, Sabdono A and Trianto A. 2017. Isolation, Identification And Screening Antibacterial Activity from Marine Sponge-Associated Fungi Against Multidrug-Resistant (MDR) Escherichia coli. IOP Conference Series: Earth and Environmental Science 55(1), 012028.
Smith AB, Paterson GLJ and Lafay B. 2011. Ophiuroid phylogeny and higher taxonomy: morphological, molecular and palaeontological perspectives. Zoological Journal of the Linnean Society 114(2), 213-243.
Strobel G and Daisy B. 2003. Bioprospecting for microbial endophytes and their natural products. Microbiol Mol Biol Rev 67(4), 491-502.
Trianto A, Sabdono A, Rochaddi B, Desy A and Triningsih D. 2017. Exploration Of Marine Sponges-Associated Fungi Producing Antifungal Compounds.
van Soest R, Meesters E and Becking L. 2014. Deep-water sponges (Porifera) from Bonaire and Klein Curaçao, Southern Caribean.
Van Soest RWMBE, Hooper JNA, Rützler K, de Voogd J, Alvarez, B, Hajdu E, Pisera B, Manconi, R, Schönberg C, Klautau M, Picton B, Kell M, Vacelet J, Dohrman M, Díaz, MC, Cárdenas P, Carballo JL, Ríos P, Downey R. 2019. World Porifera Database. Cinachyrella Wilson, 1925.
Vasanthabharathi V. 2012. Bioactive potential of symbiotic bacteria and fungi from marine sponges.
Venkatachalam G, Ambayeram V, Suryanarayanan T and Doble M. 2011. Isolation and Characterization of New Antioxidant and Antibacterial Compounds from Algicolous Marine Fungus Curvularia Tuberculata.
Vicente J, Stewart A, Song B, Hill RT and Wright JL. 2013. Biodiversity of Actinomycetes associated with Caribbean sponges and their potential for natural product discovery. Mar Biotechnol (NY) 15(4), 413-424.
Volgraf M, Lumb JP, Brastianos HC, Carr, Chung MK, Munzel M, Mauk AG, Andersen RJ and Trauner D. 2008. Biomimetic synthesis of the IDO inhibitors exiguamine A and B. Nat Chem Biol 4(9), 535-537.
von Rintelen K, Arida E and Häuser C. 2017. A review of biodiversity-related issues and challenges in megadiverse Indonesia and other Southeast Asian countries.
WHO. 2017. WHO publishes list of bacteria for which new antibiotics are urgently needed.
Yin C, Jin L, Sun F, Xu X, Shao M and Zhang Y. 2018. Phytotoxic and Antifungal Metabolites from Curvularia crepinii QTYC-1 Isolated from the Gut of Pantala flavescens. Molecules (Basel, Switzerland) 23(4), 951.
Yu Z, Lang G, Kajahn I, Schmaljohann R and Imhoff JF. 2008. Scopularides A and B, cyclodepsipeptides from a marine sponge-derived fungus, Scopulariopsis brevicaulis. J Nat Prod 71(6), 1052-1054.
Yuliarti K, Hadinegoro S, Supriyatno B and Karuniawati A. 2012. Invasive pneumococcal disease among hospitalized children aged 28 days to 60 months in Jarkarta.

Most read articles by the same author(s)

1 2 3 > >>