Antibacterial, antioxidant, and anticancer activities of Penicillium citrinum Thom. endophytic in Jatropha heynei

Gowdru Basanna Ashoka; Manchanahally Byrappa Shivanna

doi:10.7324/JAPS.2023.95958

Abstract

In the present study, the leaf, fruit, and root samples of Jatropha heynei were incubated using potato dextrose agar, malt extract agar, czapek dox agar, and water agar methods to determine colonization frequency and diversity indices of endophytic fungi. Thirty three endophytic fungal species of 20 genera were recovered from 5,400 segments of J. heynei and were identified based on their morphological characteristics. Species richness was high in leaf followed by root and fruit. Diversity indices varied depending on the season and different plant parts. The metabolites of endophytic fungus Penicillium citrinum were tested for antibacterial, antioxidant, and cytotoxic studies in vitro. The culture filtrate (CF) extract of P. citrinum showed high antibacterial activity to Pseudomonas syringae (zone of inhibition 17.65 ± 1 mm) and Staphylococcus aureus (zone of inhibition 16.32 ± 0.5 mm). The antioxidant potential was determined by cyclic voltammetry method based on the detection of redox potential of metabolites. The CF extract exhibited significant cytotoxic effect in both A549 and MCF-7 cell lines at 500 μg ml−1 with IC50 values of 280.7 and 283.0 μg ml−1, respectively. Orbitrap high resolution liquid chromatography mass spectroscopy (OHR-LCMS) analysis of CF extract documented 21 bio-active compounds; major compounds include 8-hydroxyquinoline, trigonelline, spectinomycin, psoralidin, nicotinic acid, kanosamine, sulfamethazine, artemisinin, and other compounds with bioactive properties. Fourier Transform Infrared Spectroscopic analysis confirmed the presence of functional groups that are attributed to antibacterial, antioxidant, and anticancer compounds profiled in the OHR-LCMS.

Keyword: Jatropha heynei OHR-LCMS A549 and MCF-7 cancer cell lines cyclic voltammetry FTIR

Citation:

Ashoka GB, Shivanna MB. Antibacterial, antioxidant, and anticancer activities of Penicillium citrinum Thom. endophytic in Jatropha heynei. J Appl Pharm Sci, 2022. https://doi.org/10.7324/JAPS.2023.95958

Copyright: © The Author(s). This is an open-access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Reference

Aamir S, Sutar S, Singh SK, Baghela A. A rapid and efficient method of fungal genomic DNA extraction, suitable for PCR based molecular methods. Plant Pathol Quar, 2015; 5(2):74-81. https://doi.org/10.5943/ppq/5/2/6

Abubakar IB, Malami I, Yahaya Y, Sule SM. A review on the ethnomedicinal uses, phytochemistry and pharmacology of Alpinia officinarum Hance. J Ethnopharmacol, 2018; 224:5-62. https://doi.org/10.1016/j.jep.2018.05.027

Achar KS, Shivanna MB. Colletotrichum leaf spot disease in Naravelia zeylanica and its distribution in Bhadra Wildlife Sanctuary, India. Indian Phytopathol, 2013; 66(2):125-31.

Adeleke BS, Babalola OO. Pharmacological potential of fungal endophytes associated with medicinal plants: a review. J Fungi, 2021; 7(2):147. https://doi.org/10.3390/jof7020147

Aharwal RP, Kumar S, Sandhu SS. Endophytic mycoflora: antibacterial secondary metabolites and their therapeutic potential. Curr Pharmacol Rep, 2021; 7(4):150-70. https://doi.org/10.1007/s40495-021-00261-w

Amamra S, Cartea ME, Belhaddad OE, Soengas P, Baghiani A, Kaabi I, Arrar L. Determination of total phenolics contents, antioxidant capacity of Thymus vulgaris extracts using electrochemical and spectrophotometric methods. Int J Electrochem Sci, 2018; 13(8):7882-93. https://doi.org/10.20964/2018.08.57

Ambele CF, Bisseleua HD, Akutse KS, Babalola OO, Humbert P, Patel A, Vidal S, Djuideu CT, Ekesi S. Testing a co-formulation of CO2 releasing material with an entomopathogenic fungus for the management of subterranean termite pests. Mycol Prog, 2019; 18:1201-11. https://doi.org/10.1007/s11557-019-01517-y

Arsenault PR, Wobbe KK, Weathers PJ. Recent advances in artemisinin production through heterologous expression. Curr Med Chem, 2008; 15(27):2886-96. https://doi.org/10.2174/092986708786242813

Arulpriya P, Lalitha P, Hemalatha S. Cyclic voltammetric assessment of the antioxidant activity of petroleum ether extract of Samanea saman (Jacq). Adv Appl Sci Res, 2010; 1:24-35.

Cai Y, Luo Q, Sun M, Corke H. Antioxidant activity and phenolic compounds of 112 traditional Chinese medicinal plants associated with anticancer. Life Sci, 2004; 74(17):2157-84. https://doi.org/10.1016/j.lfs.2003.09.047

Chandra H, Kumari P, Prasad R, Gupta SC, Yadav S. Antioxidant and antimicrobial activity displayed by a fungal endophyte Alternaria alternata isolated from Picrorhiza kurroa from Garhwal Himalayas, India. Biocataly Agric Biotechnol, 2021; 33:101955. https://doi.org/10.1016/j.bcab.2021.101955

Chandrappa CP, Anitha R, Jyothi P, Rajalakshmi K, Seema Mahammadi H, Govindappa M, Sharanappa P. Phytochemical analysis and antibacterial activity of endophytes of Embelia tsjeriam cottam Linn. Int J Pharma Bio Sci, 2013; 3:201-3.

Chapdelaine JM. MTT reduction-a tetrazolium-based colorimetric assay for cell survival and proliferation. Pharm Res Int, 2001:1-6.

Cronstein BN. Adenosine, an endogenous anti-inflammatory agent. J Appl Physiol, 1994; 76(1):5-13. https://doi.org/10.1152/jappl.1994.76.1.5

Darriba D, Taboada GL, Doallo R, Posada D. jModelTest 2: more models, new heuristics and parallel computing. Nat Methods, 2012; 9(8):772. https://doi.org/10.1038/nmeth.2109

de Carvalho CR, Maia MQ, Sobral M, Pereira GMD, da Silva K, Vital MJS, Rosa LH. Diversity and antimicrobial activity of culturable endophytic fungi associated with the neotropical ethnomedicinal plants Copaifera langsdorffii and Copaifera pubiflora. S Afr J Bot, 2021; 142:305-15. https://doi.org/10.1016/j.sajb.2021.06.021

Dwibedi V, Saxena S. In vitro anti-oxidant, anti-fungal and anti-staphylococcal activity of resveratrol-producing endophytic fungi. In: Proceedings of the National Academy of Sciences, India Section B: Biological Sciences, vol. 90, no. 1, pp 207-19, 2020. https://doi.org/10.1007/s40011-019-01098-6

Fadiji AE, Babalola OO. Elucidating mechanisms of endophytes used in plant protection and other bioactivities with multifunctional prospects. Front Bioeng Biotechnol, 2020; 8:467. https://doi.org/10.3389/fbioe.2020.00467

Ferreira MGP, Kayano AM, Silva-Jardim I, Silva TOD, Zuliani, JP, Facundo VA, Stábeli RG. Antileishmanial activity of 3-(3, 4, 5-trimethoxyphenyl) propanoic acid purified from Amazonian Piper tuberculatum Jacq. Piperaceae, fruits. Rev Bras Farmacogn, 2010; 20:1003-6. https://doi.org/10.1590/S0102-695X2010005000033

Gagana SL, Kumaraswamy BE, Shivanna MB. Diversity, antibacterial and antioxidant activities of the fungal endophytes associated with Schleichera oleosa (Lour.) Merr S Afr J Bot, 2020; 134:369-81. https://doi.org/10.1016/j.sajb.2020.06.012

Gamble JS. Flora of the Presidency of Madras, vol. III. Botanical Survey of India, 1934.

George, TK, Joy A, Divya K, Jisha MS. In vitro and in silico docking studies of antibacterial compounds derived from endophytic Penicillium setosum. Microb Pathog, 2019; 131:87-97. https://doi.org/10.1016/j.micpath.2019.03.033

Ghasemzadeh A, Jaafar HZE, Rahmat A. Antioxidant activities, total phenolics and flavonoids content in two varieties of Malaysia Young Ginger (Zingiber officinale Roscoe). Molecules, 2010; 15:4324-33. https://doi.org/10.3390/molecules15064324

Ghobrial IM, Witzig TE, Adjei AA. Targeting apoptosis pathways in cancer therapy. CA Cancer J Clin, 2005; 55(3):178-94. https://doi.org/10.3322/canjclin.55.3.178

Gille A, Bodor ET, Ahmed K, Offermanns S. Nicotinic acid: pharmacological effects and mechanisms of action. Annu Rev Pharmacol Toxicol, 2008; 48:79-106. https://doi.org/10.1146/annurev.pharmtox.48.113006.094746

Gottesman MM, Fojo T, Bates E. Multidrug resistance in cancer: role of ATP-dependent transporters. Nat Rev Cancer, 2002; 2(1):48-58. https://doi.org/10.1038/nrc706

Holloway WJ. Spectinomycin. J Urol, 1982; 128(4):876. https://doi.org/10.1016/S0022-5347(17)53236-X

Huang Z, Nong X, Ren Z, Wang J, Zhang X, Qi S. Anti-HSV-1, antioxidant and antifouling phenolic compounds from the deep-sea-derived fungus Aspergillus versicolor SCSIO 41502. Bioorgan Med Chem Lett, 2017; 27(4):787-91. https://doi.org/10.1016/j.bmcl.2017.01.032

Janiak AM, Milewski S. Mechanism of antifungal action of kanosamine. Med Mycol, 2001; 39(5):401-8. https://doi.org/10.1080/mmy.39.5.401.408

Kannabiran K. Bioactivity-guided extraction and identification of antibacterial compound from marine actinomycetes strains isolated from costal soil samples of Rameswaram and Dhanushkodi, Tamil Nadu, India. Asian J Pharm, 2016; 10(04).

Keffous F, Belboukhari N, Sekkoum K, Djeradi H, Cheriti A, Aboul-Enein HY. Determination of the antioxidant activity of Limoniastrum feei aqueous extract by chemical and electrochemical methods. Cogent Chem, 2016; 2(1):1186141. https://doi.org/10.1080/23312009.2016.1186141

Khare E, Mishra J, Arora NK. Multifaceted interactions between endophytes and plant: developments and prospects. Front Microbiol, 2018; 9:2732. https://doi.org/10.3389/fmicb.2018.02732

Klayman DL. Qinghaosu (artemisinin): an antimalarial drug from China. Science, 1985; 228(4703). https://doi.org/10.1126/science.3887571

Li SJ, Zhang X, Wang XH, Zhao CQ. Novel natural compounds from endophytic fungi with anticancer activity. Eur J Med Chem, 2018; 156:316-43. https://doi.org/10.1016/j.ejmech.2018.07.015

Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods, 1983; 65(1-2):55-63. https://doi.org/10.1016/0022-1759(83)90303-4

Nagata H, Inagaki Y, Yamamoto Y, Maeda K, Kataoka K, Osawa K, Shizukuishi S. Inhibitory effects of macrocarpals on the biological activity of Porphyromonas gingivalis and other periodontopathic bacteria. Oral Microbiol Immunol, 2006; 21(3):159-63. https://doi.org/10.1111/j.1399-302X.2006.00269.x

Newman DJ, Cragg GM. Natural products as sources of new drugs over the last 25 years. J Nat Prod, 2007; 70(3):461-77. https://doi.org/10.1021/np068054v

Nischitha R, Shivanna MB. Metabolite fingerprinting, in vitro antimicrobial and antioxidant activities and in-silico docking in Alloteropsis cimicina and its endophytic fungus Penicillium pinophilum. Mol Biol Rep, 2021:1-17. https://doi.org/10.1007/s11033-021-06410-0

Nischitha R, Vasanthkumari MM, Kumaraswamy BE, Shivanna MB. Antimicrobial and antioxidant activities and chemical profiling of Curvularia tsudae endophytic in Cynodon dactylon (L.) Pers. 3 Biotech, 2020; 10(7):1-2. https://doi.org/10.1007/s13205-020-02250-0

Okoro EE, Ahmad MS, Osoniyi OR, Onajobi FD. Antifungal and antileishmanial activities of fractions and isolated isoflavanquinones from the roots of Abrus precatorius. Comp Clin Path, 2019:1-6. https://doi.org/10.1007/s00580-019-03073-z

Paramanantham P, Pattnaik S, Siddhardha B. Natural products from endophytic fungi: synthesis and applications. In: Singh B (Ed.). Advances in endophytic fungal research, Springer, Cham, Switzerland, pp 83-103, 2019. https://doi.org/10.1007/978-3-030-03589-1_5

Petrini O. Fungal endophytes of tree leaves. Microbial ecology of leaves. Springer, New York, NY, pp 179-97, 1991. https://doi.org/10.1007/978-1-4612-3168-4_9

Prasher P, Sharma M. Medicinal chemistry of anthranilic acid derivatives: a mini review. Drug Dev Res, 2021; 82(7):945-58. https://doi.org/10.1002/ddr.21842

Rama Rao P, Manoharachary C. Soil fungi from Andhra Pradesh. Osmania University, Hyderabad, India, pp 159-64, 1990.

Sharifi-Rad J, Kamiloglu S, Yeskaliyeva B, Beyatli A, Alfred MA, Salehi B, Martorell M. Pharmacological activities of Psoralidin: a comprehensive review of the molecular mechanisms of action. Front Pharmacol, 2020; 11. https://doi.org/10.3389/fphar.2020.571459

Shivanna MB, Vasanthakumari MM. Temporal and spatial variability of rhizosphere and rhizoplane fungal communities in grasses of the subfamily Chloridoideae in the Lakkavalli region of the Western Ghats in India. Mycoshere, 2011; 2(3):255-71. https://doi.org/10.1264/jsme2.ME10163

Sochor J, Dobes J, Krystofova O, Ruttkay-Nedecky B, Babula P, Pohanka M, Kizek R. Electrochemistry as a tool for studying antioxidant properties. Int J Electrochem Sci, 2013; 8(6):8464-89.

Sopalun K, Laosripaiboon W, Wachirachaikarn A, Iamtham S. Biological potential and chemical composition of bioactive compounds from endophytic fungi associated with Thai mangrove plants. S Afr J Bot, 2021; 141:66-76. https://doi.org/10.1016/j.sajb.2021.04.031

Stierle A, Strobel G, Stierle D, Grothaus P, Bignami G. The search for a taxol-producing microorganism among the endophytic fungi of the pacific yew, Taxus brevifoliaJ. Nat Prod, 1995; 58:1315-24. https://doi.org/10.1021/np50123a002

Strong FM. Toxicants occurring naturally in foods. Nutr Rev, 1966; 1354:94.

Subramanian CV. Hyphomycetes. Taxonomy and biology. Academic Press, New York, NY, 1983.

Tan RX, Zou WX. Endophytes: a rich source of functional metabolites. Nat Prod Rep, 2001; 18:448-59. https://doi.org/10.1039/b100918o

Tedesco D, Haragsim L. Cyclosporine: a review. J Transplant, 2012; 2012:230386. https://doi.org/10.1155/2012/230386

Ting L, Yuan-peng H, Qiu-ping L, Guang-Xiong Z. Study on chemical constituents from root and stem of Lycium barbarum L. Nat Prod Res Dev, 2019; 31(9):1491.

Torres M, Ribeiro MA, Oliveira JAS, Meurer EC, Schwan- Estrada KR. Partial chemical characterization of the yeast extracts Lachancea thermotolerans CCMA 0763. Afr J Microbiol Res, 2021; 15(7):388-95. https://doi.org/10.5897/AJMR2020.9459

Turcios AE, Papenbrock J. Enzymatic degradation of the antibiotic sulfamethazine by using crude extracts of different halophytic plants. Int J Phytoremediation, 2019; 21(11):1104-11. https://doi.org/10.1080/15226514.2019.1606782

Unterseher M, Schnittler M. Dilution-to-extinction cultivation of leaf-inhabiting endophytic fungi in beech (Fagus sylvatica L.)-different cultivation techniques influence fungal biodiversity assessment. Mycol Res, 2009; 113(5):645-54. https://doi.org/10.1016/j.mycres.2009.02.002

Vieira ML, Hughes AF, Gil VB, Vaz AB, Alves TM, Zani CL, Rosa LH. Diversity and antimicrobial activities of the fungal endophyte community associated with the traditional Brazilian medicinal plant Solanum cernuum Vell. (Solanaceae). Can J Microbiol, 2012; 58(1):54-66. https://doi.org/10.1139/w11-105

Wu L, Hao H, Wang G. LC/MS-based tools and strategies on qualitative and quantitative analysis of herbal components in complex matrixes. Curr Drug Metab, 2012; 13(9):1251-65. https://doi.org/10.2174/138920012803341285

Zeb A. Chemistry of phenolic antioxidants. Phenolic antioxidants in foods: chemistry, biochemistry and analysis. Springer, Cham, Switzerland, pp 25-87, 2021. https://doi.org/10.1007/978-3-030-74768-8_2

Zhou J, Chan L, Zhou S. Trigonelline: a plant alkaloid with therapeutic potential for diabetes and central nervous system disease. Curr Med Chem, 2012; 19(21):3523-31. https://doi.org/10.2174/092986712801323171

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