Diversity and antibacterial activity of endophytic fungi isolated from the medicinal plant of Syzygium jambos

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KURRATUL ‘AINI
ELFITA
HARY WIDJAJANTI
ARUM SETIAWAN

Abstract

Abstract. Aini K, Elfita, Widjajanti H, Setiawan A. 2022. Diversity and antibacterial activity of endophytic fungi isolated from the medicinal plant of Syzygium jambos. Biodiversitas 23: 2981-2989. Currently, antimicrobial resistance is one of the most important threats to global public health. This is due to the various mechanisms of antimicrobial resistance. Thus, the need for new sources of bioactive compounds outside conventional antibiotics is a top priority. This investigation evaluated the diversity and antibacterial activities of endophytic fungi isolated from the leaves and root bark of jambu mawar (Syzygium jambos (L.) Alston). The endophytic fungi were grown on PDA media, and their antibacterial activities were tested using the Kirby-Bauer method on two Gram-positive and two Gram-negative bacteria. A total of 10 (SJD1-SJD10) and 11 isolates (SJA1-SJA11) of endophytic fungi were identified from the leaves and root bark of S. jambos, respectively. Among them, SJA8 isolate exhibited strong antibacterial activity. Based on morphological characterization and phylogenetic tree analysis, SJA8 was identified as Pleiocarpon livistonae. Isolation and identification of pure compounds from the fungi may reveal potential candidates for new antibiotic substances.

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References
Aiello D, Gusella G, Vitale A, Guarnaccia V, Polizzi G. 2020. Cylindrocladiella peruviana and Pleiocarpon algeriense Causing Stem and Crown Rot on Avocado (Persea americana). European Journal of Plant Pathology, 158(2): 419–430. https://doi.org/10.1007/s10658-020-02082-x
Aiello D, Polizzi G, Crous PW, Lombard L. 2017. Pleiocarpon gen. nov. and a new species of Ilyonectria causing basal rot of Strelitzia reginae in Italy. IMA Fungus, 8(1): 65–76. https://doi.org/10.5598/imafungus.2017.08.01.05
Aini K, Elfita, Widjajanti H, Setiawan A, Kurniawati AR. 2022. Antibacterial activity of endophytic fungi isolated from the stem bark of jambu mawar (Syzygium jambos). Biodiversitas, 23(1), 521–532. https://doi.org/10.13057/biodiv/d230156
Al-Nasrawi HG, Hughes AR. 2012. Fungal Diversity Associated With Salt Marsh Plants Spartina alterniflora And Juncus roemerianus In Florida. Jordan Journal of Biological Sciences, 5(4), 247–254.
Aminin ALN, Cahyanti N, Sari A, Mulyani NS, Cahyono, B. 2020. Antioxidant and Antimicrobial Screening of Endophytic Fungi Culture Filtrate from Purwoceng (Pimpinella alpina Molk) Leaf. Jurnal Kimia Sains dan Aplikasi, 23(9), 319–324. https://doi.org/10.14710/jksa.23.9.319-324
Ammad F, Benchabane M, Toumi M. 2014. Diversity of Fungal Trunk Pathogens Associated with Grapevine Dieback of Grapevine in Algeria. Jordan Journal of Biological Sciences, 7(1), 35–39. https://doi.org/10.12816/0008211
Astuti P, Pratoko DK, Rollando R, Nugroho GW, Wahyuono S, Hertiani T, Nurrochmad A. 2021. Bioactivities of A Major Compound from Arthrinium rasikravindrae An Endophytic Fungus of Coleus amboinicus Lour. Fabad Journal of Pharmaceutical Sciences, 46(1), 23–30.
Bhavana NS, Prakash HS, Nalini MS. 2020. Fungal Endophytes from Tabernaemontana heyneana Wall. (Apocynaceae), their Molecular Characterization, L-asparaginase and Antioxidant Activities. Jordan Journal of Biological Sciences, 13(4), 543–550.
Bugg TDH, Braddick D, Dowson CG, Roper DI. 2011. Bacterial cell wall assembly: Still an attractive antibacterial target. Trends in Biotechnology, 29(4), 167–173. https://doi.org/10.1016/j.tibtech.2010.12.006
Cai J, Zhou XM, Yang X, Tang MM, Liao QY, Meng BZ, Liao S, Chen GY. 2020. Three new bioactive natural products from the fungus Talaromyces assiutensis JTY2. Bioorganic Chemistry, 94, 1–22. https://doi.org/10.1016/j.bioorg.2019.103362
Caicedo NH, Davalos AF, Puente PA, Rodriguez AY, Caicedo PA. 2019. Antioxidant Activity of Exo?Metabolites Produced by Fusarium oxysporum: An Endophytic Fungus Isolated from Leaves of Otoba gracilipes. Microbiology Open, 8(10), 1–7. https://doi.org/10.1002/mbo3.903
Cao Y, Zhang Z, Lin F, Lai D, Yao Y, Xie B, Zhou L. 2019. Secondary Metabolites of Endophytic Fungus Acremonium implicatum and Their Biological Activities. Natural Product Reports, 28, 182–187.
Cock IE, Cheesman M. 2014. Plants of The Genus Syzygium (Myrtaceae): A Review on Ethnobotany, Medicinal Properties and Phytochemistry. In Bioactive Compounds of Medicinal Plants (pp. 35–84)
Collado IG, Viaud M. 2016. Secondary Metabolism in Botrytis cinerea?: Combining Genomic and Metabolomic Approaches. In Botrytis - The Fungus, the Pathogen and its Management in Agricultural Systems (bll 291–313). https://doi.org/10.1007/978-3-319-23371-0
Deka D, Jha DK. 2018. Antimicrobial Activity of Endophytic Fungi from Leaves and Barks of Litsea cubeba Pers., a Traditionally Important Medicinal Plant of North East India. Jordan Journal of Biological Sciences, 11(1), 73–79.
Devi R, Kaur T, Guleria G, Rana KL, Kour D, Yadav N, Yadav AN, Saxena AK. 2020. Fungal secondary metabolites and their biotechnological applications for human health. In New and Future Developments in Microbial Biotechnology and Bioengineering (bll 147–161). Elsevier Inc. https://doi.org/10.1016/b978-0-12-820528-0.00010-7
Díaz-Rojas M, Raja H, González-Andrade M, Rivera-Chávez J, Rangel-Grimaldo M, Rivero-Cruz I, Mata R. 2021. Protein tyrosine phosphatase 1B inhibitors from the fungus Malbranchea albolutea. Phytochemistry, 184, 1–12. https://doi.org/10.1016/j.phytochem.2021.112664
El Aamri L, Hafidi M, Scordino F, Krasowska A, Lebrihi A, Orlando MG, Barresi C, Criseo G, Barreca D, Romeo O. 2020. Arthrographis curvata and Rhodosporidium babjevae as New Potential Fungal Lipase Producers for Biotechnological Applications. Brazilian Archives of Biology and Technology, 63, 1–9. https://doi.org/10.1590/1678-4324-2020180444
Elfita, Mardiyanto, Fitrya, Larasati JE, Julinar, Widjajanti H, Muharni. 2019. Antibacterial Activity of Cordyline Fruticosa Leaf Extracts and Its Endophytic Fungi Extracts. Biodiversitas, 20(12), 3804–3812. https://doi.org/10.13057/biodiv/d201245
Felsenstein J. 1985. Confidence Limits on Phylogenies: An Approach Using the Bootstrap. Evolution, 39(4), 783–791.
Granato MQ, Mello TP, Nascimento RS, Pereira MD, Rosa TLSA, Pessolani MCV, McCann M, Devereux M, Branquinha MH, Santos ALS, Kneipp LF. 2021. Silver(I) and Copper(II) Complexes of 1,10-Phenanthroline-5,6-Dione Against Phialophora verrucosa: A Focus on the Interaction With Human Macrophages and Galleria mellonella Larvae. Frontiers in Microbiology, 12(April), 1–12. https://doi.org/10.3389/fmicb.2021.641258
Hameed A, Hussain SA, Yang J, Ijaz MU, Liu Q, Suleria HAR, Song Y. 2017. Antioxidants Potential of the Filamentous Fungi (Mucor circinelloides). Nutrients, 9(10), 1–20. https://doi.org/10.3390/nu9101101
Handayani D, Rivai H, Hutabarat M, Rasyid R. 2017. Antibacterial Activity of Endophytic Fungi Isolated from Mangrove Plant Sonneratia griffithii Kurz. Journal of Applied Pharmaceutical Science, 7(4), 209–212. https://doi.org/10.7324/JAPS.2017.70431
Hartanti D, Supriyanto J, Sugijanto NEN. 2016. Antimicrobial Activity of Fractions of Ethyl Acetate Extract of Cladosporium oxysporum, An Endophytic Fungus Derived from Alyxia reinwardtii. Jurnal Kefarmasian Indonesia, 6(1), 1–7. https://doi.org/10.22435/jki.v6i1.5413.1-7
Hernandez-Restrepo M, Giraldo A, van Doorn R, Wingfield MJ, Groenewald JZ, Barreto RW, Colman AA, Mansur PSC, Crous PW. 2020. The Genera od Fungi-G6: Arthrographis, Kramasamuha, Melnikomyces, Thysanorea, and Verruconis. Fungal Systematics and Evolution, 6(Desember), 1–24.
Idris A, Al-tahir I, Idris E. 2013. Antibacterial activity of endophytic fungi extracts from the medicinal plant Kigelia africana. Egyptian Academic Journal of Biological Sciences, G. Microbiology, 5(1), 1–9. https://doi.org/10.21608/eajbsg.2013.16639
Ilyas M, Praptiwi, Wulansari D, Fathoni A, Agusta A. 2019. An assemblages of fungal endophytes isolated from medicinal plants collected from Toba and Samosir, North Sumatra. IOP Conference Series: Earth and Environmental Science, 308(1), 1–10. https://doi.org/10.1088/1755-1315/308/1/012070
Khan MS, Gao J, Munir I, Zhang M, Liu Y, Moe TS, Xue J, Zhang X. 2021. Characterization of Endophytic Fungi, Acremonium sp., from Lilium davidii and Analysis of Its Antifungal and Plant Growth-Promoting Effects. BioMed Research International, 2021, 1–14. https://doi.org/10.1155/2021/9930210
Kohanski MA, Dwyer DJ, Collins JJ. 2010. How antibiotics kill bacteria: From targets to networks. Nature Reviews Microbiology, 8(6), 423–435. https://doi.org/10.1038/nrmicro2333
Lan D, Wu B. 2020. Chemistry and Bioactivities of Secondary Metabolites from the Genus Talaromyces. Chemistry and Biodiversity, 17(8), 1–41. https://doi.org/10.1002/cbdv.202000229
Lutfia A, Munir E, Yurnaliza,Y. 2020. Molecular identification of endophytic fungi from torch ginger (Etlingera elatior) antagonist to phytopathogenic fungi. Biodiversitas, 21(6), 2681–2689. https://doi.org/10.13057/biodiv/d210641
Martins T, Schinke C, Queiroz SCN, de C Braga PA, Silva FSP, Melo IS, Reyes FGR. 2021. Role of Bioactive Metabolites from Acremonium camptosporum Associated with The Marine Sponge Aplysina fulva. Chemosphere, 274, 1–11. https://doi.org/10.1016/j.chemosphere.2021.129753
Mbekou MIK, Dize D, Yimgang VL, Djague F, Toghueo RMK, Sewald N, Lenta BN, Boyom FF. 2021. Antibacterial and Mode of Action of Extracts from Endophytic Fungi Derived from Terminalia mantaly, Terminalia catappa, and Cananga odorata. BioMed Research International, 2021(Pcv 13), 1–13. https://doi.org/10.1155/2021/6697973
Meena H, Hnamte S, Siddhardha B. 2019. Secondary Metabolites from Endophytic Fungi: Chemical Diversity and Application. In Advances in Endophytic Fungal Research, Fungal Biology (bll 145–169). https://doi.org/10.1007/978-3-030-03589-1
Miklasi?ska-Majdanik M, K?pa M, Wojtyczka RD, Idzik D, W?sik TJ. 2018. Phenolic Compounds Diminish Antibiotic Resistance of Staphylococcus aureus Clinical Strains. International Journal of Environmental Research and Public Health, 15(10), 1–18. https://doi.org/10.3390/ijerph15102321
Nagarajan D. 2019. In Vitro Antioxidant Potential of Endophytic Fungi Isolated from Enicostemma axillare (Lam.) Raynal. and Ormocarpum cochinchinense (Lour.) Merr. Journal of Pharmacognosy and Phytochemistry, 8(1), 1356–1363.
Nalli Y, Mirza DN, Wani ZA, Wadhwa B, Mallik FA, Raina C, Chaubey A, Riyaz-Ul-Hassan S, Ali A. 2015. Phialomustin A-D, New Antimicrobial and Cytotoxic Metabolites From An Endophytic Fungus, Phialophora mustea. RSC Advances, 5, 95307–95312. https://doi.org/10.1039/c5ra18121f
Nei M, Kumar S. 2000. Molecular Evolution and Phylogenetics. Oxford University Press, Inc. https://doi.org/10.1002/wilm.10463
Newton BA. 1965. Mechanisms of Antibiotic Action. Annual Review of Microbiology, 19, 209–240. https://doi.org/10.1146/annurev.mi.19.100165.001233
Nicoletti R, Trincone A. 2016. Bioactive Compounds Produced by Strains of Penicillium and Talaromyces of Marine Origin. In Marine Drugs (Vol 14, Number 2). https://doi.org/10.3390/md14020037
Nurhaida, Yenn TW, Ibrahim D. 2019. Endophytic fungi from Syzygium cumini (L.) Skeels leaves and its potential as antimicrobial agents. IOP Conference Series: Earth and Environmental Science, 364(1). https://doi.org/10.1088/1755-1315/364/1/012023
Octarya Z, Novianty R, Suraya N, Saryono. 2021. Antimicrobial activity and GC-MS analysis of bioactive constituents of Aspergillus fumigatus 269 isolated from Sungai Pinang hot spring, Riau, Indonesia. Biodiversitas, 22(4), 1839–1845. https://doi.org/10.13057/biodiv/d220429
Palanisamy M, Venkatapathy N, Rajendran V, Shobana CS. 2015. Keratomycosis Caused By Graphium eumorphum (Graphium State of Scedosporium apiospermum). Journal of Clinical and Diagnostic Research, 9(4), DD03–DD04. https://doi.org/10.7860/JCDR/2015/12089.5802
Praptiwi P, Palupi KD, Fathoni A, Wulansari D, Ilyas M, Agusta A. 2016. Evaluation of antibacterial and antioxidant activity of extracts of endophytic fungi isolated from Indonesian Zingiberaceous plants. Nusantara Bioscience, 8(2), 306–311. https://doi.org/10.13057/nusbiosci/n080228
Rajamanikyam M, Vadlapudi V. 2017. Endophytic Fungi Therapeutics as Novel Resources of natural. Brazilian Archives of Biology and Technology, 60(December), 1–26.
Ramirez CSP, Notarte KIR, Dela Cruz TEE. 2020. Antibacterial Activities of Mangrove Leaf Endophytic Fungi From Luzon Island, Philippines. Studies in Fungi, 5(1), 320–331. https://doi.org/10.5943/sif/5/1/14
Rana KL, Kour D, Sheikh I, Yadav N, Yadav AN, Kumar V, Singh BP, Dhaliwal HS, Saxena AK. 2019. Biodiversity of Endophytic Fungi from Diverse Niches and Their Biotechnological Applications. In Advances in Endophytic Fungal Research, Fungal Biology (bll 105–144). https://doi.org/10.1007/978-3-030-03589-1_6
Rebollar-Ramos D, Ovalle-Magallanes B, Palacios-Espinosa JF, Macías-Rubalcava ML, Raja HA, González-Andrade M, Mata R. 2021. ??Glucosidase and PTP-1B Inhibitors from Malbranchea. ACS Omega, 6(35), 22969–22981.
Roux J, Nkuekam GK, Marincowitz S, van der Merwe NA, Uchida J, Wingfield MJ, Chen SF. 2020. Cryphonectriaceae Associated with Rust-Infected Syzygium Jambos in Hawaii. MycoKeys, 76, 49–79. https://doi.org/10.3897/MYCOKEYS.76.58406
Russo CADM, Selvatti AP. 2018. Bootstrap and Rogue Identification Tests for Phylogenetic Analyses. Molecular Biology and Evolution, 35(9), 2327–2333. https://doi.org/10.1093/molbev/msy118
Sainaghi PP, Rossati A, Buccheri C, Bargiacchi O, Garavelli PL, Andreoni, S. 2015. Arthrographis kalrae Arthritis: A New Case Report. Infezioni in Medicina, 23(2), 192–194.
Saitou N, Nei M. 1987. The Neighbor-joining Method: A New Method for Reconstructing Phylogenetic Trees. Molecular biology and evolution, 4(4), 406–425. https://doi.org/10.1093/oxfordjournals.molbev.a040454
Samal N, Narasimham MV, Sahu SK, Padhi S. 2021. First case of Arthrographis kalrae Pulmonary Infection in A Patient with AIDS. Microbiologia Medica, 36(1), 1–4. https://doi.org/10.4081/mm.2021.9684
Shaala LA, Youssef DTA. 2015. Identification and Bioactivity of Compounds from the Fungus Penicillium sp. CYE-87 Isolated from a Marine Tunicate. Marine Drugs, 13(4), 1698–1709. https://doi.org/10.3390/md13041698
Singha IM, Kakoty Y, Unni BG, Das J, Kalita MC. 2016. Identification and Characterization of Fusarium sp. Using ITS and RAPD causing Fusarium Wilt of Tomato Isolated from Assam, North East India. Journal of Genetic Engineering and Biotechnology, 14(1), 99–105. https://doi.org/10.1016/j.jgeb.2016.07.001
Slama HB, Bouket AC, Alenezi FN, Pourhassan Z, Goli?ska P, Oszako T, Belbahri L. 2021. Potentials of Endophytic Fungi in the Biosynthesis of Versatile Secondary Metabolites and Enzymes. Forests, 12(12), 1–13. https://doi.org/10.3390/f12121784
Son YM, Kang HK, Na SY, Lee HY, Baek JO, Lee JR, Roh JY, Seo YH. 2010. Chromoblastomycosis Caused By Phidophora richardsiae. Annals of Dermatology, 22(3), 362–366. https://doi.org/10.5021/ad.2010.22.3.362
Sugijanto NE, Dorra BL. 2016. Antimicrobial Activity of Cladosporium oxysporum Endophytic Fungus Extract Isolated From Aglaia odorata Lour. Indonesian Journal of Medicine, 01(02), 108–115. https://doi.org/10.26911/theijmed.2016.01.02.04
Tamura K, Stecher, Kumar S. 2021. MEGA11: Molecular Evolutionary Genetics Analysis Version 11. Molecular Biology and Evolution, 38(7), 3022–3027. https://doi.org/10.1093/molbev/msab120
Tenover FC. 2019. Antimicrobial Susceptibility Testing. Encyclopedia of Microbiology, October 2014, 166–175. https://doi.org/10.1016/B978-0-12-801238-3.02486-7
Ullah H, Ali S. 2017. Classification of Anti?Bacterial Agents and Their Functions. In Antibacterial Agents. InTech. https://doi.org/10.5772/intechopen.68695
Walsh TH, Hayden RT, Larone DH. 2018. Larone’s Medically Important Fungi: A Guide to Idetification (6th Editio). ASM Press, Washington, DC. https://doi.org/10.1128/9781555819880 Printed
Watanabe T. 2010. Pictorial Atlas of Soil and Seed Fungi: Morfologies of Cultural Fungi and Key to Species. In Pictorial Atlas of Soil and Seed Fungi (Third Edit). CRC Press: Taylor & Francis Group. https://doi.org/10.1201/ebk1439804193
Wu CL, Chao CM, Lin WT. 2018. Traumatic Wound Infection with Graphium. The Ulutas Medical Journal, 4(1), 44–46. https://doi.org/10.5455/umj.20181126062738
Xi L, Fukushima K, Lu C, Takizawa K, Liao R, Nishimura K. 2004. First case of Arthrographis kalrae Ethmoid sinusitis and ophthalmitis in the People’s Republic of China. Journal of Clinical Microbiology, 42(10), 4828–4831. https://doi.org/10.1128/JCM.42.10.4828-4831.2004
Yan L, Zhao H, Zhao X, Xu X, Di Y, Jiang C, Shi J, Shao D, Huang Q, Yang H, Jin M. 2018. Production of bioproducts by endophytic fungi: chemical ecology, biotechnological applications, bottlenecks, and solutions. Applied Microbiology and Biotechnology, 102(15), 6279–6298. https://doi.org/10.1007/s00253-018-9101-7
Yasser MM, Marzouk MA, El-Shafey NM, Shaban SA. 2020. Diversity and Antimicrobial Activity of Endophytic Fungi from the Medicinal Plant Pelargonium graveolens (geranium) in Middle Egypt. Jordan Journal of Biological Sciences, 13(2), 197–205.
Yodsing N, Lekphrom R, Sangsopha W, Aimi T, Boonlue S. 2018. Secondary Metabolites and Their Biological Activity from Aspergillus aculeatus KKU-CT2. Current Microbiology, 75(5), 513–518. https://doi.org/10.1007/s00284-017-1411-y
Youssef FS, Alshammari E, Ashour ML. 2021. Bioactive Alkaloids from Genus Aspergillus: Mechanistic Interpretation of Their Antimicrobial and Potential SARS-CoV-2 Inhibitory Activity Using Molecular Modelling. International Journal of Molecular Sciences, 22(4), 1–23. https://doi.org/10.3390/ijms22041866
Zhai, MM, Li J, Jiang CX, Shi YP, Di DL, Crews P, Wu QX. 2016. The Bioactive Secondary Metabolites from Talaromyces species. Natural Products and Bioprospecting, 6(1), 1–24. https://doi.org/10.1007/s13659-015-0081-3
Zheng R, Li S, Zhang X, Zhao C. 2021. Biological Activities of Some New Secondary Metabolites Isolated from Endophytic Fungi: A Review Study. International Journal of Molecular Sciences, 22(959), 1–80. https://doi.org/10.3390/ijms22020959