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Antimicrobial activity and metabolite profiling of endophytic fungi in Digitaria bicornis (Lam) Roem. and Schult. and Paspalidium flavidum (Retz.) A. Camus.

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Abstract

Endophytic fungal occurrences were studied in aerial regions of Digitaria bicornis and Paspalidium flavidum by three isolation methods: potato dextrose agar (PDA), malt extract agar (MEA), and moist blotters. Seventy species of 29 genera of endophytic fungi in D. bicornis and 71 species of 30 genera in P. flavidum were documented. Endophytic fungal communities were grouped into 40 and 43 anamorphic ascomycetes (21 and 23 genera) and 20 teleomorphic ascomycetes (6 and 7 genera) in D. bicornis and P. flavidum, respectively. PDA supported the expression of larger number of fungal communities than MEA and MB; and P. flavidum hosted more number of endophytic fungi than D. bicornis. Seasons played an important role in supporting the assemblage of fungal endophytes. Endophytic fungal species richness and assemblages in plant regions were determined for alpha, beta, and gamma diversities. The ethyl acetate followed by methanolic extracts of certain fungal species showed good antagonistic and antibacterial activities. Among fungal endophytes, Curvularia protuberata and Penicillium citrinum exhibited high antagonistic and antibacterial activities. The high-resolution orbitrap liquid chromatography–mass spectrometry of ethyl acetate crude extracts of C. protuberata and P. citrinum revealed the presence of antifungal and antimicrobial, besides a host of compounds in the extracts. The present study indicated that grass endophytes are the sources of compounds with antimicrobial and other pharmacological activities.

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References

  • Abdelfattah A, Wisniewski M, Nicosia MGLD, Cacciola SO, Schena L (2016) Metagenomic analysis of fungal diversity on strawberry plants and the effect of management practices on the fungal community structure of aerial organs. PLoS ONE 11(8):1–17

    Article  Google Scholar 

  • Achar KGS, Shivanna MB (2013) Colletotrichum leaf spot disease in Naravelia zeylanica and its distribution in Bhadra Wildlife Sanctuary, India. Ind Phytopathol 66:125–131

    Google Scholar 

  • Adam M, Dobiáš P, Eisner A, Ventura K (2009) Extraction of antioxidants from plants using ultrasonic methods and their antioxidant capacity. J Sep Sci 32(2):288–294

    Article  CAS  PubMed  Google Scholar 

  • Au N, Rettie AE (2008) Pharmacogenomics of 4-hydroxycoumarin anticoagulants. Drug Metab Rev 40(2):355–375

    Article  CAS  PubMed  Google Scholar 

  • Aydaş SB, Ozturk S, Aslım B (2013) Phenylalanine ammonia lyase (PAL) enzyme activity and antioxidant properties of some cyanobacteria isolates. Food chem 136(1):164–169

    Article  Google Scholar 

  • Barnett HL (1972) Illustrated Genera of imperfect fungi. Burgess Publishing Company, Minneapolis, pp 225–426

    Google Scholar 

  • Bastien N, Millau JF, Rouabhia M, Davies RJH, Drouin R (2010) The sunscreen agent 2-phenylbenzimidazole-5-sulfonic acid photosensitizes the formation of oxidized guanines in cellulo after UV-A or UV-B exposure. J Invest Dermatol 130(10):2463–2471

    Article  CAS  PubMed  Google Scholar 

  • Bazotte RB, Lopes-Bertolini G (2012) Effects of oral L-carnitine and DL-carnitine supplementation on alloxan-diabetic rats. Braz Arch Biol Technol 55(1):81–88

    Article  CAS  Google Scholar 

  • Corbridge DEC (1996) Phosphorus: an outline of its chemistry, biochemistry, and technology 5th edn Elsevier: Amsterdam. ISBN 0–444–89307–5.

  • Daoubi M, Deligeorgopoulou A, Macías-Sánchez AJ, Hernández-Galán R, Hitchcock PB, Hanson JR, Collado IG (2005) Antifungal activity and biotransformation of diisophorone by Botrytis cinerea. J Agric Food Chem 53(15):6035–6039

    Article  CAS  PubMed  Google Scholar 

  • Deshmukh SK, Kolet MJ, Verekar SA (2010) Distribution of endophytic fungi in lemon grass (Cymbopogon citratus (DC) Stapf.). J Cell Tissue Res 10(2):2263–2267

    Google Scholar 

  • Devarajan PT, Suryanarayanan TS (2002) Endophytic fungi associated with the tropical seagrass. Halophila ovalis (Hydrocharitaceae) 31(1):73–74

    Google Scholar 

  • Du FY, Li XM, Li CS, Wang BG (2012) Chemical constituents of Aspergillus sydowii EN-198, an endophytic fungus derived from the marine-mangrove plant Hibicus tiliaceus. Marine Sci 36:6–11

    CAS  Google Scholar 

  • Fisher PJ, Petrini O (1988) Tissue specificity by fungi endophytic in Ulex europaeus. Sydowia 40:46–50

    Google Scholar 

  • Giauque H, Hawkes CV (2016) Historical and current climate drive spatial and temporal patterns in fungal endophyte diversity. Fungal Ecol 20:108–114

    Article  Google Scholar 

  • Giridharan P, Verekar SA, Khanna A, Mishra PD, Deshmukh SK (2012) Anticancer activity of sclerotiorin, isolated from an endophytic fungus Cephalotheca faveolata Yaguchi, Nishim. & Udagawa. Indian J Exp Biol 50:464–468

    CAS  PubMed  Google Scholar 

  • Gomes T, Pereira JA, Benhadi J, Lino-Neto T, Baptista P (2018) Endophytic and epiphytic phyllosphere fungal communities are shaped by different environmental factors in a mediterranean ecosystem. Microb Ecol 76(3):668–679

    Article  PubMed  Google Scholar 

  • Goswami DG, Kant R, Tewari-Singh N, Agarwal R (2018) Efficacy of anti-inflammatory, antibiotic and pleiotropic agents in reversing nitrogen mustard-induced injury in ex vivo cultured rabbit cornea. Toxicol Lett 293:127–132

    Article  CAS  PubMed  Google Scholar 

  • Hammer O, Harper DAT, Ryan PD (2001) Paleontological statistics Software Package for education and data analysis. http://palaeo-electronica.org/2001

  • Hosseini MM, Soltani J, Babolhavaeji F, Hamzei J, Nazeri S, Mirzaei S (2013) Bioactivities of endophytic Penicillia from Cupressaceae. J Crop Prot 2(4):421–433

    Google Scholar 

  • Hua Y, Jenke D (2012) Increasing the sensitivity of an LC–MS method for screening material extracts for organic extractables via mobile phase optimization. J Chromatogr Sci 50(3):213–227

    Article  CAS  PubMed  Google Scholar 

  • Jalgaonwala RE, Mahajan RT (2015) Investigation about seasonal variation and tissue specificity by endophytic fungi from fifteen Indian medicinal plants. Int J Multidiscip Res Dev 2(3):506–512

    Google Scholar 

  • Kannabiran K (2016) 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 10(4):2–6

    Google Scholar 

  • Konig J, Guerreiro MA, Persoh D, Begerow D, Krauss J (2018) Knowing your neighbourhood—the effects of Epichloë endophytes on foliar fungal assemblages in perennial ryegrass in dependence of season and land-use intensity. PeerJ 6:1–21

    Article  Google Scholar 

  • Kosswig K (2005) Surfactants in Ullmann’s encyclopedia of industrial chemistry. Wiley Weinheim. ISBN: 9783527303854

  • Kour A, Shawl AS, Rehman S, Sultan P, Qazi PH, Suden P, Khajuria RK, Verma V (2008) Isolation and identification of an endophytic strain of Fusarium oxysporum producing podophyllotoxin from Juniperus recurva. World J Microbiol Biotechnol 24(7):1115–1121

    Article  CAS  Google Scholar 

  • Kuldau G, Bacon C (2008) Clavicipitaceous endophytes: their ability to enhance resistance of grasses to multiple stresses. Biol Contrl 46(1):57–71

    Article  Google Scholar 

  • Li D, Ellis EM (2012) Inducible protection of human astrocytoma 1321N1 cells against hydrogen peroxide and aldehyde toxicity by 7-hydroxycoumarin is associated with the upregulation of aldo-keto reductases. Neurotoxicology 33(5):1368–1374

    Article  PubMed  Google Scholar 

  • Marquez SS, Bills GF, Acuna LD, Zabalgogeazcoa I (2010) Endophytic mycobiota of leaves and roots of the grass Holcus lanatus. Fungal Diver 41(1):115–123

    Article  Google Scholar 

  • Martins F, Pereira JA, Bota P, Bento A, Baptista P (2016) Fungal endophyte communities in above-and belowground olive tree organs and the effect of season and geographic location on their structures. Fungal ecol 20:193–201

    Article  Google Scholar 

  • Mauro V, Carette D, Pontier-Bres R, Dompierre J, Czerucka D, Segretain D, Gilleron J, Pointis G (2013) The anti-mitotic drug griseofulvin induces apoptosis of human germ cell tumor cells through a connexin 43-dependent molecular mechanism. Apoptosis 18(4):480–491

    Article  CAS  PubMed  Google Scholar 

  • Murafuji T, Fujiwara Y, Yoshimatsu D, Miyakawa I, Migita K, Mikata Y (2011) Bismuth heterocycles based on a diphenyl sulfone scaffold: Synthesis and substituent effect on the antifungal activity against Saccharomyces cerevisiae. Eur J Med chem 46(2):519–525

    Article  CAS  PubMed  Google Scholar 

  • Murata T, Mori N, Nishida R (2011) Larval feeding stimulants for a rutaceae-feeding swallowtail butterfly, Papilio xuthus L. Citrus unshiu leaves J chem ecol 37(10):1099–1109

    Article  CAS  PubMed  Google Scholar 

  • Nath A, Prajwal R, Joshi SR (2012) Diversity and biological activities of endophytic fungi of Emblica officinalis, an ethnomedicinal plant of India. Mycobiol 40:8–13

    Article  Google Scholar 

  • Nisa S, Khan N, Shah W, Sabir M, Khan W, Bibi Y, Jahangir M, Haq IU, Alam S, Qayyum A (2020) Identification and bioactivities of two endophytic fungi Fusarium fujikuroi and Aspergillus tubingensis from foliar parts of Debregeasia salicifolia. Arabian J Sci Engingr 45(6):4477–4487

    Article  CAS  Google Scholar 

  • Nischitha R, Shivanna MB (2020) Influence of seasons on endophytic fungal assemblage in Alloteropsis cimicina (L.) Stapf. and Heteropogon contortus (L.) P. Beauv of the sub-family panicoideae. Curr Res Environ App Mycol 10(1):10–25

    Article  Google Scholar 

  • Nischitha R, Vasanthkumari MM, Kumaraswamy BE, Shivanna MB (2020) Antimicrobial and antioxidant activities and chemical profiling of Curvularia tsudae endophytic in Cynodon dactylon (L.) Pers 3. Biot 10(7):1–12

    Google Scholar 

  • Oh SY, Mead PJ, Sharma BS, Quinton VM, Boermans HJ, Smith TK, Swamy HVLN, Karrow NA (2015) Effect of Penicillium mycotoxins on the cytokine gene expression, reactive oxygen species production, and phagocytosis of bovine macrophage (BoMacs) function. Toxicol in Vitro 30(1):446–453

    Article  CAS  PubMed  Google Scholar 

  • Oršolić N, Kunštić M, Kukolj M, Gračan R, Nemrava J (2016) Oxidative stress, polarization of macrophages and tumour angiogenesis: efficacy of caffeic acid. Chem -Biol Interact 256:111–124

    Article  PubMed  Google Scholar 

  • Pamphile JA, Azevedo JL (2002) Molecular characterization of endophytic strains of Fusarium verticillioides (=Fusarium moniliforme) from maize (Zea mays L.). World J Microbiol Biotechnol. 18(5):391–396

    Article  CAS  Google Scholar 

  • Pan H, Piermartiri TC, Chen J, McDonough J, Oppel C, Driwech W, Grunberg N (2015) Repeated systemic administration of the nutraceutical alpha-linolenic acid exerts neuroprotective efficacy, an antidepressant effect and improves cognitive performance when given after soman exposure. Neurotoxicol 51:38–50

    Article  CAS  Google Scholar 

  • Rajamani T, Suryanarayanan TS, Murali TS, Thirunavukkarasu N (2018) Distribution and diversity of foliar endophytic fungi in the mangroves of Andaman Islands, India. Fungal ecol 36:109–116

    Article  Google Scholar 

  • Raviraja NS, Maria GL, Sridhar KR (2006) Antimicrobial evaluation of endophytic fungi inhabiting medicinal plants of the Western Ghats of India. Engineer Life Sci 6(5):515–520

    Article  CAS  Google Scholar 

  • Rekha D, Shivanna MB (2014) Diversity, antimicrobial and antioxidant activities of fungal endophytes in Cynodon dactylon (L.) Pers. and Dactyloctenium aegyptium (L.) P. Beauv. Int J Curr Microbiol App Sci 3(8):573–591

    Google Scholar 

  • Rider CV, Janardhan KS, RaoD MJP, McPherson CA, Harry GJ (2012) Evaluation of N-butylbenzenesulfonamide (NBBS) neurotoxicity in Sprague-Dawley male rats following 27-day oral exposure. NeuroToxicol 33(6):1528–1535

    Article  CAS  Google Scholar 

  • Rodriguez RJ, White JF Jr, Arnold AE, Redman ARA (2009) Fungal endophytes: diversity and functional roles. New Phytol 182(2):314–330

    Article  CAS  PubMed  Google Scholar 

  • Sarma P, Dkhar MS, Kayang H, Kumar M, Raghuwanshi DNK, R, (2018) Diversity of endophytic fungi associated with the medicinally important aromatic plant Gaultheria fragrantissima Wall. Stud Fungi 3(1):309–320

    Article  Google Scholar 

  • Schulthess FM, Faeth SH (1998) Distribution, abundances, and associations of the endophytic fungal community of Arizona fescue (Festuca arizonica). Mycolog 90(4):569–578

    Article  Google Scholar 

  • Seifert K, Morgan-Jones G, Gams W, Kendrick B (2011) The Genera of hyphomycetes: Utrecht.CBS-KNAW Fungal Biodiversity Centre, CBS Biodiversity Series, Netherlands. 8:997.

  • Shao J, He Y, Li F, Zhang H, Chen A, Luo S, Gu JD (2016) Growth inhibition and possible mechanism of oleamide against the toxin-producing cyanobacterium Microcystis aeruginosa NIES-843. Ecotoxicol 25(1):225–233

    Article  CAS  Google Scholar 

  • Shivanna MB, Vasanthakumari MM (2011) 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. Mycosphere 2(3):255–271

    Google Scholar 

  • Shivanna MB, Parashurama TR, Somashekhara Achar KG, Vasanthakumari MM (2013) Fungal foliar diseases in Withania somnifera and its effect on secondary metabolites. Plant Biosyst 66(3):287–293

    Google Scholar 

  • Shweta S, Gurumurthy BR, Vasanthakumari MM, Ravikanth G, Dayanandan S, Storms R, Shaanker Shivanna MB, RU, (2015) Endophyte fungal diversity in Nothapodytes nimmoniana along its distributional gradient in the Western Ghats, India: are camptothecine (anticancer alkaloid) producing endophytes restricted to specific clades? Curr Sci 109 (1):127–138

    Google Scholar 

  • Sidoryk K, Jaromin A, Edward JA, Świtalska M, Stefańska J, Cmoch P, Zagrodzka J, Szczepek W, Peczyńska-Czoch W, Wietrzyk J, Kozubek A (2014) Searching for new derivatives of neocryptolepine: synthesis, antiproliferative, antimicrobial and antifungal activities. Eur J Med chem 78:304–313

    Article  CAS  PubMed  Google Scholar 

  • Singh DK, Sharma VK, Kumar J, Mishra A, Verma SK, Sieber TN, Kharwar RN (2016) The diversity of endophytic mycobiota of tropical tree Tectona grandis Linn. f: Spatio-temporal and tissue type effects. Sci Rep 7(1):1–14

    CAS  Google Scholar 

  • Supaphon P, Phongpaichit S, Rukachaisirikul V, Sakayaroj J (2014) Diversity and antimicrobial activity of endophytic fungi isolated from the seagrass Enhalus acoroides. Ind J Geo-Marine Sci 43(5):785–797

    Google Scholar 

  • Suryanarayanan TS, Johnson JA (2014) Fungal endosymbionts of macroalgae: need for enquiries into diversity and technological potential. Oceanography 2(119):1–3

    Google Scholar 

  • Suryanarayanan TS, Senthilarasu G, Muruganandam V (2000) Endophytic fungi from Cuscuta reflexa and its host plants. Fungal Divers 4:117–123

    Google Scholar 

  • Talapatra K, Das AR, Saha AK, Das P (2017) In vitro antagonistic activity of a root endophytic fungus towards plant pathogenic fungi. J Appl Biol Biotechnol 5(02):068–071

    Google Scholar 

  • Tigges B, Dederichs T, Möller M, Liu T, Richtering W, Weichold O (2010) Interfacial properties of emulsions stabilized with surfactant and nonsurfactant coated boehmite nanoparticles. Langmuir 26(23):17913–17918

    Article  CAS  PubMed  Google Scholar 

  • Tsuzuki T, Tokuyama Y, Igarashi M, Miyazawa T (2004) Tumor growth suppression by α-eleostearic acid, a linolenic acid isomer with a conjugated triene system, via lipid peroxidation. Carcinogenesis 25(8):1417–1425

    Article  CAS  PubMed  Google Scholar 

  • Vasanthakumari MM, Shivanna MB (2009) Fungal assemblages in the rhizosphere and rhizoplane of grasses of the subfamily Panicoideae in the Lakkavalli region of Karnataka India. Microbes Environ 26(3):228–236

    Article  Google Scholar 

  • Venkatesan R, Karuppiah PS, Arumugam G, Balamuthu K (2019) β-Asarone exhibits antifungal activity by inhibiting ergosterol biosynthesis in Aspergillus niger ATCC 16888. Proc Natl Acad Sci India Sect B Biol Sci 89(1):173–184

    Article  CAS  Google Scholar 

  • Wang KC, Chang JS, Chiang LC, Lin CC (2009) 4-Methoxycinnamaldehyde inhibited human respiratory syncytial virus in a human larynx carcinoma cell line. Phytomedicine 16(9):882–886

    Article  CAS  PubMed  Google Scholar 

  • Wang S, Yue K, Liu L, Yang W (2013) Photoreactive, core–shell cross-linked/hollow microspheres prepared by delayed addition of cross-linker in dispersion polymerization for antifouling and immobilization of protein. J Colloid Interface Sci 389(1):126–133

    Article  CAS  PubMed  Google Scholar 

  • Wille T, Kaltenbach L, Thiermann H, Worek F (2013) Investigation of kinetic interactions between approved oximes and human acetylcholinesterase inhibited by pesticide carbamates. Chem-biol intera 206(3):569–572

    Article  CAS  Google Scholar 

  • Wollweber, Hartmund (2000) “Hypnotics”. Ullmann’s encyclopedia of industrial chemistry: 11. ISBN: 9783527303854

  • Wu ZH, Wang TH, Huang W, Qu YB (2001) A simplified method for chromosome DNA preparation from filamentous Fungi. Mycosyst 20:575–577

    CAS  Google Scholar 

  • Yasukawa K, Akihisa T, Kanno H, Kaminaga T, Izumida M, Sakoh T, Tamura T, Takido M (1996) Inhibitory effects of sterols isolated from Chlorella vulgaris on 12-O-tetradecanoylphorbol-13-acetate-induced inflammation and tumor promotion in mouse skin. Biol Pharm Bull 19(4):573–576

    Article  CAS  PubMed  Google Scholar 

  • Zhang P, Zhou PP, Yu LJ (2009) An endophytic taxol-producing fungus from Taxus media, Cladosporium cladosporioides MD2. Curr microbiol 59(3):227–232

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The first author thanks the UGC, New Delhi for awarding Junior Research Fellowship and is also thankful to SAIF, IIT, Bombay for OHR LC–MS service.

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MBS conceived the initial work idea and NR performed the laboratory experiments and data analysis. MBS and NR worked on the data interpretation of the work. NR prepared the first draft copy of the manuscript, and the corrections were made and finalized by MBS and approved the final manuscript.

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Correspondence to M. B. Shivanna.

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Nischitha, R., Shivanna, M.B. Antimicrobial activity and metabolite profiling of endophytic fungi in Digitaria bicornis (Lam) Roem. and Schult. and Paspalidium flavidum (Retz.) A. Camus.. 3 Biotech 11, 53 (2021). https://doi.org/10.1007/s13205-020-02590-x

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