Bioactivity Endophytic Fungi Isolated from the Leaf Stalk of Syzygium jambos L. Alston http://www.doi.org/10.26538/tjnpr/v6i11.4
Main Article Content
Abstract
Antibiotic resistance and free radicals are a problem to be overcome by using antibiotics and antioxidants from natural ingredients. This study aimed to investigate the antibacterial and antioxidant activity of endophytic fungi (EF) isolated from the leaf stalks of jambu mawar (Syzygium jambos (L.) Alston). EF isolated from the leaf stalk of S. jambos was identified microscopically (shape of hyphae and spores) and macroscopically (growth patterns, colony color, texture, margin, and other characteristics). Antibacterial activity was tested on Salmonella typhi, Escherichia coli, Staphylococcus aureus, and Bacillus subtilis bacteria using the Kirby Bauer method. Antioxidant test using 2,2-diphenyl-1-picrylhydrazyl (DPPH) method. The molecular identified of EF with high antioxidant and antibacterial activity to determine the species and continued with the isolation of pure compounds. Identification of pure compounds was carried out by spectroscopic methods including 1D NMR (¹H-NMR and C-NMR). The results of the isolation of EF from the leaf stalk of S. jambos found four isolates, namely SJS1- SJS4. The results of the antibacterial test represented that the EF isolate SJS1 had strong activity against S. aureus and B. subtilis bacteria. The antioxidant activity test showed IC50 value of 29.29 g/mL. Molecular identification results showed that SJS1 was identified as Lasiodiplodia theobromae. Spectroscopic results of the pure compound identified as 3,5-dihydroxy-4-(4-
hydroxyphenyl)tetrahydro-2H-pyran-2-one. The endophytic fungus Lasiodiplodia theobromae was isolated from the leaf stalk of S. jambos (L.) Alston has the potential as a source of antioxidants and antibacterial bioactive compounds that can be developed through further research, including in vitro and in vivo tests.
Article Details
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
References
Toghueo RMK. Bioprospecting endophytic fungi from Fusarium genus as sources of bioactive metabolites. Mycology. 2020;11(1):1–21.
Du W, Yao Z, Li J, Sun C, Xia J, Wang B, Shi D, Ren L. Diversity and Antimicrobial Activity of Endophytic Fungi Isolated from Securinega suffruticosa in the Yellow River Delta. PLoS One. 2020; 15(3):1–18.
An C, Ma S, Shi X, Xue W, Liu C, Ding H. Diversity and Antimicrobial Activity of Endophytic Fungi Isolated from Chloranthus japonicus Sieb in Qinling Mountains, China. Int J Mol Sci. 2020; 21(17):1–15.
Aini K, Elfita, Widjajanti H, Setiawan A, Kurniawati AR. Antibacterial activity of endophytic fungi isolated from the stem bark of jambu mawar (Syzygium jambos). Biodiversitas. 2022; 23(1):521–532.
Manganyi MC and Ateba CN. Untapped Potentials of Endophytic Fungi: A Review of Novel Bioactive Compounds with Biological Applications. Microorgan. 2020; 8(12):1–25.
Atta EM, Mohamed NH, Abdelgawad AAM. Antioxidants: an Overview on the Natural and Synthetic Types. Eur Chem Bull. 2017; 6(8):365–375.
Mhamdi A and Van Breusegem F. Reactive oxygen species in plant development. Dev. 2018; 145(15):1–12.
Das K and Roychoudhury A. Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Front Environ Sci. 2014; 2(DEC):1–13.
Ibrahim M, Oyebanji E, Fowora M, Aiyeolemi A, Orabuchi C, Akinnawo B, Adekunle AA. Extracts of endophytic fungi from leaves of selected Nigerian ethnomedicinal plants exhibited antioxidant activity. BMC Complement Med Ther. 2021; 21(1):1– 13.
Hidayat A, Turjaman M, Faulina SA, Ridwan F, Aryanto, Najmulah, Irawadi, TT, Iswanto AH. Antioxidant and Antifungal Activity of Endophytic Fungi Associated with Agarwood Trees. J Korean Wood Sci Technol. 2019; 47(4):459–471.
Caicedo NH, Davalos AF, Puente PA, Rodriguez AY, Caicedo PA. Antioxidant Activity of Exo‐Metabolites Produced by Fusarium oxysporum: An Endophytic Fungus Isolated from Leaves of Otoba gracilipes. Microbiol Open. 2019;8(10):1–7.
Lim TK. Syzygium jambos. In: Edible Medicinal And Non Medicinal Plants. Springer Netherlands; 2012; 760–766.
Wamba BEN, Nayim P, Mbaveng AT, Voukeng IK, Dzotam JK,Ngalani OJT, Kuete V . Syzygium jambos Displayed Antibacterial and Antibiotic-Modulating Activities against Resistant Phenotypes. Evidence-based Complement Altern Med. 2018;2018. doi:10.1155/2018/5124735
Fathima SBN, Pandian R, Perumal PV. Antimicrobial Activity of Methanol and Ethyl Acetate Extracts of Three Medicinal Plants. Int J Adv Sci Eng Technol. 2017; 5(1):16–22.
Jayasinghe ULB, Ratnayake RMS, Medawala MMWS, Fujimoto Y. Dihydrochalcones with Radical Scavenging Properties from the Leaves of Syzygium jambos. Nat Prod Res. 2007; 21(6):551–554.
Hossain H, Rahman SE, Akbar PN, Khan TA, Rahman MM, Jahan IA. HPLC Profiling, Antioxidant and In Vivo Anti-Inflammatory Activity of The Ethanol Extract of Syzygium jambos Available in Bangladesh. 2016; 1–8.
Devakumar J and Sudha SS. In vitro Phytochemical , Antioxidant and Cytotoxic Evaluation of Syzygium jambos L . (Alston). J Pharm Res. 2017; 11(3):235–238.
Selvam NT, Venkatakrishnan V, Kumar SD. Tissue Level Antioxidant Activity of Leaf Extract of Syzygium jambos Linn . In Paracetamol Intoxicated Wistar rats. J Intern Med. 2014; 2(8):107– 111.
Reynertson KA, Kennelly EJ, Basile MJ. Antioxidant Potential of Seven Myrtaceous Fruits. 2005; 25–35.
Borah SN, Goswami D, Sarma HK, Cameotra SS, Deka S. Rhamnolipid Biosurfactant against Fusarium verticillioides to Control Stalk and Ear Rot Disease of Maize. Front Microbiol. 2016; 7:1–10.
Sen A and Imlay JA. How Microbes Defend Themselves From Incoming Hydrogen Peroxide. Front Immunol. 2021; 12(April):1– 19.
Nakai K and Tsuruta D. What are reactive oxygen species, free radicals, and oxidative stress in skin diseases? Int J Mol Sci. 2021; 22(19):1–16.
Wilson D. Endophyte: The Evolution of a Term, and Clarificationof Its Use and Definition. Oikos. 1995;73(2):274.
Selim KA, El-Beih AA, Abdel-Rahman TM, El-Diwany AI. Biology of Endophytic Fungi. Curr Res Environ Appl Mycol. 2012; 2(1):31–82.
Elfita, Munawar, Muharni, Sudrajat MA. Identification of New Lactone Derivatives Isolated from Trichoderma sp., An Endophytic
Fungus of Brotowali (Tinaspora crispa). HAYATI J Biosci. 2014; 21(1):15–20.
Gakuubi MM, Munusamy M, Liang ZX, Ng SB. Fungal Endophytes: A Promising Frontier for Discovery of Novel Bioactive Compounds. J Fungi. 2021;7(10):1–24.
Adeleke BS and Babalola OO. Pharmacological Potential of Fungal Endophytes Associated with Medicinal Plants: A Review. J Fungi. 2021; 7(2):1–16.
Rajamanikyam M and Vadlapudi V. Endophytic Fungi as Novel Resources of natural Therapeutics. Brazilian Arch Biol Technol. 2017; 60:1–26.
Watanabe T. Pictorial Atlas of Soil and Seed Fungi: Morfologies of Cultural Fungi and Key to Species. Third Edit. New York: CRC Press: Taylor & Francis Group; 2010.
Walsh TH, Hayden RT, Larone DH. Larone’s Medically Important Fungi: A Guide to Idetification. 6th Edition. ASM Press, Washington, DC; 2018.
Nagarajan D. In Vitro Antioxidant Potential of Endophytic Fungi Isolated from Enicostemma axillare (Lam.) Raynal. and Ormocarpum cochinchinense (Lour.) Merr. J Pharmacogn Phytochem. 2019; 8(1):1356–1363.
Elfita, Mardiyanto, Fitrya, Larasati JE, Julinar, Widjajanti H, Muharni. Antibacterial Activity of Cordyline fruticosa Leaf Extracts and Its Endophytic Fungi Extracts. Biodiversitas. 2019; 20(12):3804–3812.
Habisukan UH, Elfita, Widjajanti H, Setiawan A, Kurniawati AR. Antioxidant and Antimicrobial Activity of Endophytyc Fungi Isolated from Syzygium aqueum Leaves. J Phys Conf Ser. 2021; 1751(1):1–8.
Singha IM, Kakoty Y, Unni BG, Das J, Kalita MC. Identification and Characterization of Fusarium sp. Using ITS and RAPD causing Fusarium Wilt of Tomato Isolated from Assam, North East India. J Genet Eng Biotechnol. 2016; 14(1):99–105.
Tamura K, Stecher G, Kumar S. MEGA11: Molecular Evolutionary Genetics Analysis Version 11. Mol Biol Evol. 2021; 38(7):3022– 3027.
Elfita E, Munawar M, Muharni M, Pratiwi G, Rahmadania R. A New Benzoyl Compound Isolated from the Endophytic Fungi of Kandis Gajah (Garcinia griffithii) and Asam Kandis (Garcinia cowa). Makara J Sci. 2016; 20(4):167–172.
Hapida Y, Elfita, Widjajanti H, Salni. Biodiversity and antibacterial activity of endophytic fungi isolated from jambu bol (Syzygium
malaccense). Biodiversitas. 2021;22(12):5668–5677.
Elfita S, Widjajanti H, Setiawan A, Kurniawati AR. Diversity of Endophytic Fungi from The Root Bark of Syzygium zeylanicum, and The Antibacterial Activity of Fungal Extracts, and Secondary Metabolite. Biodiversitas. 2021; 22(10):4572–4582.
Yadav M, Yadav A, Yadav JP. In vitro antioxidant activity and total phenolic content of endophytic fungi isolated from Eugenia jambolana Lam. Asian Pac J Trop Med. 2014; 7(S1):S256–S261.
Habisukan UH, Elfita E, Widjajanti H, Setiawan A. Secondary Metabolite and Antioxidant Activity of Endophytic Fungi Isolated from Syzygium aqueum Leaves Stalk. Biointerface Res Appl Chem. 2022; 12(6):7584–7595.
Jinu MV, Gini CK, Jayabaskaran C. In vitro antioxidant activity of cholestanol glucoside from an endophytic fungus Lasiodiplodia
theobromae isolated from Saraca asoca. J Chem Pharm Res. 2015;7(1):952–962.
Zhou J, Diao X, Wang T, Chen G, Lin Q, Yang X, Xu J. Phylogenetic diversity and antioxidant activities of culturable fungal endophytes associated with the mangrove species Rhizophora stylosa and R. mucronata in the South China Sea. PLoS One. 2018; 13(6):1–18.
Taufiq MMJ and Darah I. Anti-Mrsa of the Ethyl Acetate Crude Extract From Lasiodiplodia Pseudotheobromae Ibrl Os-64, an Endophytic Fungus Isolated From Leaf of Ocimum Sanctum Linn. Int J Pharm Pharm Sci. 2018; 10(8):50.
Setyaningsih R, Susilowati A, Prasetyani D. Antibacterial Activity of Endophytic Fungi in Pometia pinnata Against Staphylococcus aureus and Methicillin-Resistant Staphylococcus aureus. Biodiversitas. 2020;21(11):5408–5413.
Chen S, Chen D, Cai R, Cui H, Long Y, Lu Y, Li C, She Z. Cytotoxic and Antibacterial Preussomerins from the Mangrove Endophytic Fungus Lasiodiplodia theobromae ZJ-HQ1. J Nat Prod. 2016; 79(9):2397–2402.
Salvatore MM, Alves A, Andolfi A. Secondary metabolites of Lasiodiplodia theobromae: Distribution, chemical diversity, bioactivity, and implications of their occurrence. Toxins (Basel). 2020; 12(7):1–29.
Balbool BA, Abdel-azeem AM, Moubasher MH, Helmy EA. Production of L-Asparaginase (L-ASN) from endophytic Lasiodiplodia theobromae hosted Teucrium polium in Egypt. Microb Biosyst. 2018; 3(2):46–55.
Chen S, Liu Z, Liu H, Long Y, Chen D, Lu Y, She Z. Lasiodiplactone A, a novel lactone from the mangrove endophytic fungus Lasiodiplodia theobromae ZJ-HQ1. Org Biomol Chem. 2017; 15(30):6338–6341.
Eng F, Haroth S, Feussner K, Meldau D, Rekhter D, Ischebeck T, Brodhun F, Feussner I. Optimized Jasmonic Acid Production by Lasiodiplodia theobromae Reveals Formation of Valuable Plant Secondary Metabolites. PLoS One. 2016; 11(12):1–18.
Daghir GM, Tomah AA, Alyaseri II. First Record the Fungus Bipolaris australiensis as a Cause of Leaf Blight Date Palm in Misan and Attempt to Control It in In Vitro Condition. Plant Arch. 2020; 20(July):966–970.
Liu MT, He Y, Shen L, Hu ZX, Zhang YH. Bipolarins A–H, eight new ophiobolin-type sesterterpenes with antimicrobial activity from fungus Bipolaris sp. TJ403-B1. Chin J Nat Med. 2019; 17(12):935– 944.
Liu M, Zhang X, Shen L, Sun W, Lin S, Liu J, Cao F, Qi C, Wang J, Hu Z, Zhang Y. Bioactive Polyketide-Terpenoid Hybrids from a Soil-Derived Fungus Bipolaris zeicola. J Org Chem. 2021; 86(16):10962–10974.
Yu JJ, Jin YX, Huang SS, He J. Sesquiterpenoids and xanthones from the kiwifruit-associated fungus Bipolaris sp. And their antipathogenic microorganism activity. J Fungi. 2022; 8(9):1–17.
He J, Li ZH, Ai HL, Feng T, Liu JK. Anti-bacterial chromones from cultures of the endophytic fungus Bipolaris eleusines. Nat Prod Res. 2019; 33(24):3515–3520.
Maehara S, Yamane C, Kitamura C, Hinokuma M, Hata T. High ophiobolin A production in endophytic fungus Bipolaris sp. associated with Datura metel. Nat Prod Res. 2020;34(20):2990– 2992. doi:10.1080/14786419.2019.1597352
Di Francesco A, Zajc J, Gunde-Cimerman N, Aprea E, Gasperi F, Placi N, Caruso F, Baraldi E. Bioactivity of volatile organic compounds by Aureobasidium species against gray mold of tomato and table grape. World J Microbiol Biotechnol. 2020; 36(171):1– 11.
Botić T, Kralj-Kunčič M, Sepčić K, Batista U, Zalar P, Knez Z, Gunde-Cimerman N. Biological activities of organic extracts of four Aureobasidium pullulans varieties isolated from extreme marine and terrestrial habitats. Nat Prod Res. 2014; 28(12):874– 882.
Bozoudi D and Tsaltas D. The Multiple and Versatile Roles of Aureobasidium pullulans in the Vitivinicultural Sector. Fermentation. 2018; 4(85):1–15.
Li Y, Chi Z, Wang GY, Wang ZP, Liu GL, Lee CF, Ma ZC, Chi ZM. Taxonomy of Aureobasidium spp. and biosynthesis and regulation of their extracellular polymers. Crit Rev Microbiol. 2015; 41(2):1–10.
Choi HG, Kim JW, Choi H, Kang KS, Shim SH. New Hydroxydecanoic Acid Derivatives Produced by an Endophytic Yeast Aureobasidium pullulans AJF1 from Flowers of Aconitum carmichaeli. Molecules. 2019; 24(22):1–11.
Abdel-Lateff A, Elkhayat ES, Fouad MA, Okino T. Aureobasidin, New Antifouling Metabolite from Marine-Derived Fungus Aureobasidium sp. Nat Prod Commun. 2009; 4(3):389–394.
Harishchandra DL, Zhang W, Li X, Chethana KWT, Hyde KD, Brooks S, Yan J, Peng J. A LysM Domain-Containing Protein LtLysM1 Is Important for Vegetative Growth and Pathogenesis in Woody Plant Pathogen Lasiodiplodia theobromae. Plant Pathol J. 2020; 36(4):323–334.
Daengsuwan W, Wonglom P, Sunpapao A. First report of Lasiodiplodia theobromae causing spadix rot in Anthurium andraeanum. J Phytopathol. 2020; 168(2):129–133.
Munirah MS, Azmi AR, Yong SYC, Nur Ain Izzati MZ. Characterization of Lasiodiplodia theobromae and L. pseudotheobromae causing fruit rot on pre-harvest mango in Malaysia. Plant Pathol Quar. 2017;7(2):202–213.
Netto MSB, Assunção IP, Lima GSA, Marques MW, Lima WG, Monteiro JHA, Balbino VDQ, Michereff SJ, Phillips AJL, Camara MPS. Species of Lasiodiplodia associated with papaya stem-end rot in Brazil. Fungal Divers. 2014; 67(1):127–141.
Netto MSB, Lima WG, Correia KC, da Silva CFB, Thon M, Martins RB, Miller RNG, Michereff SJ, Camara MPS. Analysis of phylogeny, distribution, and pathogenicity of Botryosphaeriaceae species associated with gummosis of Anacardium in Brazil, with a new species of Lasiodiplodia. Fungal Biol. 2017; 121(4):437–451.
Sathya K, Parthasarathy S, Thiribhuvanamala G, Prabakar K. Morphological and Molecular Variability of Lasiodiplodia theobromae Causing Stem End Rot of Mango in Tamil Nadu, India. Int J Pure Appl Biosci. 2017;5(6):1024–1031.
Peng J, Wu L, Zhang W, Zhang Q, Xing Q, Wang X, Li X, Yan J. Systemic Identification and Functional Characterization of Common in Fungal Extracellular Membrane Proteins in Lasiodiplodia theobromae. Front Plant Sci. 2021; 12(December):1– 15.
Marsberg A, Kemler M, Jami F, Nagel JH, Postma-Smidt A, Naidoo S, Wingfield MJ, Crous PW, Spatafora J, Hesse CN, Robbertse B, Slippers B. Botryosphaeria dothidea: A latent pathogen of global importance to woody plant health. Mol Plant Pathol. 2016; 18(4):477–488.
Paolinelli-Alfonso M, Villalobos-Escobedo JM, Rolshausen P, Herrera-Estrella A, Galindo-Sanchez C, Lopez-Hernandez JF, Hernadez-Martinez R. Global transcriptional analysis suggests Lasiodiplodia theobromae pathogenicity factors involved in modulation of grapevine defensive response. BMC Genomics. 2016; 17(1):1–20.