Skip to main content
SpringerLink
Log in

Effects of temperature and relative humidity on Aflatoxin B1 reduction in corn grains and antagonistic activities against Aflatoxin-producing Aspergillus flavus by a volatile organic compound-producing yeast, Kwoniella heveanensis DMKU-CE82

  • Published:
BioControl Aims and scope Submit manuscript

This article has been updated

Abstract

As shown in our previous study, Kwoniella heveanensis DMKU-CE82, a volatile organic compound (VOC)-producing yeast, demonstrated promising antagonistic activity against aflatoxin-producing strain of Aspergillus flavus. This yeast’s volatile organic compounds (VOCs) could reduce Aflatoxin B1 (AFB1) in corn grains. In the current study, we evaluated the effect of temperatures and relative humidity on AFB1 reduction during grain storage when co-incubated with this VOC-producing yeast. The VOCs produced by K. heveanensis DMKU-CE82 could promote reduction of AFB1 to less than 20 part per billion (ppb) in the fungal contaminated corn grains under most storage conditions at 35 °C. The major VOCs produced by 2-, 4-, and 6-day-old yeast cultures were closely matched to 3-methyl-1-butanol, 2-methyl-1-butanol, hydrazine-1-1-dimethyl, and butanoic acid-3-methyl. In addition, this yeast strain had the ability to produce β-1,3-glucanase, amylase, cellulase, chitinase, siderophores, and biofilms. Scanning electron microscopy also confirmed the antagonistic activity of K. heveanensis DMKU-CE82 as it caused structural damage to conidia and inhibited the development of mycelia and conidiophores in both direct fungal–yeast interaction and the VOC method in corn grains. These results demonstrated that this yeast strain could be a promising biocontrol agent against aflatoxin-producing fungi in agricultural products.

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.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Change history

  • 09 April 2021

    The original version of this article has been revised: A missing supplementary file has been added.

References

  • Abdallah MF, Ameye M, De Saeger S, Audenaert K, Haesaert G (2018) Biological control of mycotoxigenic fungi and their toxins: an update for the pre-harvest approach. In: Njobeh PB (ed) Mycotoxins-impact and management strategies. IntechOpen Ltd, London, pp 59–89

    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 

  • Bajaj BK, Raina S, Singh S (2013) Killer toxin from a novel killer yeast Pichia kudriavzevii RY55 with idiosyncratic antibacterial activity. J Basic Microbiol 53:645–656

    Article  CAS  PubMed  Google Scholar 

  • Bar-Shimon M, Yehuda H, Cohen L, Weiss B, Kobeshnikov A, Daus A, Goldway M, Wisniewski M, Droby S (2004) Characterization of extracellular lytic enzymes produced by the yeast biocontrol agent Candida oleophila. Curr Genet 45:140–148

    Article  CAS  PubMed  Google Scholar 

  • Beuchat LR (1983) Influence of water activity on growth, metabolic activities and survival of yeasts and molds. J Food Prot 46:135–141

    Article  PubMed  Google Scholar 

  • Boller R, Schroeder H (1974) Influence of relative humidity on production of aflatoxin in rice by Aspergillus parasiticus. Phytopathology 64:17–21

    Article  CAS  Google Scholar 

  • Bovo F, Corassin CH, Rosim RE, de Oliveira CA (2013) Efficiency of lactic acid bacteria strains for decontamination of Aflatoxin M1 in phosphate buffer saline solution and in skimmed milk. Food Bioprocess Tech 6:2230–2234

    Article  CAS  Google Scholar 

  • Calvente V, de Orellano MAE, Sansone G, Benuzzi D, de Tosetti MIS (2001) A simple agar plate assay for screening siderophore producer yeasts. J Microbiol Methods 47:273–279

    Article  CAS  PubMed  Google Scholar 

  • Carrasco M, Villarreal P, Barahona S, Alcaíno J, Cifuentes V, Baeza M (2016) Screening and characterization of amylase and cellulase activities in psychrotolerant yeasts. BMC Microbiol 16:21

    Article  PubMed  PubMed Central  Google Scholar 

  • Creppy EE (2002) Update of survey, regulation and toxic effects of mycotoxins in Europe. Toxicol Lett 127:19–28

    Article  CAS  PubMed  Google Scholar 

  • Devereau A, Myhara R, Anderson C (2002) Physical factors in post-harvest quality. In: Golob P (ed) Crop post-harvest: science and technology. Blackwell Science Ltd, Hoboken, New Jersey, pp 69–92

    Chapter  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 

  • Fiori S, Urgeghe PP, Hammami W, Razzu S, Jaoua S, Migheli Q (2014) Biocontrol activity of four non- and low-fermenting yeast strains against Aspergillus carbonarius and their ability to remove ochratoxin A from grape juice. Int J Food Microbiol 189:45–50

    Article  CAS  PubMed  Google Scholar 

  • Food and Agriculture Organization (2003) Mycotoxin. In: Worldwide limits for aflatoxins. http://www.fao.org/3/a-y5499e.pdf. Accessed 20 Jan 2021

  • Giobbe S, Marceddu S, Scherm B, Zara G, Mazzarello VL, Budroni M, Migheli Q (2007) The strange case of a biofilm-forming strain of Pichia fermentans, which controls Monilinia brown rot on apple but is pathogenic on peach fruit. FEMS Yeast Res 7:1389–1398

    Article  CAS  PubMed  Google Scholar 

  • Giorni P, Leggieri MC, Magan N, Battilani P (2012) Comparison of temperature and moisture requirements for sporulation of Aspergillus flavus sclerotia on natural and artificial substrates. Fungal Biol 116:637–642

    Article  PubMed  Google Scholar 

  • Giorni P, Magan N, Pietri A, Battilani P (2011) Growth and aflatoxin production of an Italian strain of Aspergillus flavus: influence of ecological factors and nutritional substrates. World Mycotoxin J 4:425–432

    Article  CAS  Google Scholar 

  • Gonzales HB, Armstrong PR, Maghirang RG (2009) Simultaneous monitoring of stored grain with relative humidity, temperature, and carbon dioxide sensors. Appl Eng Agric 25:595–604

    Article  Google Scholar 

  • Greenspan L (1977) Humidity fixed points of binary saturated aqueous solutions. J Res Natl Bur Stand 81:89–96

    Article  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 

  • Hu Q, Xu J (2011) A simple double-layered chrome azurol S agar (SD-CASA) plate assay to optimize the production of siderophores by a potential biocontrol agent Bacillus. Afr J Microbiol Res 5:4321–4327

    CAS  Google Scholar 

  • Hua SST, 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 30:71–78

    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 101:859–869

    Article  CAS  PubMed  Google Scholar 

  • Jaibangyang S, Nasanit R, Limtong S (2020) Biological control of aflatoxin-producing Aspergillus flavus by volatile organic compound-producing antagonistic yeasts. BioControl 65:377–386

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Janisiewicz WJ, Leverentz B, Conway WS, Saftner RA, Reed A, Camp MJ (2003) Control of bitter rot and blue mold of apples by integrating heat and antagonist treatments on 1-MCP treated fruit stored under controlled atmosphere conditions. Postharvest Biol Technol 29:129–143

    Article  CAS  Google Scholar 

  • Kaaya AN, Kyamuhangire W (2006) The effect of storage time and agroecological zone on mould incidence and aflatoxin contamination of maize from traders in Uganda. Int J Food Microbiol 110:217–223

    Article  CAS  PubMed  Google Scholar 

  • Kabak B, Dobson AD, Var I (2006) Strategies to prevent mycotoxin contamination of food and animal feed: a review. Crit Rev Food Sci Nutr 46:593–619

    Article  CAS  PubMed  Google Scholar 

  • Kheiralla ZH, Hassanin NI, Amra H (1992) Effect of incubation time, temperature and substrate on growth and aflatoxin production. Int Biodeter Biodegr 30:17–27

    Article  CAS  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 122:785–799

    Article  PubMed  Google Scholar 

  • Kurtzman CP, Droby S (2001) Metschnikowia fructicola, a new ascosporic yeast with potential for biocontrol of postharvest fruit rots. Syst Appl Microbiol 24:395–399

    Article  CAS  PubMed  Google Scholar 

  • Lawrence J, Maier DE (2011) Aeration strategy simulations for wheat storage in the sub-tropical region of north India. Trans ASABE 54:1395–1405

    Article  Google Scholar 

  • Lopes MR, Klein MN, Ferraz LP, da Silva AC, Kupper KC (2015) Saccharomyces cerevisiae: a novel and efficient biological control agent for Colletotrichum acutatum during pre-harvest. Microbiol Res 175:93–99

    Article  PubMed  Google Scholar 

  • Lyu A, Yang L, Wu M, Zhang J, Li G (2020) High efficacy of the volatile organic compounds of Streptomyces yanglinensis 3–10 in suppression of Aspergillus contamination on peanut kernels. Front Microbiol 11:142

    Article  PubMed  PubMed Central  Google Scholar 

  • Magan N, Lacey J (1984) Effect of temperature and pH on water relations of field and storage fungi. Trans Br Mycol Soc 82:71–81

    Article  Google Scholar 

  • Mannaa M, Kim KD (2018) Effect of temperature and relative humidity on growth of Aspergillus and Penicillium spp. and biocontrol activity of Pseudomonas protegens AS15 against Aflatoxigenic Aspergillus flavus in stored rice grains. Mycobiology 46:287–295

    Article  PubMed  PubMed Central  Google Scholar 

  • Marín S, Companys E, Sanchis V, Ramos A, Magan N (1998) Effect of water activity and temperature on competing abilities of common maize fungi. Mycol Res 102:959–964

    Article  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 22:1133–1142

    Article  CAS  PubMed  Google Scholar 

  • Mayer FL, Wilson D, Hube B (2013) Candida albicans pathogenicity mechanisms. Virulence 4:119–128

    Article  PubMed  PubMed Central  Google Scholar 

  • Mishra H, Das C (2003) A review on biological control and metabolism of aflatoxin. Crit Rev Food Sci Nutr 43:245–264

    Article  CAS  PubMed  Google Scholar 

  • Montross JE, Montross MD, Bakker-Arkema FW (1999) Grain storage. In: Bakker-Arkema FW (ed) CIGR handbook of agricultural engineering. American Society of Agricultural Engineering, St. Joseph, Michigan, pp 46–59

    Google Scholar 

  • Mousa W, Ghazali FM, Jinap S, Ghazali HM, Radu S (2013) Modeling growth rate and assessing aflatoxins production by Aspergillus flavus as a function of water activity and temperature on polished and brown rice. J Food Sci 78:M56–M63

    Article  CAS  PubMed  Google Scholar 

  • Northolt MD, van Egmond HP, Paulsch WE (1977) Differences between Aspergillus flavus strains in growth and aflatoxin B1 production in relation to water activity and temperature. J Food Prot 40:778–781

    Article  CAS  PubMed  Google Scholar 

  • Ogundero VW (1987) Temperature and aflatoxin production by Aspergillus flavus and A. parasiticus strains from Nigerian groundnuts. J Basic Microbiol 27:511–514

    Article  CAS  PubMed  Google Scholar 

  • Panrapee I, Phakpoom K, Thanapoom M, Nampeung A, Warapa M (2016) Exposure to Aflatoxin B1 in Thailand by consumption of brown and color rice. Mycotoxin Res 32:19–25

    Article  CAS  PubMed  Google Scholar 

  • Parafati L, Cirvilleri G, Restuccia C, Wisniewski M (2017) Potential role of exoglucanase genes (WaEXG1 and WaEXG2) in the biocontrol activity of Wickerhamomyces anomalus. Microb Ecol 73:876–884

    Article  CAS  PubMed  Google Scholar 

  • Pratiwi C, Rahayu W, Lioe H, Herawati D, Broto W, Ambarwati S (2015) The effect of temperature and relative humidity for Aspergillus flavus BIO 2237 growth and aflatoxin production on soybeans. Int Food Res J 22:82–87

    CAS  Google Scholar 

  • Pretscher J, Fischkal T, Branscheidt S, Jäger L, Kahl S, Schlander M, Thines E, Claus H (2018) Yeasts from different habitats and their potential as biocontrol agents. Fermentation 4:31

    Article  Google Scholar 

  • Rehman ZU, Habib F, Zafar S (2002) Nutritional changes in maize (Zea mays) during storage at three temperatures. Food Chem 77:197–201

    Article  CAS  Google Scholar 

  • Schwyn B, Neilands J (1987) Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160:47–56

    Article  CAS  PubMed  Google Scholar 

  • Shah WH, Rehman ZU, Kausar T, Hussain A (2002) Storage of wheat with ears. Pakistan J Agric Res 17:206–209

    Google Scholar 

  • Souza CP, Burbano-Rosero EM, Almeida BC, Martins GG, Albertini LS, Rivera IN (2009) Culture medium for isolating chitinolytic bacteria from seawater and plankton. World J Microbiol Biotechnol 25:2079–2082

    Article  Google Scholar 

  • Spadaro D, Droby S (2016) Development of biocontrol products for postharvest diseases of fruit: the importance of elucidating the mechanisms of action of yeast antagonists. Trends Food Sci Tech 47:39–49

    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 

  • Williams R, McDonald D (1983) Grain molds in the tropics: problems and importance. Ann Rev of Phytopathol 21:153–178

    Article  Google Scholar 

  • Wright S, Linton C, Edwards R, Drury E (1991) Isoamyl alcohol (3-methyl-1-butanol), a volatile anti-cyanobacterial and phytotoxic product of some Bacillus spp. Lett Appl Microbiol 13:130–132

    Article  CAS  Google Scholar 

  • Zajc J, Gostinčar C, Černoša A, Gunde-Cimerman N (2019) Stress-tolerant yeasts: opportunistic pathogenicity versus biocontrol potential. Genes 10:42

    Article  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors would like to thank Dr. Amara Chinaphuti, Department of Agriculture (DOA), Thailand, for providing Aspergillus flavus A39.

Funding

This work was supported by the Thailand Research Fund (TRF) through the TRF Research-Team Promotion Grant (RTA 6080004).

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 authors

Correspondence to Rujikan Nasanit or Savitree Limtong.

Ethics declarations

Conflict of interest

The authors have no conflicts of interest to declare that are relevant to the content of this article.

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.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 189 kb)

Supplementary file2 (PDF 73 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. Effects of temperature and relative humidity on Aflatoxin B1 reduction in corn grains and antagonistic activities against Aflatoxin-producing Aspergillus flavus by a volatile organic compound-producing yeast, Kwoniella heveanensis DMKU-CE82. BioControl 66, 433–443 (2021). https://doi.org/10.1007/s10526-021-10082-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10526-021-10082-x

Keywords

Search

Navigation