Skip to main content
SpringerLink
Log in

Antimicrobial properties of 6-pentyl-α-pyrone produced by endophytic strains of Trichoderma koningii and its effect on aflatoxin B1 production

  • Published:
Biologia Aims and scope Submit manuscript

Abstract

A total of 60 endophytic fungal strains were isolated and screened for their producing-ability of 6-pentyl-α-pyrone (6PP), which has a coconut-like aroma. Of these isolated strains, four strains of Trichoderma koningii Oudemans were positive for 6PP production. Agar well diffusion assay was employed to test the antimicrobial activity of 6PP against 22 microbial strains. Although 6PP showed no antibacterial activity against several bacterial strains, it interestingly exhibited positive inhibitory activity against Staphylococcus aureus recording a minimal inhibitory concentration (MIC) of 100 μg/mL. The 6PP displayed a good antifungal activity against all filamentous fungi tested with MICs ranged from 80 to 90 μg.mL. To demonstrate its mode of antimicrobial activity, Staphylococcus aureus, Aspergillus flavus, Penicillium expansum and Fusarium acuminatum were treated with 6PP at sub-MICs and examined by scanning and transmission electron microscopy. Several morphological alterations were caused by 6PP, such as induction of a bleb-like structure on the outer surface of the treated bacteria and surface depression with loosing hyphal linearity of the treated fungi. Additionally, several extensive cellular damages were also observed in microbial cells and the most frequent alteration noticed was the detachment of plasma membrane from cell wall. The inhibitory activity of 6PP was further demonstrated on aflatoxin B1 (AFB1) production by several strains of Aspergillus flavus and Aspergillus parasiticus grown in liquid medium and results showed that 6PP had a good efficacy in suppression of AFB1 by 34.28–54.63%. These findings hold a promise to control pathogenic organisms and their toxicity using a lactone metabolite.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

6PP:

6-pentyl-α-pyrone

AFB1:

aflatoxin B1

LSD:

least significant difference

MBC:

minimum bactericidal concentration

MDW:

mycelial dry weight

MFC:

minimum fungicidal concentration, MIC, minimal inhibitory concentration

PDA:

potato-dextrose agar; PDB, potato-dextrose broth

SEM:

scanning electron microscopy

TEM:

transmission electron microscopy

TLC:

thin-layer chromatography

YES:

yeast-sucrose

References

  • Aala F., Yusuf U.K. & Nulit R. 2013. Electron microscopy studies of the effects of garlic extract against Trichophyton rubrum. Sains Malaysiana 42: 1585–1590.

    Google Scholar 

  • Anderson R.C., Haverkamp R.G & Yu P.L. 2004. Investigation of morphological changes to Staphylococcus aureus induced by ovine derived antimicrobial peptides using TEM and AFM. FEMS Microbiol. Lett. 240: 105–110.

    Article  CAS  PubMed  Google Scholar 

  • Benoni H., Taraz K., Korth H. & Pulverer G. 1990. Characterization of 6-pentyl-α-pyrone from the soil fungus Trichoderma koningii. Naturwissenschaften 77: 539–540.

    Article  CAS  Google Scholar 

  • Berger R.G. 1995. Aroma Biotechnology. Springer-Verlag, Berlin, Heidelberg.

    Book  Google Scholar 

  • Bonnarme P., Djian A., Latrasse A., Féron G., Ginies C., Durand A. & Le Quéré J.L. 1997. Production of 6-pentyl-α-pyrone by Trichoderma sp. from vegetable oils. J. Biotechnol. 56: 143–150.

    Article  CAS  Google Scholar 

  • Claydon N., Allan M., Hanson J.R. & Avent A.G. 1987. Antifungal alkyl pyrones of Trichoderma harzianum. Trans. Br. Mycol. Soc. 88: 503–513.

    Article  CAS  Google Scholar 

  • Collins R.P. & Halim A.F. 1972. Characterization of the major aroma constituent of the fungus Trichoderma viride (Pers.). J. Agric. Food Chem. 20: 437–438.

    Article  CAS  Google Scholar 

  • Cutler H.G., Cox R.H., Crumley F.G. & Cole P.D. 1986. 6-pentyl-α-pyrone from Trichoderma harzianum: its plant growth inhibitory and antimicrobial properties. Agric. Biol. Chem. 50: 2943–2945.

    CAS  Google Scholar 

  • Dodd S.L., Hill R.A. & Stewart A. 2000. Control of Athelia rolfsii disease on lentil seedlings using 6-pentyl-α-pyrone. Soil Biol. Biochem. 32: 1033–1034.

    Article  CAS  Google Scholar 

  • El-Hasan A., Walker F. & Buchenauer H. 2008. Trichoderma harzianum and its metabolite 6-pentyl-alpha-pyrone suppress fusaric acid produced by Fusarium moniliforme. J. Phytopathol. 156: 79–87.

    Article  CAS  Google Scholar 

  • El-Hasan A., Walker F., Schöne J. & Buchenauer H. 2007. Antagonistic effect of 6-pentyl-alpha-pyrone produced by Trichoderma harzianum toward Fusarium moniliforme. J. Plant Dis. Prot. 114: 62–68.

    Article  CAS  Google Scholar 

  • Giorgio A., De Stradis A., Lo Cantore P. & Lacobellis N.S. 2015. Biocide effects of volatile organic compounds produced by potential biocontrol rhizobacteria on Sclerotinia sclerotiorum. Front. Microbiol. 6: 1056.

    Article  PubMed  PubMed Central  Google Scholar 

  • Helal G.A., Sarhan M.M., Abu Shahla A.N.K. & Abou El-Khair E.K. 2006. Effects of Cymbopogon citratus L. essential oil on the growth, lipid content and morphogenesis of Aspergillus niger ML2-strain. J. Basic Microbiol. 46: 456–469.

    Article  CAS  PubMed  Google Scholar 

  • Hyo Y., Yamada S., Ishimatsu M., Fukutsuji K. & Harada T. 2012. Antimicrobial effects of Burow’s solution on Staphylococcus aureus and Pseudomonas aeruginosa. Med. Mol. Morphol. 45: 66–71.

    Article  PubMed  Google Scholar 

  • Ismaiel A.A., Bassyouni R.H., Kamel Z. & Gabr S.M. 2016b. Detoxification of patulin by kombucha tea culture. CyTA J. Food 14: 271–279.

    Article  CAS  Google Scholar 

  • Ismaiel A.A., Ghaly M.F. & El-Naggar A.K. 2011. Milk kefir: ultrastructure, antimicrobial activity, and efficacy on afla-toxin B1 production by Aspergillus flavus. Curr. Microbiol. 62: 1602–1609.

    Article  CAS  PubMed  Google Scholar 

  • Ismaiel A.A. & Papenbrock J. 2014. The effects of patulin from Penicillium vulpinum on seedling growth, root tip ultrastructure and glutathione content of maize. Eur. J. Plant Pathol. 139: 497–509.

    Article  CAS  Google Scholar 

  • Ismaiel, A.A. & Papenbrock, J. 2015. Mycotoxins: producing fungi and mechanisms of phytotoxicity. Agriculture 5: 492–537.

    Article  CAS  Google Scholar 

  • Ismaiel A.A., Rabie G.H. & Abd El-Aal M.A. 2016a Antimicrobial and morphogenic effects of emodin produced by Aspergillus awamori WAIR120. Biologia 71: 464–474.

    Article  CAS  Google Scholar 

  • Ismaiel A.A. & Tharwat N.A. 2014. Antifungal activity of silver ion on ultrastructure and production of aflatoxin B1 and patulin by two mycotoxigenic strains, Aspergillus flavus OC1 and Penicillium vulpinum CM1. J. Mycol. Med. 24: 193–204.

    Article  CAS  PubMed  Google Scholar 

  • Krishnamurthy Y.L. & Shashikala J. 2006. Inhibition of aflatoxin B1 production of Aspergillus flavus, isolated from soybean seeds by certain natural plant products. Lett. Appl. Microbiol. 43: 469–474.

    Article  CAS  PubMed  Google Scholar 

  • Liu X., Wang L.P., Li Y.C., Li H.Y., Yu T. & Zheng X.D. 2009. Antifungal activity of thyme oil against Geotrichum citriaurantii in vitro and in vivo. J. Appl. Microbiol. 107: 1450–1456.

    Article  CAS  PubMed  Google Scholar 

  • Metcalf D.A. & Wilson C.R. 2001. The process of antagonism of Sclerotium cepivorum in white rot affected onion roots byTrichoderma koningii. Plant Pathol. 50: 249–257.

    Article  CAS  Google Scholar 

  • Moubasher A.H. 1993. Soil Fungi in Qatar and Other Arab Countries. The Centre for Science and Applied Research, Doha, Qatar.

    Google Scholar 

  • Nisa H., Kamili A.N., Nawchoo I.A., Shafi S., Shameem N. & Bandh S.A. 2015. Fungal endophytes as prolific source of phytochemicals and other bioactive natural products: a review. Microb. Pathog. 82: 50–59.

    Article  CAS  PubMed  Google Scholar 

  • Nobuhara A. 1969. Unsaturated lactones. III. Flavorous nature of some δ-decalactones having the double bond at various sites. Agric. Biol. Chem. 33: 1264.

    CAS  Google Scholar 

  • Oda S., Isshiki K. & Ohashi S. 2009. Production of 6-pentyl-α-pyrone with Trichoderma atroviride and its mutant in a novel extractive liquid-surface immobilization (Ext-LSI) system. Process Biochem. 44: 625–630.

    Article  CAS  Google Scholar 

  • Parker S.R., Cutler H.G., Jacyno J.M. & Hill R.A. 1997. Biological activity of 6-pentyl-2H-pyran-2-one and its analogs. J. Agric. Food Chem. 45: 2774–2776.

    Article  CAS  Google Scholar 

  • Poole P.R. & Whitaker G. 1997. Biotransformation of 6-pentyl-2-pyrone by Botrytis cinerea in liquid cultures. J. Agric. Food Chem. 45: 249–252.

    Article  CAS  Google Scholar 

  • Ramos A.S., Fiaux S.B. & Leite S.G.F. 2008. Production of 6-pentyl-α-pyrone by Trichoderma harzianum in solid-state fermentation. Braz. J. Microbiol. 39: 712–717.

    Article  Google Scholar 

  • Santos L., Marin S., Sanchis V. & Ramos A.J. 2011. In vitro effect of some fungicides on growth and aflatoxins production by Aspergillus flavus isolated from Capsicum powder. Food Addit. Contam. Part A Chem. Anal. Control Expo. Risk Assess. 28: 98–106.

    Article  CAS  Google Scholar 

  • Scarselletti R. & Faull J.L. 1994. In vitro activity of 6-pentyl-α-pyrone, a metabolite of Trichoderma harzianum, in the inhibition of Rhizoctonia solani and Fusarium oxysporum f. sp. lycopersici. Mycol. Res. 98: 1207–1209.

    Article  CAS  Google Scholar 

  • Serrano-Carreon L., Hathout Y., Bensoussan M. & Belin J.M. 1993. Metabolism of linoleic acid or mevalonate and 6-pentyl-α-pyrone biosynthesis by Trichoderma species. Appl. Environ. Microbiol. 59: 2945–2950.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sharma D., Pramanik A. & Agrawal P.K. 2016. Evaluation of bioactive secondary metabolites from endophytic fungus Pestalotiopsis neglecta BAB-5510 isolated from leaves of Cupressus torulosa D.Don. 3 Biotech. 6: 210.

    Article  PubMed  PubMed Central  Google Scholar 

  • Simon A., Dunlop R.W., Ghisalberti E.L. & Sivasithamparam K. 1988. Trichoderma koningii produces a pyrone compound with antibiotic properties. Soil Biol. Biochem. 20: 263–264.

    Article  CAS  Google Scholar 

  • Sivasithamparam K. & Ghisalberti E.L. 1998. Secondary metabolism in Trichoderma and Gliocladium, Vol. 1, pp: 139–191. In: Kubicek C.P. & Harman G.E. (eds) Trichoderma and Gliocladium, Taylor and Francis, London.

    CAS  Google Scholar 

  • Tahir H.A.S., Gu Q., Wu H., Niu Y., Huo R. & Gao X. 2017. Bacillus volatiles adversely affect the physiology and ultra-structure of Ralstonia solanacearum and induce systemic resistance in tobacco against bacterial wilt. Sci. Rep. 7: 40481.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Walter M., Boyd-Wilson K.S.H., Perry J.H. & Hill R.A. 2000. Botrytis tolerance to 6-pentyl-α-pyrone and massoialactone. N. Z. Plant Prot. 53: 375–381.

    CAS  Google Scholar 

  • Worasatit N., Sivasithamparam K., Ghisalberti E.L. & Rowland C. 1994. Variation in pyrone production, lytic enzymes and control of Rhizoctonia root rot of wheat among single-spore isolates of Trichoderma koningii. Mycol Res. 98: 1357–1363.

    Article  CAS  Google Scholar 

  • Wurz R.E.M., Kepner R.E. & Weeb A.D. 1988. The biosynthesis of certain gamma-lactones from glutamic acid by film yeast activity on the surface of flour sherry. Am. J. Enol. Vitic. 39: 234–238.

    CAS  Google Scholar 

  • Xiao-Yan S., Qing-Tao S., Shu-Tao X., Xiu-Lan C., Cai-Yun S. & Yu-Zhong Z. 2006. Broad-spectrum antimicrobial activity and high stability of trichokonins from Trichoderma koningii SMF2 against plant pathogens. FEMS Microbiol. Lett. 260: 119–125.

    Article  PubMed  CAS  Google Scholar 

  • Yoshida S., Kasuga S., Hayashi N., Ushiroguchui T., Matsuura H. & Nakagawa S. 1987. Antifungal activity of ajoene derived from garlic. Appl. Environ. Microbiol. 53: 615–617.

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Botany and Microbiology, Faculty of Science, Zagazig University, Zagazig, 44519, Egypt

    Ahmed A. Ismaiel

  2. Department of Botany and Microbiology, Faculty of Science, Cairo University, Cairo, Egypt

    Dalia M. I. Ali

Authors
  1. Ahmed A. Ismaiel
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Dalia M. I. Ali
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ahmed A. Ismaiel.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ismaiel, A.A., Ali, D.M.I. Antimicrobial properties of 6-pentyl-α-pyrone produced by endophytic strains of Trichoderma koningii and its effect on aflatoxin B1 production. Biologia 72, 1403–1415 (2017). https://doi.org/10.1515/biolog-2017-0173

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1515/biolog-2017-0173

Key words

Search

Navigation