Skip to main content
Log in

Antibacterial potential of secondary metabolites produced by Aspergillus sp., an endophyte of Mitrephora wangii

  • Original Paper
  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abstract

Mitrephora wangii, an ethnomedicinal plant, has been used as a natural antibiotic and immunity booster in Thailand. A total of 22 fungi were isolated from M. wangii flowers. The fungal isolates were categorized into six genera including Agrocybe, Aspergillus, Colletotrichum, Nigrospora, Puccinia and Ustilago. Most extracts exhibited antibacterial activity against at least one of the test bacteria. Aspergillus sp. MFLUCC16-0845 was identified as the most bioactive fungus. Chemical composition of Aspergillus sp. MFLUCC16-0845 investigated using gas chromatography–mass spectrometry indicated that the major antibacterial compound was β-thujaplicin. Moreover, the newly isolated Aspergillus sp. MFLUCC16-0845 could be exploited as a potential source of bioactive compounds and plant defense activators. In addition, it is the first time that strain of Aspergillus sp. isolated and cultured from M. wangii flowers could produce β-thujaplicin at high yield with strong antimicrobial spectrum, which may lead to wide utilization in producing cosmetics and clinical products.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Adams RP (2007) Identification of essential oil components by gas chromatography/mass spectroscopy, 4th edn. Allured Publishing Corporation, Illinois

    Google Scholar 

  • Aly AH, Debbab A, Kjer J, Proksch P (2010) Fungal endophytes from higher plants: a prolific source of phytochemicals and other bioactive natural products. Fungal Divers 41:1–16

    Article  Google Scholar 

  • Araújo WL, Marcon J, Maccheroni W, van Elsas JD, van Vuurde JW, Azevedo JL (2002) Diversity of endophytic bacterial populations and their interaction with Xylella fastidiosa in citrus plants. Appl Environ Microbiol 68:4906–4914

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Arima Y, Nakai Y, Hayakawa R, Nishino T (2003) Antibacterial effect of β-thujaplicin on staphylococci isolated from atopic dermatitis: relationship between changes in the number of viable bacterial cells and clinical improvement in an eczematous lesion of atopic dermatitis. J Antimicrob Chemother 51:113–122

    Article  PubMed  CAS  Google Scholar 

  • Atiphasaworn P, Monggoot S, Gentekaki E, Brooks S, Pripdeevech P (2017) Antibacterial and antioxidant constituents of extracts of endophytic fungi isolated from Ocimum basilicum var. thyrsiflora leaves. Curr Opin Microbiol 74:1185–1193

    Article  CAS  Google Scholar 

  • Azevedo JL, Maccheroni JW, Pereira JO, de Araújo WL (2000) Endophytic microorganisms: a review on insect control and recent advances on tropical plants. Electron J Biotechnol 3:40–65

    Article  Google Scholar 

  • Barnett HL, Hunter BB (1998) Illustrated genera of imperfect fungi. Illustrated genera of imperfect fungi, 3rd edn. APS Press, Minnesota

    Google Scholar 

  • Barrero AF, del Moral JFQ, Lara A, Herrador MM (2005) Antimicrobial activity of sesquiterpenes from the essential oil of Juniperus thurifera wood. Planta Med 71:67–71

    Article  PubMed  CAS  Google Scholar 

  • Berdy J (2005) Bioactive microbial metabolites. J Antibiot 58:1–26

    Article  PubMed  CAS  Google Scholar 

  • Cakir A, Kordali S, Zengin H, Izumi S, Hirata T (2004) Composition and antifungal activity of essential oils isolated from Hypericum hyssopifolium and H. heterophyllum. Flavour Fragr J 19:62–68

    Article  CAS  Google Scholar 

  • Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T (2009) trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25:1972–1973

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cha JD, Jeong MR, Jeong SI, Moon SE, Kim JY, Kil BS, Song YH (2005) Chemical composition and antimicrobial activity of the essential oils of Artemisia scoparia and A. capillaris. Planta Med 71:186–190

    Article  PubMed  CAS  Google Scholar 

  • Cristani M, D’Arrigo M, Mandalari G, Castelli F, Sarpietro MG, Micieli D, Trombetta D (2007) Interaction of four monoterpenes contained in essential oils with model membranes: implications for their antibacterial activity. J Agric Food Chem 55:6300–6308

    Article  PubMed  CAS  Google Scholar 

  • Farshori NN, Banday MR, Ahmad A, Khan AU, Rauf A (2011) 7-Hydroxy-coumarin derivatives: synthesis, characterization and preliminary antimicrobial activities. Med Chem Res 20:535–541

    Article  CAS  Google Scholar 

  • Ge H, Kong X, Shi L, Hou L, Liu Z, Li P (2009) Gamma-linolenic acid induces apoptosis and lipid peroxidation in human chronic myelogenous leukemia K562 cells. Cell Biol Int Rep 33:402–410

    Article  CAS  Google Scholar 

  • Geiser DM (2009) Sexual structures in Aspergillus: morphology, importance and genomics. Med Mycol 47:21–26

    Article  CAS  Google Scholar 

  • Gunatilaka AL (2006) Natural products from plant-associated microorganisms: distribution, structural diversity, bioactivity, and implications of their occurrence. J Nat Prod 69:509–526

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Inoue Y, Shiraishi A, Hada T, Hirose K, Hamashima H, Shimada J (2004) The antibacterial effects of terpene alcohols on Staphylococcus aureus and their mode of action. FEMS Microbiol Lett 237:325–331

    PubMed  CAS  Google Scholar 

  • Katoh K, Toh H (2010) Parallelization of the MAFFT multiple sequence alignment program. Bioinformatics 26:1899–1900

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kurose D, Furuya N, Tsuchiya K, Tsushima S, Evans H (2012) Endophytic fungi associated with Fallopia japonica (Polygonaceae) in Japan and their interactions with Puccinia polygoni-amphibii var. tovariae, a candidate for classical biological control. Fungal Biol 116:785–791

    Article  PubMed  Google Scholar 

  • Kusari S, Lamshöft M, Spiteller M (2009) Aspergillus fumigatus Fresenius, an endophytic fungus from Juniperus communis L. Horstmann as a novel source of the anticancer pro-drug deoxypodophyllotoxin. J Appl Microbiol 107:1019–1030

    Article  PubMed  CAS  Google Scholar 

  • Li XJ, Zhang Q, Zhang AL, Gao JM (2012) Metabolites from Aspergillus fumigatus, an endophytic fungus associated with Melia azedarach, and their antifungal, antifeedant, and toxic activities. J Agric Food Chem 60:3424–3431

    Article  PubMed  CAS  Google Scholar 

  • Lu H, Zou WX, Meng JC, Hu J, Tan RX (2000) New bioactive metabolites produced by Colletotrichum sp., an endophytic fungus in Artemisia annua. Plant Sci 151:67–173

    Article  CAS  Google Scholar 

  • Machumi F, Samoylenko V, Yenesew A, Derese S, Midiwo JO, Wiggers FT, Muhammad I (2010) Antimicrobial and antiparasitic abietane diterpenoids from the roots of Clerodendrum eriophyllum. Nat Prod Commun 5:853–858

    PubMed  PubMed Central  CAS  Google Scholar 

  • Márquez SS, Bills GF, Zabalgogeazcoa I (2007) The endophytic mycobiota of the grass Dactylis glomerata. Fungal Divers 27:171–195

    Google Scholar 

  • Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: Proceedings of the gateway computing environments workshop (GCE), 14 November, Ieee, Louisiana, pp 1–8

  • Owen NL, Hundley N (2004) Endophytes—the chemical synthesizers inside plants. Sci Prog 87:79–99

    Article  PubMed  CAS  Google Scholar 

  • Petrini O, Sieber TN, Toti L, Viret O (1993) Ecology, metabolite production, and substrate utilization in endophytic fungi. Nat Toxins 1:185–196

    Article  Google Scholar 

  • Rai M, Rathod D, Agarkar G, Dar M, Brestic M, Pastore GM, Junior MRM (2014) Fungal growth promotor endophytes: a pragmatic approach towards sustainable food and agriculture. Symbiosis 62:63–79

    Article  CAS  Google Scholar 

  • Rodrigues KF (1994) The foliar fungal endophytes of the Amazonian palm Euterpe oleracea. Mycologia 86:376–385

    Article  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  PubMed  CAS  Google Scholar 

  • Sanyacharernkul S, Nantapap S, Sangrueng K, Nuntasaen N (2016) Antifungal of modified neolignans from Mitrephora wangii Hu. Appl Biol Chem 59:385–389

    Article  CAS  Google Scholar 

  • Schulz B, Boyle C (2005) The endophytic continuum. Mycol Res 109:661–686

    Article  PubMed  Google Scholar 

  • Senadeera SPD, Wiyakrutta S, Mahidol C, Ruchirawat S, Kittakoop P (2012) A novel tricyclic polyketide and its biosynthetic precursor azaphilone derivatives from the endophytic fungus Dothideomycete sp. Org Biomol Chem 10:7220–7226

    Article  PubMed  CAS  Google Scholar 

  • Shih YH, Chang KW, Hsia SM, Yu CC, Fuh LJ, Chi TY, Shieh TM (2013) In vitro antimicrobial and anticancer potential of hinokitiol against oral pathogens and oral cancer cell lines. Microbiol Res 168:254–262

    Article  PubMed  CAS  Google Scholar 

  • Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690

    Article  PubMed  CAS  Google Scholar 

  • Stinson M, Ezra D, Hess WM, Sears J (2003) An endophytic Gliocladium sp. of Eucryphia cordifolia producing selective volatile antimicrobial compounds. Plant Sci 165:913–922

    Article  CAS  Google Scholar 

  • Stojanović-Radić Z, Čomić L, Radulović N, Blagojević P, Denić M, Miltojević A, Mihajilov-Krstev T (2012) Antistaphylococcal activity of Inula helenium L. root essential oil: eudesmane sesquiterpene lactones induce cell membrane damage. Eur J Clin Microbiol Infect Dis 31:1015–1025

    Article  PubMed  CAS  Google Scholar 

  • Stone JK, Polishook JD, White JF (2004) Endophytic fungi. In: Mercedes SF, Gerald FB (eds) Biodiversity of fungi. Elsevier Academic Press, Burlington, pp 241–270

    Chapter  Google Scholar 

  • Strobel G (2003) Rainforest endophytes and bioactive products. Crit Rev Biotechnol 22:315–333

    Article  Google Scholar 

  • Strobel G, Daisy B (2003) Bioprospecting for microbial endophytes and their natural products. Microbiol Mol Biol Rev 67:491–502

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Strobel G, Daisy B, Castillo U, Harper J (2004) Natural products from endophytic microorganisms. J Nat Prod 67:257–268

    Article  PubMed  CAS  Google Scholar 

  • Sureshjani MH, Yazdi FT, Mortazavi SA, Behbahani BA, Shahidi F (2014) Antimicrobial effects of Kelussia odoratissima extracts against food borne and food spoilage bacteria “in vitro”. J Paramed Sci 5:115–120

    Google Scholar 

  • Tanamatayarat P, Sotanaphun U, Limsirichaikul S, Girmay S (2012) Cytotoxic dihydrobenzofurans from Mitrephora Wangii Hu. Pharm Biol 50:578–579

    Google Scholar 

  • Wani MA, Sanjana K, Kumar DM, Lal DK (2010) GC-MS analysis reveals production of 2-phenylethanol from Aspergillus niger endophytic in rose. J Basic Microbiol 50:110–114

    Article  PubMed  CAS  Google Scholar 

  • Weerasooriya AD, Saunders RM (2010) Systematic botany monographs: monograph of mitrephora (Annonaceae). American Society of Plant Taxonomists Press, Michigan

    Google Scholar 

  • Wibowo M, Prachyawarakorn V, Aree T, Wiyakrutta S, Mahidol C, Ruchirawat S, Kittakoop P (2014) Tricyclic and spirobicyclic norsesquiterpenes from the endophytic fungus Pseudolagarobasidium acaciicola. Eur J Org Chem 19:3976–3980

    Article  CAS  Google Scholar 

  • Wibowo M, Prachyawarakorn V, Aree T, Mahidol C, Ruchirawat S, Kittakoop P (2016) Cytotoxic sesquiterpenes from the endophytic fungus Pseudolagarobasidium acaciicola. Phytochemistry 122:126–138

    Article  PubMed  CAS  Google Scholar 

  • Woguem V, Fogang HP, Maggi F, Tapondjou LA, Womeni HM, Quassinti L, Papa F (2014) Volatile oil from striped African pepper (Xylopia parviflora, Annonaceae) possesses notable chemopreventive, anti-inflammatory and antimicrobial potential. Food Chem 149:183–189

    Article  PubMed  CAS  Google Scholar 

  • Zhao K, Ping W, Li Q, Hao S, Zhao L, Gao T, Zhou D (2009a) Aspergillus niger var. taxi, a new species variant of taxol-producing fungus isolated from Taxus cuspidata in China. J Appl Microbiol 107:1202–1207

    Article  PubMed  CAS  Google Scholar 

  • Zhao X, Sugawara T, Kuroda S, Arisawa J, Kimura K (2009b) Antimicrobial activity of Beta-Thujaplicin (Hinokitiol) on heterotrophic bacteria isolated from reverse osmosis water using for the preparation of hemodialysis fluids. In: Proceedings of the world congress on medical physics and biomedical engineering, 7–12 September, Springer Berlin Heidelberg, Munich, pp 30–33

Download references

Acknowledgements

The authors are thankful to Department of Medical Science, Ministry of Health, Bangkok, Thailand for bacterial pathogens. Authors express thanks to Institute of Excellence in Fungal Research and Botanical garden of Mae Fah Luang University for collecting of isolated fungal endophytes and identifying of plants, respectively. The financial support from Mae Fah Luang University is highly appreciated.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Patcharee Pripdeevech.

Ethics declarations

Conflict of interest

The authors have no conflict of interest to declare.

Additional information

Communicated by Erko Stackebrandt.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Monggoot, S., Pichaitam, T., Tanapichatsakul, C. et al. Antibacterial potential of secondary metabolites produced by Aspergillus sp., an endophyte of Mitrephora wangii. Arch Microbiol 200, 951–959 (2018). https://doi.org/10.1007/s00203-018-1511-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00203-018-1511-5

Keywords

Navigation