Mycobiology

The Korean Society of Mycology (한국균학회)
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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

  • Mannaa, Mohamed (Laboratory of Plant Disease and Biocontrol, Department of Biosystems and Biotechnology, Korea University) ;
  • Kim, Ki Deok (Laboratory of Plant Disease and Biocontrol, Department of Biosystems and Biotechnology, Korea University)
  • Received : 2018.04.07
  • Accepted : 2018.07.23
  • Published : 2018.09.01
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Abstract

In this study, we evaluated the effect of different temperatures (10, 20, 30, and $40^{\circ}C$) and relative humidities (RHs; 12, 44, 76, and 98%) on populations of predominant grain fungi (Aspergillus candidus, Aspergillus flavus, Aspergillus fumigatus, Penicillium fellutanum, and Penicillium islandicum) and the biocontrol activity of Pseudomonas protegens AS15 against aflatoxigenic A. flavus KCCM 60330 in stored rice. Populations of all the tested fungi in inoculated rice grains were significantly enhanced by both increased temperature and RH. Multiple linear regression analysis revealed that one unit increase of temperature resulted in greater effects than that of RH on fungal populations. When rice grains were treated with P. protegens AS15 prior to inoculation with A. flavus KCCM 60330, fungal populations and aflatoxin production in the inoculated grains were significantly reduced compared with the grains untreated with strain AS15 regardless of temperature and RH (except 12% RH for fungal population). In addition, bacterial populations in grains were significantly enhanced with increasing temperature and RH, regardless of bacterial treatment. Higher bacterial populations were detected in biocontrol strain-treated grains than in untreated control grains. To our knowledge, this is the first report showing consistent biocontrol activity of P. protegens against A. flavus population and aflatoxin production in stored rice grains under various environmental conditions of temperature and RH.

Keywords

References

  1. KOSTAT. Annual Trends of Food Grain Consumption in 2016. Korean Statistical Information Service, [WWW document]. Available from: http://kostat.go.kr/portal/eng/pressReleases/2/11/index.board [accessed 2 March 2017]; 2017.
  2. Kabak B, Dobson ADW, Var I. Strategies to prevent mycotoxin contamination of food and animal feed: a review. Crit Rev Food Sci Nutr. 2006;46:593-619. https://doi.org/10.1080/10408390500436185
  3. Magan N, Lacey J. Effect of temperature and pH on water relations of field and storage fungi. Trans Br Mycol Soc. 1984;82:71-81. https://doi.org/10.1016/S0007-1536(84)80213-2
  4. Christensen CM, Kaufmann HH. Grain storage: the role of fungi in quality loss. Minneapolis (MN): University of Minnesota Press; 1969.
  5. Hocking AD, Pitt JI. Water relations of some Penicillium species at $25^{\circ}C$. Trans Br Mycol Soc. 1979;73:141-145. https://doi.org/10.1016/S0007-1536(79)80084-4
  6. Magan N, Lacey J. Ecological determinants of mould growth in stored grain. Int J Food Microbiol. 1988;7:245-256. https://doi.org/10.1016/0168-1605(88)90043-8
  7. Mannaa M, Kim KD. Influence of temperature and water activity on deleterious fungi and mycotoxin producing during grain storage. Mycobiology. 2017;45:240-254. https://doi.org/10.5941/MYCO.2017.45.4.240
  8. Klich MA. Environmental and developmental factors influencing aflatoxin production by Aspergillus flavus and Aspergillus parasiticus. Mycoscience. 2007;48:71-80. https://doi.org/10.1007/S10267-006-0336-2
  9. Squire RA. Ranking animal carcinogens: a proposed regulatory approach. Science. 1981;214:877-880. https://doi.org/10.1126/science.7302565
  10. Sweeney MJ, Dobson ADW. Mycotoxin production by Aspergillus, Fusarium and Penicillium species. Int J Food Microbiol. 1998;43:141-158. https://doi.org/10.1016/S0168-1605(98)00112-3
  11. Mannaa M, Kim KD. Microbe-mediated control of mycotoxigenic grain fungi in stored rice with focus on aflatoxin biodegradation and biosynthesis inhibition. Mycobiology. 2016;44:67-78. https://doi.org/10.5941/MYCO.2016.44.2.67
  12. Oh JY, Kim EN, Ryoo MI, et al. Morphological and molecular identification of Penicillium islandicum isolate KU101 from stored rice. Plant Pathol J. 2008;24:469-473. https://doi.org/10.5423/PPJ.2008.24.4.469
  13. Oh JY, Sang MK, Oh JE, et al. Microbial population, aflatoxin contamination and predominant Aspergillus species in Korean stored rice. Plant Pathol J. 2010;26:121-129. https://doi.org/10.5423/PPJ.2010.26.2.121
  14. Oh JY, Sang MK, Lee HJ, et al. First detection of Penicillium fellutanum from stored rice in Korea. Res Plant Dis. 2011;17:216-221. https://doi.org/10.5423/RPD.2011.17.2.216
  15. Mannaa M, Kim KD. Biocontrol activity of volatile-producing Bacillus megaterium and Pseudomonas protegens against Aspergillus and Penicillium spp. predominant in stored rice grains: study II. Mycobiology. 2018;46:52-63. https://doi.org/10.1080/12298093.2018.1454015
  16. Mannaa M, Oh JY, Kim KD. Microbe-mediated control of Aspergillus flavus in stored rice grains with a focus on aflatoxin inhibition and biodegradation. Ann Appl Biol. 2017;171:376-392. https://doi.org/10.1111/aab.12381
  17. Mannaa M, Oh JY, Kim KD. Biocontrol activity of volatile-producing Bacillus megaterium and Pseudomonas protegens against Aspergillus flavus and aflatoxin production on stored rice grains. Mycobiology. 2017;45:213-219. https://doi.org/10.5941/MYCO.2017.45.3.213
  18. Greenspan L. Humidity fixed points of binary saturated aqueous solutions. J Res Natl Bur Stan Sect A. 1977;81A:89-96. https://doi.org/10.6028/jres.081A.011
  19. Pardo E, Marin S, Sanchis V, et al. Impact of relative humidity and temperature on visible fungal growth and OTA production of ochratoxigenic Aspergillus ochraceus isolates on grapes. Food Microbiol. 2005;22:383-389. https://doi.org/10.1016/j.fm.2004.11.004
  20. Wexler A, Hasegawa S. Relative humidity-temperature relationships of some saturated salt solutions in the temperature range 0 to $50^{\circ}C$. J Res Natl Bur Stan. 1954;53:19-26. https://doi.org/10.6028/jres.053.003
  21. Gu Q, Han N, Liu J, et al. Expression of Helicobacter pylori urease subunit B gene in transgenic rice. Biotechnol Lett. 2006;28:1661-1666. https://doi.org/10.1007/s10529-006-9141-4
  22. Hocking AD, Pitt JI. Dichloran-glycerol medium for enumeration of xerophilic fungi from low-moisture foods. Appl Environ Microbiol. 1980;39:488-492.
  23. Levene H. Robust tests for equality of variances. In: Olkin I, Ghurye SG, Hoeffding W, Madow WG, Mann HB, editors. Contributions to probability and statistics: essays in honor of Harold hotelling. Stanford (CA): Stanford University Press; 1960. p. 278-292.
  24. Marin S, Companys E, Sanchis V, et al. Effect of water activity and temperature on competing abilities of common maize fungi. Mycol Res. 1998;102:959-964. https://doi.org/10.1017/S0953756297005613
  25. Choi S, Jun H, Bang J, et al. Behaviour of Aspergillus flavus and Fusarium graminearum on rice as affected by degree of milling, temperature, and relative humidity during storage. Food Microbiol. 2015;46:307-313. https://doi.org/10.1016/j.fm.2014.08.019
  26. Holmquist GU, Walker HW, Stahr HM. Influence of temperature, pH, water activity and antifungal agents on growth of Aspergillus flavus and A. parasiticus. J Food Sci. 1983;48:778-782. https://doi.org/10.1111/j.1365-2621.1983.tb14897.x
  27. Misra N. Influence of temperature and relative humidity on fungal flora of some spices in storage. Z Lebensm Unters Forch. 1981;172:30-31. https://doi.org/10.1007/BF01255458
  28. Boller RA, Schroeder HW. Influence of relative humidity on production of aflatoxin in rice by Aspergillus parasiticus. Phytopathology. 1974;64:17-21. https://doi.org/10.1094/Phyto-64-17
  29. Punja ZK, Rodriguez G, Tirajoh A. Effects of Bacillus subtilis strain QST 713 and storage temperatures on post-harvest disease development on greenhouse tomatoes. Crop Prot. 2016;84:98-104. https://doi.org/10.1016/j.cropro.2016.02.011
  30. Lahlali R, Hamadi Y, El Guilli M, et al. Efficacy assessment of Pichia guilliermondii strain Z1, a new biocontrol agent, against citrus blue mould in Morocco under the influence of temperature and relative humidity. Biol Control. 2011;56:217-224. https://doi.org/10.1016/j.biocontrol.2010.12.001
  31. Mislivec PB, Dieter CT, Bruce VR. Effect of temperature and relative humidity on spore germination of mycotoxic species of Aspergillus and Penicillium. Mycologia. 1975;67:1187-1189. https://doi.org/10.1080/00275514.1975.12019863
  32. Gqaleni N, Smith JE, Lacey J, et al. Effects of temperature, water activity, and incubation time on production of aflatoxins and cyclopiazonic acid by an isolate of Aspergillus flavus in surface agar culture. Appl Environ Microbiol. 1997;63:1048-1053.
  33. Mousa W, Ghazali FM, Jinap S, et al. 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. 2013;78:M56-M63. https://doi.org/10.1111/j.1750-3841.2012.02986.x
  34. Ogundero VW. Temperature and aflatoxin production by Aspergillus flavus and A. parasiticus strains from Nigerian groundnuts. J Basic Microbiol. 1987;27:511-514. https://doi.org/10.1002/jobm.3620270910
  35. Kheiralla ZH, Hassanin NI, Amra H. Effect of incubation time, temperature and substrate on growth and aflatoxin production. Int Biodeterior Biodegr. 1992;30:17-27. https://doi.org/10.1016/0964-8305(92)90021-F
  36. Georgianna DR, Payne GA. Genetic regulation of aflatoxin biosynthesis: from gene to genome. Fungal Genet Biol. 2009;46:113-125. https://doi.org/10.1016/j.fgb.2008.10.011
  37. Yu J, Bhatnagar D, Cleveland TE. Completed sequence of aflatoxin pathway gene cluster in Aspergillus parasiticus. FEBS Lett. 2004;564:126-130. https://doi.org/10.1016/S0014-5793(04)00327-8
  38. OBrian GR, Georgianna DR, Wilkinson JR, et al. The effect of elevated temperature on gene transcription and aflatoxin biosynthesis. Mycologia. 2007;99:232-239. https://doi.org/10.1080/15572536.2007.11832583
  39. Schmidt-Heydt M, Abdel-Hadi A, Magan N, et al. Complex regulation of the aflatoxin biosynthesis gene cluster of Aspergillus flavus in relation to various combinations of water activity and temperature. Int J Food Microbiol. 2009;135:231-237. https://doi.org/10.1016/j.ijfoodmicro.2009.07.026
  40. Yu J, Fedorova ND, Montalbano BG, et al. Tight control of mycotoxin biosynthesis gene expression in Aspergillus flavus by temperature as revealed by RNA-Seq. FEMS Microbiol Lett. 2011;322:145-149. https://doi.org/10.1111/j.1574-6968.2011.02345.x

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