Isolation and Molecular Identification of Endophytic Fungi Associated with Brown Algae for Inhibiting Escherichia coli ESBL
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Background: The marine environment is the main source of research on natural products in the future. In addition, marine microorganisms have been identified as a natural source capable of developing new antibiotic compounds, including controlling urinary tract infections caused by Escherichia coli ESBL. Purpose: This study aims to isolate, select, and test the potential of brown macroalgae endophytic fungi (Phaeophyceae) collected from the coastal waters of Sanur, Bali Province. Methods: Three types of brown algae were collected from Sanur Beach and their endophytic fungi were isolated using PDA media. Antibacterial activity was determined by measuring the inhibition zone and determining the inhibition category. The selected isolates were cultured and the phytochemical profile was determined qualitatively. In addition, molecular identification using the Internal Transcribed Spacer (ITS) primer set and comparison with the GenBank (NCBI) database were carried out in this study. Results: The results showed that 10 isolates were successfully isolated from three types of brown macroalgae. It was found that isolates T1, S1, and P3 had the highest inhibition in the very strong category. There were variations in mycelial weight, pH value, and inhibition shown by the culture filtrate of the three endophytic fungal isolates against Escherichia coli ESBL. Isolate S1 had the highest phytochemical profile, namely alkaloids, triterpenoids, saponins, and phenolics. The three endophytic fungal isolates showed isolate T1 (Phlebiopsis magnicystidiata) (MT5617191), isolate P3 (Neurospora crassa strain RT3M) (MT1028551), and isolate S1 (Peniophora sp.) (MH2680421). Conclusion: The results of this study provide initial information regarding the potential of bioprospecting brown macroalgal endophytic fungi as a source of new antibiotics against Escherichia coli ESBL.
Agyekum, A., Fajardo-Lubián, A., Ansong, D., Partridge, S.R., Agbenyega, T., and Iredell, J.R., 2016. blaCTX-M-15 Carried by IncF-type Plasmids is the Dominant ESBL Gene in Escherichia coli and Klebsiella pneumoniae at a hospital in Ghana. Diagnostic Microbiology and Infectious Disease, 84(4), 328–333.
Al-Mustapha, A. I., Raufu, I. A., Ogundijo, O. A., Odetokun, I. A., Tiwari, A., Brouwer, M. S. M., Adetunji, V., and Heikinheimo, A., 2023. Antibiotic Resistance Genes, Mobile Elements, Virulence Genes, And Phages in Cultivated ESBL-producing Escherichia coli of Poultry Origin in Kwara State, North Central Nigeria. International Journal of Food Microbiology, 389, 110086, 1-9.
Ali, S. S., El-Zawawy, N. A., Al-Tohamy, R., El-Sapagh, S., Mustafa, A. M., and Sun, J., 2020. Lycium shawii Roem. & Schult.: A New Bioactive Antimicrobial and Antioxidant Agent to Combat Multi-drug/ Pan-drug Resistant Pathogens of Wound Burn Infections. Journal of Traditional and Complementary Medicine, 10(1), 13–25.
An, C., Ma, S., Shi, X., Xue, W., Liu, C., and Ding, H., 2020. Diversity and Antimicrobial Activity of Endophytic Fungi Isolated from Chloranthus japonicus Sieb in Qinling Mountains, China. International Journal of Molecular Sciences, 21(17), 5958, 1-15.
Apsari, P. P., Budiarti, S., and Wahyudi, A. T., 2019. Actinomycetes of Rhizosphere Soil Producing Antibacterial Compounds Against Urinary Tract Infection Bacteria. Biodiversitas Journal of Biological Diversity, 20(5), 1259-1265.
Azuma, T., Uchiyama, T., Zhang, D., Usui, M., and Hayashi, T., 2022. Distribution and Characteristics of Carbapenem-resistant and Extended-spectrum β-lactamase (ESBL) producing Escherichia coli in Hospital Effluents, Sewage Treatment Plants, and River Water in An Urban Area of Japan. Science of The Total Environment, 839, 156232, 1-10.
Bonugli-santos, R. C., Durrant, L. R., and Sette, L. D., 2010. Laccase Activity and Putative Laccase Genes in Marine-derived Basidiomycetes. Fungal Biology, 114(10), 863–872.
Chaudhary, P., Agri, U., Chaudhary, A., Kumar, A., and Kumar, G., 2022. Endophytes and Their Potential in Biotic Stress Management and Crop Production. Frontiers in Microbiology, 13, 1-22.
Dalazen, G., Fuentes-Castillo, D., Pedroso, L. G., Fontana, H., Sano, E., Cardoso, B., Esposito, F., Moura, Q., Matinata, B. S., Silveira, L. F., Mohsin, M., Matushima, E. R., and Lincopan, N., 2023. Ctx-m-producing Escherichia Coli ST602 Carrying A Wide Resistome in South American Wild Birds: Another Pandemic Clone of One Health Concern. One Health, 17, 100586, 1-7.
de Felício, R., Paví£o, G.B., de Oliveira, A. L. L., Erbert, C., Conti, R., Pupo, M.T., Furtado, N. A.J.C., Ferreira, E. G., Costa-Lotufo, L.V., Young, M.C.M., Yokoya, N.S., and Debonsi, H.M., 2015. Antibacterial, Antifungal and Cytotoxic Activities Exhibited by Endophytic Fungi from The Brazilian Marine Red Alga Bostrychia tenella (Ceramiales). Revista Brasileira de Farmacognosia, 25(6), 641–650.
Deutsch, Y., Gur, L., Berman Frank, I., and Ezra, D., 2021. Endophytes From Algae, a Potential Source for New Biologically Active Metabolites for Disease Management in Aquaculture. Frontiers in Marine Science, 8, 1-13.
El-Zawawy, N. A., Ali, S. S., Khalil, M. A., Sun, J., and Nouh, H.S., 2022. Exploring The Potential of Benzoic Acid Derived from The Endophytic Fungus Strain Neurospora crassa SSN01 as A Promising Antimicrobial Agent in Wound Healing. Microbiological Research, 262, 127108.
Falodun, O. I., Afolabi, M. C., and Rabiu, A.G., 2022. Detection of Extended Spectrum β-lactamase (ESBL) genes in Escherichia coli Isolated from Fecal Samples of Apparently Healthy Dogs in Ibadan, Nigeria. Animal Gene, 26, 200133.
Gong, A., Zhou, T., Xiao, C., Jiang, W., Zhou, Y., Zhang, J., Liang, Q., Yang, C., Zheng, W., and Zhang, C., 2019. Association Between Dipsacus Saponin VI Level and Diversity of Endophytic Fungi in Roots of Dipsacus Asperoides. World Journal of Microbiology and Biotechnology, 35(3), 42.
Guerreiro, M.A., Brachmann, A., Begerow, D., and PerÅ¡oh, D., 2018. Transient Leaf Endophytes Are the Most Active Fungi In 1-year-old Beech Leaf Litter. Fungal Diversity, 89(1), 237–251.
Harikrishnan, M., Saipriya, P.P., Prakash, P., Jayabaskaran, C., and Bhat, S.G., 2021. Multi-functional Bioactive Secondary Metabolites Derived from Endophytic Fungi of Marine Algal Origin. Current Research in Microbial Sciences, 2, 100037.
Hasyyati, N. S., Suprihadi, A., Raharjo, B., and Dwiatmi, K., 2017. Isolasi dan Karakterisasi Kapang Endofit dari Pegagan (Centella asiatica (L.) URBAN). Jurnal Biologi, 6(2), 66–74.
Hayer, J., Salgado-Caxito, M., Opazo-Capurro, A., Muñoz, P. G., Millán, J., Piñeiro, A., Munita, J., Rivas, L., and Benavides, J., 2023. Multiple Clonal Transmissions of Clinically Relevant ESBL- Escherichia coli Between Livestock, Dogs, and Wildlife in Chile. Journal of Global Antimicrobial Resistance. 34, 247-252
Ibrahim, M., Oyebanji, E., Fowora, M., Aiyeolemi, A., Orabuchi, C., Akinnawo, B., and Adekunle, A.A., 2021. Extracts of Endophytic Fungi from Leaves of Selected Nigerian Ethnomedicinal Plants Exhibited Antioxidant Activity. BMC Complementary Medicine and Therapies, 21(1), 98-105.
Imran, M., Das, K. R., and Naik, M.M., 2019. CO-selection Of Multi-antibiotic Resistance in Bacterial Pathogens in Metal and Microplastic Contaminated Environments: An Emerging Health Threat. Chemosphere, 215, 846–857.
Jin, J., Zhang, H., Zhang, J., Liu, P., Chen, X., Li, Z., Xu, Y., Lu, P., and Cao, P., 2017. Integrated Transcriptomics and Metabolomics Analysis to Characterize Cold Stress Responses in Nicotiana tabacum. BMC Genomics, 18(1), 496.
Kamat, S., Kumari, M., Sajna, K. V., Mohan, S., and Jayabaskaran, C., 2022. Marine Endophytes from The Indian Coasts: The Untapped Sources of Sustainable Anticancer Drug Discovery. Sustainable Chemistry and Pharmacy, 27, 100675.
Konarzewska, Z., Śliwińska-Wilczewska, S., Felpeto, A.B., Vasconcelos, V., and Latała, A., 2020. Assessment of the Allelochemical Activity and Biochemical Profile of Different Phenotypes of Picocyanobacteria from the Genus Synechococcus. Marine Drugs, 18(4), 179.
Kraemer, S.A., Ramachandran, A., and Perron, G.G., 2019. Antibiotic Pollution in the Environment: From Microbial Ecology to Public Policy. Microorganisms, 7(6), 180.
Larsson, D.G. J., and Flach, C.F., 2022. Antibiotic resistance in the environment. Nature Reviews Microbiology, 20(5), 257–269.
Li, Q., Zou, H., Wang, D., Zhao, L., Meng, M., Wang, Z., Wu, T., Wang, S., and Li, X., 2023. Tracking Spatio Temporal Distribution and Transmission of Antibiotic Resistance in Aquatic Environments by Using ESBL-Producing Escherichia coli as an Indicator. Journal of Environmental Management, 344, 118534.
Li, Z., Wen, W., Qin, M., He, Y., Xu, D., and Li, L., 2022. Biosynthetic Mechanisms of Secondary Metabolites Promoted by the Interaction Between Endophytes and Plant Hosts. Frontiers in Microbiology, 13.
Mancuso, G., Midiri, A., Gerace, E., and Biondo, C., 2021. Bacterial Antibiotic Resistance: The Most Critical Pathogens. Pathogens, 10(10), 1310.
Mathew, D.E., Vala, A.K., Dineshkumar, R., Niharika, J., Singh, R., Shinde, P.B., and Mantri, V.A., 2023. Performance Evaluation and Yield Optimization of L-glutaminase Free L-asparaginase from Seaweed-associated Bacteria. Bioresource Technology Reports, 23, 101534.
Melotto, M., Underwood, W., Koczan, J., Nomura, K., and He, S.Y., 2006. Plant Stomata Function in Innate Immunity against Bacterial Invasion. Cell, 126(5), 969–980.
Nalini, M. S., and Prakash, H.S., 2017. Diversity And Bioprospecting of Actinomycete Endophytes from The Medicinal Plants. Letters in Applied Microbiology, 64(4), 261–270.
Newman, D., and Cragg, G., 2014. Marine-Sourced Anti-Cancer and Cancer Pain Control Agents in Clinical and Late Preclinical Development. Marine Drugs, 12(1), 255–278.
Nurzakiah, N., Desniar, D., and Tarman, K., 2020. Aktivitas Antimikroba Kapang Endofit Dari Tumbuhan Pesisir Sarang Semut (Hydnophytum Formicarum) Hasil Kultivasi. Barakuda 45: Jurnal Ilmu Perikanan dan Kelautan, 2(1), 35–42.
Oktavia, Y., Andhikawati, A., Nurhayati, T., and Tarman, K., 2014. Characterization of Crude Cellulase of Seagrass Endophytic Fungus. Jurnal Ilmu dan Teknologi Kelautan Tropis, 6(1), 209–218.
Oukala, N., Aissat, K., and Pastor, V., 2021. Bacterial Endophytes: The Hidden Actor in Plant Immune Responses against Biotic Stress. Plants, 10(5), 1012.
Paterson, D.L., and Bonomo, R.A., 2005. Extended-Spectrum β-Lactamases: a Clinical Update. Clinical Microbiology Reviews, 18(4), 657–686.
Peñuelas, J., and Terradas, J., 2014. The Foliar Microbiome. Trends in Plant Science, 19(5), 278–280.
Permatasari, A.A.A.P., Rosiana, I.W., Wiradana, P. A., Lestari, M. D., Widiastuti, N. K., Kurniawan, S. B., and Widhiantara, I. G., 2022. Extraction and Characterization of Sodium Alginate from Three Brown Algae Collected from Sanur Coastal Waters, Bali as Biopolymer Agent. Biodiversitas Journal of Biological Diversity, 23(3), 1655–1663.
Poole, K., 2017. At the Nexus of Antibiotics and Metals: The Impact of Cu and Zn on Antibiotic Activity and Resistance. Trends in Microbiology, 25(10), 820–832.
Poveda, J., 2021. Beneficial Effects of Microbial Volatile Organic Compounds (MVOCS) in Plants. Applied Soil Ecology, 168, 104118.
Prastiyanto, M. E., Kartika, A. I., Darmawati, S., and Radjasa, O. K., 2022. Bioprospecting of Bacterial Symbionts of Sponge Spongia Officinalis from Savu Sea, Indonesia for Antibacterial Potential Against Multidrug-resistant Bacteria. Biodiversitas Journal of Biological Diversity, 23(2),1-5
Rana, K. L., Kour, D., Kaur, T., Devi, R., Yadav, A.N., Yadav, N., Dhaliwal, H.S., and Saxena, A.K., 2020. Endophytic Microbes: Biodiversity, Plant Growth-promoting Mechanisms and Potential Applications for Agricultural Sustainability. Antonie van Leeuwenhoek, 113(8), 1075–1107.
Rawson, T. M., Wilson, R. C., O'Hare, D., Herrero, P., Kambugu, A., Lamorde, M., Ellington, M., Georgiou, P., Cass, A., Hope, W. W., and Holmes, A. H., 2021. Optimizing antimicrobial use: challenges, advances and opportunities. Nature Reviews Microbiology, 19 (12), 747–758.
Rinschen, M.M., Ivanisevic, J., Giera, M., and Siuzdak, G., 2019. Identification of Bioactive Metabolites Using Activity Metabolomics. Nature Reviews Molecular Cell Biology, 20(6), 353–367.
Rosiana, I.W., Wiradana, P.A., Permatasari, A.A.A.P., Pelupessy, Y.A.E.G., Dame, M.V.O., Soegianto, A., Yulianto, B., and Widhiantara, I. G., 2022. Concentrations of Heavy Metals in Three Brown Seaweed (Phaeophyta: Phaeophyceae) Collected from Tourism Area in Sanur Beach, Coast of Denpasar, Bali and Public Health Risk Assessment. Jurnal Ilmiah Perikanan Dan Kelautan, 14(2), 327–339.
Rossolini, G.M., D'Andrea, M.M., and Mugnaioli, C., 2008. The spread of CTX-M-type extended-spectrum β-lactamases. Clinical Microbiology and Infection, 14, 33–41.
Sahara, R., Setyaningsih, I., and Tarman, K., 2013. Kapang Endofit dari Tumbuhan Pesisir Sarang Semut (Hydnophytum Formicarum) dan Potensinya Sebagai Antihiperglikemik. [Thesis]. IPB University.
Silva, D. .D., Cardoso, M.S., and Macedo, A.J., 2022. Endophytic Fungi as a Source of Antibacterial Compounds-A Focus on Gram-Negative Bacteria. Antibiotics, 11(11), 1509.
Thi Minh Le, T., Thi Hong Hoang, A., Thi Bich Le, T., Thi Bich Vo, T., Van Quyen, D., and Hoang Chu, H., 2019. Isolation of Endophytic Fungi and Screening of Huperzine A–producing Fungus from Huperzia Serrata in Vietnam. Scientific Reports, 9(1), 16152.
Trivedi, P., Leach, J. E., Tringe, S. G., Sa, T., and Singh, B. K., 2020. Plant–microbiome Interactions: From Community Assembly to Plant Health. Nature Reviews Microbiology, 18(11), 607–621.
Verma, H., Kumar, D., Kumar, V., Kumari, M., Singh, S. K., Sharma, V. K., Droby, S., Santoyo, G., White, J. F., and Kumar, A., 2021. The Potential Application of Endophytes in Management of Stress from Drought and Salinity in Crop Plants. Microorganisms, 9(8), 1729.
von Wintersdorff, C. J. H., Penders, J., van Niekerk, J. M., Mills, N. D., Majumder, S., van Alphen, L. B., Savelkoul, P. H. M., and Wolffs, P. F. G., 2016. Dissemination of Antimicrobial Resistance in Microbial Ecosystems through Horizontal Gene Transfer. Frontiers in Microbiology, 7, 1-10.
Wasilah, Q.A., Mawli, R. E., Sani, M.D., Soegianto, A., Wiradana, P.A., and Pradisty, N.A., 2021. Determination of Lead and Cadmium in Edible Wedge Clam (Donax faba) Collected from North and South Coasts of Sumenep, East Java, Indonesia. Pollution Research, 40(2), 593–597.
White, J.F., Kingsley, K.L., Zhang, Q., Verma, R., Obi, N., Dvinskikh, S., Elmore, M.T., Verma, S.K., Gond, S.K., and Kowalski, K.P., 2019. Review: Endophytic Microbes and Their Potential Applications in Crop Management. Pest Management Science, 75(10), 2558–2565.
Widhiantara, I. G., Putri Permatasari, A. A. A., Rosiana, I. W., Sari, N. K. Y., Sudyadnyana, I. M. G. S., Wiradana, P. A., and Jawi, I. M., 2022. The Role of Biopolymers as Candidates for Promoting Health Agents: A Review. Journal of Applied Pharmaceutical Science, 13(1), 42–055.
Xie, W., Hao, Z., Yu, M., Wu, Z., Zhao, A., Li, J., Zhang, X., and Chen, B., 2019. Improved Phosphorus Nutrition by Arbuscular Mycorrhizal Symbiosis as A Key Factor Facilitating Glycyrrhizin and Liquiritin Accumulation in Glycyrrhiza uralensis. Plant and Soil, 439(1–2), 243–257.
Zhao, Y.-N., He, S.-H., Nakasone, K. K., Wasantha Kumara, K. L., Chen, C.-C., Liu, S.-L., Ma, H.-X., and Huang, M.-R., 2021. Global Phylogeny and Taxonomy of the Wood-Decaying Fungal Genus Phlebiopsis (Polyporales, Basidiomycota). Frontiers in Microbiology, 12, 1-20.
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