Evaluation of antimicrobial activity and identification of yellow pigmented marine sponge-associated fungi from Teluk Awur, Jepara, Central Java


Mada Triandala Sibero(1*), Desy Wulan Triningsih(2), Ocky Karna Radjasa(3), Agus Sabdono(4), Agus Trianto(5)

(1) Department of Coastal Resources Management, Faculty of Fisheries and Marine Science, Diponeggoro University, St. Imam Bardjo, SH., Semarang 50241, Central Java, Indonesia
(2) Laboratory of Marine Natural Product, Integrated Laboratory of Diponegoro University, St. Prof. Soedarto, SH., Tembalang, Semarang 50269, Central Java, Indonesia
(3) Department of Coastal Resources Management, Faculty of Fisheries and Marine Science, Diponeggoro University, St. Imam Bardjo, SH., Semarang 50241, Central Java, Indonesia
(4) Department of Marine Science, Faculty of Fisheries and Marine Science, Diponegoro University, St. Prof. Soedarto, SH., Tembalang, Semarang 50269, Central Java, Indonesia
(5) Department of Marine Science, Faculty of Fisheries and Marine Science, Diponegoro University, St. Prof. Soedarto, SH., Tembalang, Semarang 50269, Central Java, Indonesia
(*) Corresponding Author


Marine sponge associated fungi are known as potential source of metabolites with various biological activities. Natural pigment is one of metabolite which produced by microorgisms. Several researches reported the antimicrobial activity from natural pigment. Unfortunatelly there are lack of information about marine fungi natural pigment and its producer. The aims of this research were to identify yellow pigmented Indonesian marine sponge-associated fungi, to extract the pigment, and to study the antimicrobial activity of the pigment against clinical MDR bacteria and clinical pathogenic fungi. Sponge associated-fungus isolate MT23 was successfully identified as Trichoderma parareesei. The fungal pigment could be extracted only in methanol with yield 6,22±0,29%. The pigment could inhibitted S. typhi and E. coli MDR strains. The biggest antibacterial activity was shown by concentration 1000µg/mL against S. typhi with inhibition zone was 4.03±0.06 mm.


associated fungi; pigment; Trichoderma parareesi

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Abu-Ghannam, N., Rajauria, G. 2013. Antimicrobial activity of compounds isolated from algae. In Functional Ingredients from Algae for Foods and Nutraceuticals; Domínguez, H., Ed. Cambridge (UK): Woodhead Publishing.

Anderson, I.C., Campbell, C. D., Prosser, J. I. 2003. Potential bias of fungal 18S rDNA and internal transcribed spacer polymerase chain reaction primers for estimating fungal biodiversity in soil. Environmental Microbiology 5(1): 36-47.

Atanasova L, Jaklitsch WM, Komoń-Zelazowska M, Kubicek CP, Druzhinina IS. 2010. Clona species Trichoderma parareesi sp. nov. likely resembles the ancestor of the cellulase producer Hypocrea jecorina/T. reesi. Applied and Environmental Microbiology 76(21): 7259-7267.

Avalos, J., Limon, M. C. 2015. Biological roles of fungal carotenoids. Current Genetic 61(3): 309-324. Balouiri, M., Sadiki, M., Ibnsouda, S. K. 2016. Methods for in vitro evaluating antimicrobial activity: A review. Journal of Pharmaceutical Analysis 6: 71-79.

Bellemain, E., Carlsen, T., Brochmann, C., Coissac, E., Taberlet, P., Kauserud, H. 2010. ITS as an environmental DNA barcode for fungi: an in silico approach reveals potential PCR biases. BMC Microbiology 10(189): 1-9.

Benkada, M. M., Pouchus, Y. F., Vérite, P., Pagniez, F., Caroff, N., Ruiz, N. 2016. Identification and biological activities of long-chain peptaibols produced by a marine-derived strain of Trichoderma longibrachiatum. Chemistry and Biodiversity 13: 521-530.

Bhalodia, N. R. and Shukla, V. J. 2011. Antibacterial and antifungal activities from leaf extracts of Cassia fistula l.: An ethnomedicinal plant. Journal of Advanced Pharmaceutical Technology and Research 2(2): 104-109.

Bhat MR and Marar T. 2015. Media optimization, extraction and partial characterization of an orange pigment from Salinicoccus sp. MKJ 997975. International Journal of Life Sciences Biotechnology and Pharma Research 4(2): 85-89.

Blumenstein, A., Vienken, K., Purschwitz, J., Tasler, R., Frankenberg, N., Fischer, R. 2005. The phytochrome FphA controls development in the filamentous fungus Aspergillus nidulans. Current Biology. 15: 1833–1838.

Celestino, J., dos, R., de Carvalho, L. E., Lima, M. da P., Lima, A. M., Ogusku, M. M., de Souza, J. V. B. (2014). Bioprospecting of Amazon soil fungi with the potential for pigment production. Process Biochemistry 49: 569–575.

de Costa Souza, P. N., Grigoletto, T. L. B., de Moraes, L. A. B., Abreu, L. M., Guimaraes, L. H. S., Santos, C., Galvao, L. R., Cardoso, P. G. 2016. Production and chemical characterization of pigments in filamentous fungi. Microbiology 162: 12-22.

Delgado-Vargas F, Jiménez AR, Paredes-Lόpez O. 2000. Natural pigments: carotenoids, anthocyanins, and betalains-characteristics, biosynthesis, processing and stability. Critical Reviews in Foods Science and Nutrition 40(3): 173-289.

Dong, Z., Saikumar, P., Weinberg, J. M., Venkatachalam, M. A. 1997. Internucleosomal DNA cleavage triggered by plasma membrane damage during necrotic cell death. Involvement of serine but not cysteine proteases. American Journal of Pathology 151(5): 1205-1213.

El Komy, M. H., Saleh, A. A., Eranthodi, A., Molan, Y. Y. 2015. Characterization of novel Trichoderma asperellum isolates to selects effective biocontrol agents against tomato Fusrium wilt. The Plant Pathology Journal 31(1): 50-60.

Ernawita, Wahyuono, R. A., Hesse, J., Hipler, U. C., Elsner, P., Bӧhm, V. 2016. Carotenoids of indigenous citrus pecies from Aceh and its in vitro antioxidant, antidiabetic and antibacterial activities. European Food Research and Technology 242(11): 1869-1881.

Gal-Hemed, I., Atanasova, L., Komon-Zelazowska, M., Druzhinina, I. S., Viterbo, A., Yarden, O. Marine isolates of Trichoderma spp. as potential halotolerant agents of biological control for arid-zone agriculture. Applied and Environmental Microbiology 77(15): 5100-5109.

Geweely, N. S. 2012. Investigation of the optimum condition and antimicrobial activities of pigments from four potent pigments-producing fungal species. Journal of Life Science 5: 697-711.

Hamed, R. E., Awad, H. M., Ghazi, E. A., El-Gamal, N. G., Shehata, H. S. 2015. Trichoderma asperellum isolated from salinity soil using rice srtaw waste as biocontrol agent for cowpea plant pathogens. Journal of Applied Pharmaceutical Science 5(2): 91-98.

Houseknecht JL, Suh SO, Zhou J. 2011. Trichoderma parareesei ATCC MYA-4777 ITS region; from TYPE material. https://www.ncbi.nlm.nih.gov/nucleotide/1051341416?report=genbank&log$=nuclalign&blast_rank=2&RID=5RZZ5WVG01R

Ibrahim D, Nazari TF, Kassim J, Lim SH. 2014. Prodigiosin-an antibacterial red pigment produced by Serratia marcescens IBRL USM 84 associated with a marine sponge Xestospongia testudinaria. Journal of Applied Pharmaceutical Science 4(10): 001-006.

Idraningrat, A. A. G., Smidt, H., Sipkema, D. 2016. Bioprospecting sponge-associated microbes for antimicrobial compounds. Marine Drugs 14(5): 87.

Larena, I., Salazar, O., González, V., Julián, M. C., Rubio, V. 1999. Design of a primer for ribosomal DNA internal transcribed spacer with enhanced specidy for ascomycetes. Journal of Biotechnology 75: 187-194.

Liu, L., Wang, C. L., Peng, W. Y., Yang, J., Lan, M. Q., Zhang, B., Li, J. B., Zhu, Y. Y., Li, C. Y. 2015. Direct DNA extraction method on an obligate parasitic fungus from infected plant tissue. Genetic and Molecular Research 14(4): 18546-18551.

Magiorakos, A. P., Srinivasan, A., Carey, R. B., Carmeli, Y., Falagas, M. E., Giske, C. G., Harbarth, S., Hindler, J. F., Kahlmeter, G., Olsson-Liljequist, B., Paterson, D. L., Rice, L. B., Stelling, J., Struelens, M. J., Vatopoulos, A., Weber, J. T., Monnet, D. L. 2012. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clinical Microbiology and Infection 18(3):268-281.

Manikkam, R., Venugopal, G., Ramasamy, B., Kumar, V. 2015. Efeect of critical medium components and culture conditions on antitubercular pigment production from novel Streptomyces sp. D25 isolated from Thar desert, Rajasthan. Journal of Applied Pharmaceutical Science 5(06): 015-019.

Méndez, A., Pérez, C., Montanez, J. C., Martinéz, G., Aguilar, C. N. 2011. Red pigment production by Penicillium purpurogenum GH2 is influenced by pH and temperature. Journal of Zhejiang University 12(12): 961-968.

Nilsson, R. H., Ryberg, M., Abarenkov, K., Sjӧkvist, E., Kristiansson, E. 2009. The ITS region as a target for characterization of fungal communities using emerging sequencing technologies. FEMS Microbiologi Letter 296: 97-101.

Norman M, Bartczak P, Zdarta J, Ehrlich H, Jesionowski. 2016. Anthocyanin dye conjugated with Hippospongia communis marine demosponge skeleton and its antiradical activity. Dyes and Pigments 134: 541-552.

Pradeep FS and Pradeep BV. 2013. Optimization of pigment and biomass production from Fusharium moniliforme under submerged fermentation conditions. International Journal of Pharmacy and Pharmaceutical Sciences 5(3): 526-535.

Pradeep, F. S., Begam, M. S., Palaniswamy, M., Pradeep, B. V. 2013. Influence of culture media on growth and pigment production by Fusarium moniliforme KUMBF1201 isolated from paddy field soil. World Applied Sciences Journal 22: 70–77.

Qin WT and Zhuang WY. 2016. Seven wood-inhabiting new species of the genus Trichoderma (fungi, ascomycota) in Viride clade. Scientific Reports 6(27074): 1-14.

Qiu W. Y., Yao, Y. F., Zhu, Y. Y., Zhang, Y. M., Zhou P., Jin, Y. Q., Zhang, B. 2005. Fungal Spectrum Identified by a New Slide Culture and In Vitro Drug susceptibility Using Etest in Fungal Keratitis. Curretnt Eye Research 30: 1113-1120.

Radhakrishnan, M., Gopikrishnan, V., Vijayalakshmi, G., Kumar, V. 2016. In vitro antioxidant activity and antimicrobial activity against biofilm forming bacteria by the pigment from desert soil Streptomyces sp D25. Journal of Applied Pharmaceutical Science 6(6): 148-150.

Rahman, A., Begum, M. F., Rahman, M., Bari, M. A., Illas, G. N. M., Alam, M. F. 2011. Isolation and identification of Trichoderma species from different habitats and their use for bioconversion of solid waste. Turkish Journal of Biology 35: 183-194.

Rinu, K., Sati, P., Pandey, A. 2013. Trichoderma gamsii (NFCCI 2177): A newly isolated endophytic, psychrotolerant, plant growth promoting, and antagonistic fungal strain. Journal of Basic Microbiology 54(5): 408-417.

Rostami, H., Hamedi, H., Yolmeh, M. 2016. Some biological activities of pigments extracted from Micrococcus roseus (PTCC 1411) and Rhodotorula glutinis (PTCC 5257). International Journal of Immunopathology and Pharmacology 29(4): 684-695.

Rubeena M, Neethu K, Sajith S, Sreedevi S, Priji P, Unni KN, Josh MKS, Jisha VN, Pradeep S, Benjamin S. 2013. Lignocellulotic activities of novel strain of Trichoderma harzianum. Advances in Bioscience and Biotechnology 3: 214-221.

Rymbai H, Sharma RR, Srivastav M. 2011. Biocolorants and its implications in health and food industry-a review. International Journal of Pharmtech Research 3(4): 2228-2244.

Salem, N., Msaada, K., Elkahoui, S., Mangano, G., Azaeiz, S., Slimen, I. B., Kefi, S., Pintore, G., Limam, F., Marzouk, B. 2014. Evaluation of antibacterial, antifungal, and antioxidant activities of Safflower natural dyes during flowering. BioMed Research International 2014: 1-10.

Saravanakumar, K., Arasu, V. S., Kathiresan, K. 2013. Effect of Trichoderma on soil phosphate solubilization and growth improvement of Avicennia marina. Aquatic Botany 104: 101-105.

Saravanan D dan Radhakrishnan M. 2016. Antimicrobial activity of pigments produced by fungi from Western Ghats. Journal of Chemical and Pharmaceutical Research 8(1):634-638.

Sasidharan, P., Raja, R., Karthik, C., Sharma, R., Arulselvi, P. I. 2013. Isolation and characterization of yellow pigmented producing Exiguobacterium sps. Journal of Biochemical Toxicology 4(4): 632-635.

Schoch, C. L., Seifert, K. A., Huhndorf, S., Robert, V., Spouge, J. L., Levesque, C. A., Chen, W., Concortium, F. B. 2012. Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for fungi. Proceedings of The National Academy of Sciences 109(16): 6241-6246.

Sibero, M. T., Tarman, K., Hanif, N. 2016. Characterization and photoprotector activity of endophytic fungal pigments from coastal plant sarang semut (Hydnophytum formicarum). Jurnal Pengolahan Hasil Perikanan Indonesia. 19(1): 1-8.

Srilekha, V., Krishna, G., Srinivas, S. V., Charya, S. M. A. 2016. Isolation and screening of marine pigmented bacteria from Nellore Coast for antimicrobial studies. Journal of Cell and Tissue Research 16(1): 5413-5419.

Sumanta N, Haque CI, Nishika J, Suprakash R. 2014. Spectrophotometric analysis of chlorophylls and carotenoids from commonly grown fern species by using various extracting solvents. Research Journal of Chemical Science 4(9): 63-69.

Suresh, M., Renugadevi, B., Brammavidhya, S., Iyapparaj, P., Anantharaman, P. 2015. Antibacterial ctivity of red pigment produced by Halolactibacillus alkaliphilus MSRD1—an isolate from seaweed. Applied Biochemistry and Biotechnology 176(1): 185-195.

Susilowati, R., Sabdono, A., Widowati, I. 2015. Isolation and characterization of bacteria associated with brown algae Sargassum spp. from Panjang Island and their antibacterial activity. Procedia Environmental Sciences 23: 240-246.

Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., Kumar, S. 2011. MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28(10): 2731-2739.

Turan, C., Nanni, I. M., Brunelli, A., Collina, M. 2015. New rapid DNA extraction method with Chelex from Venturia ineaqualis spores. Journal of Microbiological Methods 115: 139-143.

Ushakumari, U. N. U. and Ramanujan, R. 2013. Isolation of astaxanthin from marine yeast and study of its pharmacological activity. International Current Pharmaceutical Journal 2(3): 67-69.

Vacondio B, Birolli W, Ferreira I, Porto ALM. 2015. Biodegradation of pentachlorophenol by marine-derived fungus Trichoderma harzianum CBMAI 1677 isolated from ascidian Didemnun ligulum. Biocatalysis and Agricultural Biotechnology 4(2).

Velmurungan, P., Lee, Y. H., Venil, C. K., Laksmanaperumalsamy, P., Chae, J. C., Oh, B. T. 2010. Effect of light on growth, intracellular and extracellular pigment production by five pigment-producing filamentous fungi in synthetic medium. Journal of Bioscience and Bioengineering 109(4): 345-350.

Venil CK, Zakaria ZA, Ahmad WA. 2013. Bacterial pigments and their application. Process Biochemistry 48: 1065-1079.

Walsh, P. S., Metzger, D. A., Higuchi, R. 2013. Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. BioTechniques 54(3): 134-139.

Weber GL, Boonloed A, Naas KM, Koesdjojo MT, Remcho VT, Robinson SC. 2016. A method to stimulate production of extracellular pigments from wood-degrading fungi using a water carrier. Current Research in Environmental and Applied Mycology 6(3): 218-230.

White, T. J., Bruns, T., Lee, S., Talyor, J. (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis, M.A., Gelfand, D.H., Sninisky, J.J. and White, T. J. Eds. PCR protocols: a guide to methods and applications. San Diego (US): Academic Press. Hal: 315-322.

Wu, B., Oesker, V., Wiese, J., Schmaljohann, R., Imhoff, J. F. 2014. Two new antibiotic pyridones produced by a marine fungus Trichoderma sp. strain MF106. Marine Drugs 12: 1208-1219.

Yolmeh, M., Hamedi, H., Khomeiri, M. 2016. Antimicrobial activity of pigments extracted from Rhodotorula glutinis against some bacteria and fungi. Zahedan Journal of Research in Medical Sciences 18(12): 1-5.

Yoo, A. Y., Alnaeeli, M., Park, J. K. 2016. Production control and characterization of antibacterial carotenoids from the yeast Rhodotorula mucilaginosa AY-01. Process Biochemistry 51(4): 463-473.

DOI: https://doi.org/10.22146/ijbiotech.26058

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