Skip to main content
SpringerLink
Log in

Biological control of aflatoxin-producing Aspergillus flavus by volatile organic compound-producing antagonistic yeasts

  • Published:
BioControl Aims and scope Submit manuscript

A Correction to this article was published on 07 February 2020

This article has been updated

Abstract

Aspergillus spp. are the most common phytopathogenic fungi able to produce various types of aflatoxins. Yeasts can produce volatile organic compounds (VOCs) that may be used as biocontrol agents against mycotoxigenic fungi. In this study, we aimed to evaluate antagonistic yeasts that are potentially capable of producing active VOCs against the aflatoxin-producing fungus, Aspergillus flavus A39. In total, 366 epiphytic and endophytic yeast strains isolated from leaves of rice, sugarcane, and corn in Thailand were screened for their potential. Only 49 yeast strains were able to produce antifungal volatile organic compounds (VOCs). Candida nivariensis DMKU-CE18 was the most effective yeast strain to inhibit the mycelium growth (64.9 ± 7.0% inhibition) and conidial germination (49.3 ± 3.3% inhibition) of A. flavus A39, and to reduce aflatoxin production (74.8 ± 6.5% reduction) in corn grains. The analysis results of headspace gas chromatography/mass spectrometry (GC/MS) revealed that the major VOC produced by this yeast strain was closest to 1-pentanol.

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

Fig. 1

Similar content being viewed by others

Change history

  • 07 February 2020

    In the original article, in the last sentence of the subsection 'Efficacy of VOC-producing yeasts on fungal conidial germination inhibition' in Materials and Methods, it should have read "3 = germ tube 2x to 4x" instead of "3 = germ tube 24x to 4x".

References

  • Afsah-Hejri L (2013) Saprophytic yeasts: effective biocontrol agents against Aspergillus flavus. Int Food Res J 20:3403–3409

    Google Scholar 

  • Aidoo K (1993) Post-harvest storage and preservation of tropical crops. Int Biodeterior Biodegrad 32(1–3):161–173

    Article  Google Scholar 

  • Alcoba-Flórez J, Méndez-Álvarez S, Cano J, Guarro J, Pérez-Roth E, del Pilar Arévalo M (2005) Phenotypic and molecular characterization of Candida nivariensis sp. nov., a possible new opportunistic fungus. J Clin Microbiol 43(8):4107–4111

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Amaike S, Keller NP (2011) Aspergillus flavus. Annu Rev Phytopathol. 49:107–133

    Article  CAS  PubMed  Google Scholar 

  • Arrarte E, Garmendia G, Rossini C, Wisniewski M, Vero S (2017) Volatile organic compounds produced by Antarctic strains of Candida sake play a role in the control of postharvest pathogens of apples. Biol Control 109:14–20

    Article  CAS  Google Scholar 

  • Borman AM, Petch R, Linton CJ, Palmer MD, Bridge PD, Johnson EM (2008) Candida nivariensis, an emerging pathogenic fungus with multidrug resistance to antifungal agents. J Clin Microbiol 46:933–938

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bu'Lock JD (1980) Mycotoxins as secondary metabolites. In: Steyn PS (ed) The biosynthesis of mycotoxins: a study in secondary metabolism. Academic Press, New York, pp 1–16

    Chapter  Google Scholar 

  • Çelýk K, Denlý M, Savas T (2003) Reduction of toxic effects of aflatoxin B1 by using baker yeast (Saccharomyces cerevisiae) in growing broiler chicks diets. R Bras Zootec 32(3):615–619

    Article  Google Scholar 

  • Chen P-H, Chen R-Y, Chou J-Y (2018) Screening and evaluation of yeast antagonists for biological control of Botrytis cinerea on strawberry fruits. Mycobiology 46(1):33–46

    Article  PubMed  PubMed Central  Google Scholar 

  • Chinaphuti A, Trikarunasawat C, Wongurai A, Kositcharoenkul S (2002) Production of in-house ELISA test kit for detection of aflatoxin in agricultural commodities and their validations. Kasetsart J (Nat Sci) 36:179–186

    CAS  Google Scholar 

  • Comitini F, Ciani M (2010) The zymocidial activity of Tetrapisispora phaffii in the control of Hanseniaspora uvarum during the early stages of winemaking. Lett Appl Microbiol 50(1):50–56

    Article  CAS  PubMed  Google Scholar 

  • Farbo MG, Urgeghe PP, Fiori S, Marcello A, Oggiano S, Balmas V, Hassan ZU, Jaoua S, Migheli Q (2018) Effect of yeast volatile organic compounds on ochratoxin A-producing Aspergillus carbonarius and A. ochraceus. Int J Food Microbiol 284:1–10

    Article  CAS  PubMed  Google Scholar 

  • Figueiredo-Carvalho MH, Ramos Lde S, Barbedo LS, Chaves AL, Muramoto IA, Santos AL, Almeida-Paes R, Zancopé-Oliveira RM (2016) First description of Candida nivariensis in Brazil: antifungal susceptibility profile and potential virulence attributes. Mem Inst Oswaldo Cruz 111:51–58

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fujita S, Senda Y, Okusi T, Ota Y, Takada H, Yamada K, Kawano M (2007) Catheter-related fungemia due to fluconazole-resistant Candida nivariensis. J Clin Microbiol 45:3459–3461

    Article  PubMed  PubMed Central  Google Scholar 

  • Gong A-D, Li H-P, Shen L, Zhang J-B, Wu A-B, He W-J, Yuan Q-S, He J-D, Liao Y-C (2015) The Shewanella algae strain YM8 produces volatiles with strong inhibition activity against Aspergillus pathogens and aflatoxins. Front Microbiol 6:1091

    Article  PubMed  PubMed Central  Google Scholar 

  • Gotor-Vila A, Teixidó N, Di Francesco A, Usall J, Ugolini L, Torres R, Mari M (2017) Antifungal effect of volatile organic compounds produced by Bacillus amyloliquefaciens CPA-8 against fruit pathogen decays of cherry. Food Microbiol 64:219–225

    Article  CAS  PubMed  Google Scholar 

  • Grzegorczyk M, Żarowska B, Restuccia C, Cirvilleri G (2017) Postharvest biocontrol ability of killer yeasts against Monilinia fructigena and Monilinia fructicola on stone fruit. Food Microbiol 61:93–101

    Article  PubMed  Google Scholar 

  • Guchi E (2015) Implication of aflatoxin contamination in agricultural products. Am J Food Nutr 3(1):12–20

    CAS  Google Scholar 

  • Hua S-ST, Baker JL, Flores-Espiritu M (1999) Interactions of saprophytic yeasts with a nor mutant of Aspergillus flavus. Appl Environ Microbiol 65(6):2738–2740

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hua S-ST, Beck JJ, Sarreal SBL, Gee W (2014) The major volatile compound 2-phenylethanol from the biocontrol yeast, Pichia anomala, inhibits growth and expression of aflatoxin biosynthetic genes of Aspergillus flavus. Mycotoxin Res 30(2):71–78

    Article  CAS  PubMed  Google Scholar 

  • Huang R, Li G, Zhang J, Yang L, Che H, Jiang D, Huang H (2011) Control of postharvest Botrytis fruit rot of strawberry by volatile organic compounds of Candida intermedia. Phytopathology 101(7):859–869

    Article  CAS  PubMed  Google Scholar 

  • Huang R, Che H, Zhang J, Yang L, Jiang D, Li G (2012) Evaluation of Sporidiobolus pararoseus strain YCXT3 as biocontrol agent of Botrytis cinerea on post-harvest strawberry fruits. Biol Control 62(1):53–63

    Article  Google Scholar 

  • Ismail A, Bedell GW, Lupan DM (1985) Siderophore production by the pathogenic yeast Candida albicans. Biochem Biophys Res Commun 130(2):885–891

    Article  CAS  PubMed  Google Scholar 

  • Janisiewicz W, Korsten L (2002) Biological control of postharvest diseases of fruits. Annu Rev Phytopathol 40:411–441

    Article  CAS  PubMed  Google Scholar 

  • Khunnamwong P, Jindamorakot S, Limtong S (2018) Endophytic yeast diversity in leaf tissue of rice, corn and sugarcane cultivated in Thailand assessed by a culture-dependent approach. Fungal Biol. 122(8):785–799

    Article  PubMed  Google Scholar 

  • Leelasuphakul W, Hemmanee P, Chuenchitt S (2008) Growth inhibitory properties of Bacillus subtilis strains and their metabolites against the green mold pathogen (Penicillium digitatum Sacc.) of citrus fruit. Postharvest Biol Technol 48(1):113–121

    Article  CAS  Google Scholar 

  • Limtong S, Nasanit R (2017) Phylloplane yeasts in tropical climates. In: Buzzini P, Lachance MA, Yurkov A (eds) Yeasts in natural ecosystems: diversity. Springer, Cham, pp 199–223

    Chapter  Google Scholar 

  • Magan N, Hope R, Cairns V, Aldred D (2003) Post-harvest fungal ecology: impact of fungal growth and mycotoxin accumulation in stored grain. In: Xu X, Bailey JA, Cooke BM (eds) Epidemiology of mycotoxin producing fungi. Springer, Dordrecht, pp 723–730

    Chapter  Google Scholar 

  • Mannaa M, Kim KD (2016) Microbe-mediated control of mycotoxigenic grain fungi in stored rice with focus on aflatoxin biodegradation and biosynthesis inhibition. Mycobiology 44(2):67–78

    Article  PubMed  PubMed Central  Google Scholar 

  • Masoud W, Kaltoft CH (2006) The effects of yeasts involved in the fermentation of Coffea arabica in East Africa on growth and ochratoxin A (OTA) production by Aspergillus ochraceus. Int J Food Microbiol 106(2):229–234

    Article  CAS  PubMed  Google Scholar 

  • Masoud W, Poll L, Jakobsen M (2005) Influence of volatile compounds produced by yeasts predominant during processing of Coffea arabica in East Africa on growth and ochratoxin A (OTA) production by Aspergillus ochraceus. Yeast 22(14):1133–1142

    Article  CAS  PubMed  Google Scholar 

  • Mends MT, Yu E, Strobel GA, Riyaz S, Booth E, Geary B, Sears J, Taatjes C, Hadi M (2012) An endophytic Nodulisporium sp. producing volatile organic compounds having bioactivity and fuel potential. J Pet Environ Biotechnol 3(3):117

    CAS  Google Scholar 

  • Min W-K, Kweon D-H, Park K, Park Y-C, Seo J-H (2011) Characterisation of monoclonal antibody against aflatoxin B1 produced in hybridoma 2C12 and its single-chain variable fragment expressed in recombinant Escherichia coli. Food Chem 126(3):1316–1323

    Article  CAS  Google Scholar 

  • Moss M (1998) Recent studies of mycotoxins. J Appl Microbiol 84:62S–76S

    Article  Google Scholar 

  • Oro L, Feliziani E, Ciani M, Romanazzi G, Comitini F (2018) Volatile organic compounds from Wickerhamomyces anomalus, Metschnikowia pulcherrima and Saccharomyces cerevisiae inhibit growth of decay causing fungi and control postharvest diseases of strawberries. Int J Food Microbiol 265:18–22

    Article  CAS  PubMed  Google Scholar 

  • Parafati L, Vitale A, Restuccia C, Cirvilleri G (2017) Performance evaluation of volatile organic compounds by antagonistic yeasts immobilized on hydrogel spheres against gray, green and blue postharvest decays. Food Microbiol 63:191–198

    Article  CAS  PubMed  Google Scholar 

  • Payne C, Bruce A, Staines H (2000) Yeast and bacteria as biological control agents against fungal discolouration of Pinus sylvestris blocks in laboratory-based tests and the role of antifungal volatiles. Holzforschung 54(6):563–569

    Article  CAS  Google Scholar 

  • Petersson S, Schnürer J (1995) Biocontrol of mold growth in high-moisture wheat stored under airtight conditions by Pichia anomala, Pichia guilliermondii and Saccharomyces cerevisiae. Appl Environ Microbiol 61(3):1027–1032

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ponsone ML, Chiotta ML, Combina M, Dalcero A, Chulze S (2011) Biocontrol as a strategy to reduce the impact of ochratoxin A and Aspergillus section Nigri in grapes. Int J Food Microbiol 151(1):70–77

    Article  PubMed  Google Scholar 

  • Raspor P, Miklič-Milek D, Avbelj M, Čadež N (2010) Biocontrol of grey mould disease on grape caused by Botrytis cinerea with autochthonous wine yeasts. Food Technol Biotechnol 48(3):336–343

    CAS  Google Scholar 

  • Rezende DC, Fialho MB, Brand SC, Blumer S, Pascholati SF (2015) Antimicrobial activity of volatile organic compounds and their effect on lipid peroxidation and electrolyte loss in Colletotrichum gloeosporioides and Colletotrichum acutatum mycelia. Afr J Microbiol Res 9(23):1527–1535

    Article  CAS  Google Scholar 

  • Rosa MM, Tauk-Tornisielo SM, Rampazzo PE, Ceccato-Antonini SR (2010) Evaluation of the biological control by the yeast Torulaspora globosa against Colletotrichum sublineolum in sorghum. World J Microbiol Biotechnol 26(8):1491–1502

    Article  Google Scholar 

  • Spadaro D, Gullino ML (2004) State of the art and future prospects of the biological control of postharvest fruit diseases. Int J Food Microbiol 91(2):185–194

    Article  PubMed  Google Scholar 

  • Srisuk N, Nutaratat P, Surussawadee J, Limtong S (2019) Yeast communities in sugarcane phylloplane. Microbiology 88(3):353–369

    Article  CAS  Google Scholar 

  • Suwannarach N, Kaewyana C, Yodmeeklin A, Kumla J, Matsui K, Lumyong S (2017) Evaluation of Muscodor cinnamomi as an egg biofumigant for the reduction of microorganisms on eggshell surfaces and its effect on egg quality. Int J Food Microbiol 244:52–61

    Article  CAS  PubMed  Google Scholar 

  • Toffano L, Fialho MB, Pascholati SF (2017) Potential of fumigation of orange fruits with volatile organic compounds produced by Saccharomyces cerevisiae to control citrus black spot disease at postharvest. Biol Control 108:77–82

    Article  CAS  Google Scholar 

  • Türker M (2014) Yeast biotechnology: diversity and applications. In: 27th VH yeast conference: advances in science and industrial production of baker’s yeast, Istanbul, 14–15 April 2014, pp 1–26

  • Velmourougane K, Bhat R, Gopinandhan T, Panneerselvam P (2011) Management of Aspergillus ochraceus and ochratoxin-A contamination in coffee during on-farm processing through commercial yeast inoculation. Biol Control 57(3):215–221

    Article  Google Scholar 

  • Waenlor W, Wiwanitkit V (2003) Aflatoxin contamination of food and food products in Thailand: an overview. Southeast Asian J Trop Med Public Health 34:184–190

    CAS  PubMed  Google Scholar 

  • Waliyar F, Umeh V, Traore A, Osiru M, Ntare B, Diarra B, Kodio O, Kumar KVK, Sudini H (2015) Prevalence and distribution of aflatoxin contamination in groundnut (Arachis hypogaea L.) in Mali, West Africa. Crop Prot 70:1–7

    Article  CAS  Google Scholar 

  • Wilson CL, Pusey P (1985) Potential for biological control of postharvest plant diseases. Plant Dis 69(5):375–378

    Article  Google Scholar 

  • World Health Organization (2018) Aflatoxin. In: Food safety digest. DIALOG. https://www.who.int/foodsafety/FSDigest_Aflatoxins_EN.pdf?fbclid=IwAR23wb_6iGDd-MFJVJKRXTM11qEK7_n9BSw4QZr89yTocEpUlxqpVoNt5T8. Cited 31 July 2018

  • Zain ME (2011) Impact of mycotoxins on humans and animals. J Saudi Chem Soc 15(2):129–144

    Article  CAS  Google Scholar 

  • Zeidan R, Ul-Hassan Z, Al-Thani R, Balmas V, Jaoua S (2018) Application of low-fermenting yeast Lachancea thermotolerans for the control of toxigenic fungi Aspergillus parasiticus, Penicillium verrucosum and Fusarium graminearum and their mycotoxins. Toxins 10(6):242

    Article  PubMed Central  CAS  Google Scholar 

  • Zhou Y, Li W, Zeng J, Shao Y (2018) Mechanisms of action of the yeast Debaryomyces nepalensis for control of the pathogen Colletotrichum gloeosporioides in mango fruit. Biol Control 123:111–119

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the Thailand Research Fund (TRF) through the TRF Research-Team Promotion Grant (RTA 6080004). The authors would like to thank Dr Amara Chinaphuti, Department of Agriculture (DOA), Thailand, for providing Aspergillus flavus A39.

Author information

Authors and Affiliations

  1. Department of Biotechnology, Faculty of Engineering and Industrial Technology, Silpakorn University, Sanamchandra Palace Campus, Nakhon Pathom, 73000, Thailand

    Sopin Jaibangyang & Rujikan Nasanit

  2. Department of Microbiology, Faculty of Science, Kasetsart University, Jatujak, Bangkok, 10900, Thailand

    Savitree Limtong

  3. Academy of Science, The Royal Society of Thailand, Bangkok, 10300, Thailand

    Savitree Limtong

Authors
  1. Sopin Jaibangyang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rujikan Nasanit
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Savitree Limtong
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rujikan Nasanit.

Ethics declarations

Conflicts of interest

The authors declare that there are no conflicts of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Handling Editor: Jane Debode

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (DOC 105 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jaibangyang, S., Nasanit, R. & Limtong, S. Biological control of aflatoxin-producing Aspergillus flavus by volatile organic compound-producing antagonistic yeasts. BioControl 65, 377–386 (2020). https://doi.org/10.1007/s10526-020-09996-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10526-020-09996-9

Keywords

Search

Navigation