Microbiology and Biotechnology Letters (한국미생물·생명공학회지)

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
권호 표지
DOI QR코드

DOI QR Code

Screening of Volatile Organic Compound-Producing Yeasts and Yeast-Like Fungi against Aflatoxigenic Aspergillus flavus

  • Nasanit, Rujikan (Department of Biotechnology, Faculty of Engineering and Industrial Technology, Silpakorn University, Sanamchandra Palace Campus) ;
  • Jaibangyang, Sopin (Department of Biotechnology, Faculty of Engineering and Industrial Technology, Silpakorn University, Sanamchandra Palace Campus) ;
  • Onwibunsiri, Tikamporn (Department of Food Technology, Faculty of Engineering and Industrial Technology, Silpakorn University, Sanamchandra Palace Campus) ;
  • Khunnamwong, Pannida (Department of Microbiology, Faculty of Science, Kasetsart University)
  • Received : 2022.02.07
  • Accepted : 2022.04.25
  • Published : 2022.06.28
Download PDF
⟨ Previous Next ⟩

Abstract

Aflatoxin contamination in rice has been documented in a number of studies, and has a high incidence in Asian countries, and as such, there has been a growing interest in alternative biocontrol strategies to address this issue. In this study, 147 strains of yeasts and yeast-like fungi were screened for their potential to produce volatile organic compounds (VOCs) active against Aspergillus flavus strains that produce aflatoxin B1 (AFB1). Five strains within four different genera showed greater than 50% growth inhibition of some strains of A. flavus. These were Anthracocystis sp. DMKU-PAL124, Aureobasidium sp. DMKU-PAL120, Aureobasidium sp. DMKU-PAL144, Rhodotorula sp. DMKU-PAL99, and Solicococcus keelungensis DMKU-PAL84. VOCs produced by these microorganisms ranged from 4 to 14 compounds and included alcohols, alkenes, aromatics, esters and furans. The major VOCs produced by the closely related Aureobasidium strains were found to bedistinct. Moreover, 2-phenylethanol was the most abundant compound generated by Aureobasidium sp. DMKU-PAL120, while methyl benzeneacetate was the major compound emitted from Aureobasidium sp. DMKU-PAL144. On the other hand, 2-methyl-1-butanol and 3-methyl-1-butanol were significant compounds produced by the other three genera. These antagonists apparently inhibited A. flavus sporulation and mycelial development. Additionally, the reduction of the AFB1 in the fungal-contaminated rice grains was observed after co-incubation with these VOC-producing strains and ranged from 37.7 ± 8.3% to 60.3 ± 3.4%. Our findings suggest that these same microorganisms are promising biological control agents for use against aflatoxin-producing fungi in rice and other agricultural products.

Keywords

Acknowledgement

The authors are grateful to Associate Professor Dr. Nantana Srisuk of Kasetsart University, the director of the research program. This work was supported by Kasetsart University Research and Development Institute, KURDI under Grant no. FF(KU)18.64.

References

  1. Kumar P, Mahato DK, Kamle M, Mohanta TK, Kang SG. 2017. Aflatoxins: a global concern for food safety, human health and their management. Front. Microbiol. 7: 2170. https://doi.org/10.3389/fmicb.2016.02170
  2. Koppen R, Koch M, Siegel D, Merkel S, Maul R, Nehls I. 2010. Determination of mycotoxins in foods: current state of analytical methods and limitations. Appl. Microbiol. Biotechnol. 86: 1595-1612. https://doi.org/10.1007/s00253-010-2535-1
  3. World Health Organization (WHO). 2018. Aflatoxins. Department of Food Safety and Zoonoses. Ref. No.: WHO/NHM/FOS/RAM/18.1. WHO, Geneva, Switzerland. Available at: https://www.who.int/foodsafety/Food_Safety_Digest_Aflatoxins_EN.pdf. Accessed December 24, 2011.
  4. International Agency for Research on Cancer (IARC). 2002. IARC monographs on the evaluation of carcinogenic risks to humans, Vol. 82, some traditional herbal medicines, some mycotoxins, naphthalene and styrene. pp. 171-300. IARCPress, Lyon.
  5. Milovanovic V, Smutka L. 2017. Asian countries in the global rice market. Acta Univ. Agric. et Silvic. Mendelianae Brun. 65: 679-688. https://doi.org/10.11118/actaun201765020679
  6. Ali N. 2019. Aflatoxins in rice: worldwide occurrence and public health perspectives. Toxicol. Rep. 6: 1188-1197. https://doi.org/10.1016/j.toxrep.2019.11.007
  7. Niknejad F, Zaini F, Faramarzi M, Amini M, Kordbacheh P, Mahmoudi M, et al. 2012. Candida parapsilosis as a potent biocontrol agent against growth and aflatoxin production by Aspergillus Species. Iran. J. Public Health. 41:72-80.
  8. 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. https://doi.org/10.1007/s10526-020-09996-9
  9. Jaibangyang S, Nasanit R, Limtong S. 2021. 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. https://doi.org/10.1007/s10526-021-10082-x
  10. Hua SS, Beck JJ, Sarreal SB, 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. https://doi.org/10.1007/s12550-014-0189-z
  11. Buzzini P, Martini A, Cappelli F, Pagnoni UM. Davoli P. 2003. A study on volatile organic compounds (VOCs) produced by tropical ascomycetous yeasts. Antonie Van Leeuwenhoek 84: 301-311. https://doi.org/10.1023/A:1026064527932
  12. Schulz-Bohm K, Martin-Sanchez L, Garbeva P. 2017. Microbial volatiles: small molecules with an important role in intra- and inter-kingdom interactions. Front. Microbiol. 8: 2484. https://doi.org/10.3389/fmicb.2017.02484
  13. Di Francesco A, Ugolini L, Lazzeri L, Mari M. 2015. Production of volatile organic compounds by Aureobasidium pullulans as a potential mechanism of action against postharvest fruit pathogens. Biol. Control 81: 8-14. https://doi.org/10.1016/j.biocontrol.2014.10.004
  14. Farbo MG, Urgeghe PP, Fiori S, Marcello A, Oggiano S, Balmas V, et al. 2018. Effect of yeast volatile organic compounds on ochratoxin a-producing Aspergillus carbonarius and A. ochraceus. Int. J. Food Microbiol. 284: 1-10. https://doi.org/10.1016/j.ijfoodmicro.2018.06.023
  15. Khunnamwong P, Lertwattanasakul N, Jindamorakot S, Suwannarach N, Matsui K, Limtong S. 2020. Evaluation of antagonistic activity and mechanisms of endophytic yeasts against pathogenic fungi causing economic crop diseases. Folia Microbiologica 65: 573-590. https://doi.org/10.1007/s12223-019-00764-6
  16. 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. https://doi.org/10.1016/j.funbio.2018.04.006
  17. Huang R, Li GQ, Zhang J, Yang L, Che HJ, Jiang DH, et al. 2011. Control of postharvest Botrytis fruit rot of strawberry by volatile organic compounds of Candida intermedia. Phytopathology 101: 859-869. https://doi.org/10.1094/PHYTO-09-10-0255
  18. Choinska R, Piasecka-Jozwiak K, Chablowska B, Dumka J, Lukaszewicz A. 2020. Biocontrol ability and volatile organic compounds production as a putative mode of action of yeast strains isolated from organic grapes and rye grains. Antonie Van Leeuwenhoek 113: 1135-1146. https://doi.org/10.1007/s10482-020-01420-7
  19. Contarino R, Brighina S, Fallico B, Cirvilleri G, Parafati L, Restuccia C. 2019. Volatile organic compounds (VOCs) produced by biocontrol yeasts. Food Microbiol. 82: 70-74. https://doi.org/10.1016/j.fm.2019.01.008
  20. Liu P, Cheng Y, Yang M, Liu Y, Chen K, Long CA, et al. 2014. Mechanisms of action for 2-phenylethanol isolated from Kloeckera apiculata in control of Penicillium molds of citrus fruits. BMC Microbiol. 14: 242. https://doi.org/10.1186/s12866-014-0242-2
  21. Chang PK, Hua SS, Sarreal SB, Li RW. 2015. Suppression of aflatoxin biosynthesis in Aspergillus flavus by 2-phenylethanol is associated with stimulated growth and decreased degradation of branched-chain amino acids. Toxins 7: 3887-3902. https://doi.org/10.3390/toxins7103887
  22. 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: 1527-1535. https://doi.org/10.5897/AJMR2015.7425
  23. alage Don SM, Schmidtke LM, Gambetta JM, Steel CC. 2021. Volatile organic compounds produced by Aureobasidium pullulans induce electrolyte loss and oxidative stress in Botrytis cinerea and Alternaria alternata. Res. Microbiol. 172:103788. https://doi.org/10.1016/j.resmic.2020.10.003
  24. Wu J-J, Huang J-W, Deng W-L. 2020. Phenylacetic acid and methylphenyl acetate from the biocontrol bacterium Bacillus mycoides BM02 suppress spore germination in Fusarium oxysporum f. sp. lycopersici. Front. Microbiol. 11: 569263. https://doi.org/10.3389/fmicb.2020.569263
  25. Limtong S, Nasanit R. 2017. Phylloplane yeasts in tropical climates, pp. 199-233. In Buzzini P, Lachance MA, Yurkov A (eds.), Yeasts in Natural Ecosystems: Diversity. Springer, Cham.
  26. Pagans E, Font X, Sanchez A. 2006. Emission of volatile organic compounds from composting of different solid wastes: abatement by biofiltration. J. Hazard. Mater. 131: 179-186. https://doi.org/10.1016/j.jhazmat.2005.09.017
  27. Tilocca B, Cao A, Migheli Q. 2020. Scent of a killer: Microbial volatilome and its role in the biological control of plant pathogens. Front. Microbiol. 11: 41. https://doi.org/10.3389/fmicb.2020.00041