The Plant Pathology Journal

The Korean Society of Plant Pathology (한국식물병리학회)
권호 표지
DOI QR코드

DOI QR Code

Inhibition of the Aspergillus flavus Growth and Aflatoxin B1 Contamination on Pistachio Nut by Fengycin and Surfactin-Producing Bacillus subtilis UTBSP1

  • Farzaneh, Mohsen (Medicinal Plants and Drugs Research Institute, Shahid Beheshti University) ;
  • Shi, Zhi-Qi (Institute of Food Safety and Quality, Jiangsu Academy of Agricultural Sciences) ;
  • Ahmadzadeh, Masoud (Department of Plant Protection, University of Tehran) ;
  • Hu, Liang-Bin (Institute of Food Safety and Quality, Jiangsu Academy of Agricultural Sciences) ;
  • Ghassempour, Alireza (Medicinal Plants and Drugs Research Institute, Shahid Beheshti University)
  • Received : 2015.11.24
  • Accepted : 2016.01.20
  • Published : 2016.06.01
Download PDF
⟨ Previous Next ⟩

Abstract

In this study, the treatment of pistachio nuts by Bacillus subtilis UTBSP1, a promising isolate to degrade aflatoxin B1 (AFB1), caused to reduce the growth of Aspergillus flavus R5 and AFB1 content on pistachio nuts. Fluorescence probes revealed that the cell free supernatant fluid from UTBSP1 affects spore viability considerably. Using high-performance liquid chromatographic (HPLC) method, 10 fractions were separated and collected from methanol extract of cell free supernatant fluid. Two fractions showed inhibition zones against A. flavus. Mass spectrometric analysis of the both antifungal fractions revealed a high similarity between these anti-A. flavus compounds and cyclic-lipopeptides of surfactin, and fengycin families. Coproduction of surfactin and fengycin acted in a synergistic manner and consequently caused a strong antifungal activity against A. flavus R5. There was a positive significant correlation between the reduction of A. flavus growth and the reduction of AFB1 contamination on pistachio nut by UTBSP1. The results indicated that fengycin and surfactin-producing B. subtilis UTBSP1 can potentially reduce A. flavus growth and AFB1 content in pistachio nut.

Keywords

References

  1. Bennett, J. W. and Klich, M. 2003. Mycotoxins. Clin. Microbiol. Rev. 16:497-516. https://doi.org/10.1128/CMR.16.3.497-516.2003
  2. Brul, S., Nussbaum, J. and Dielbandhoesing, S. K. 1997. Fluorescent probes for wall porosity and membrane integrity in filamentous fungi. J. Microbiol. Methods 28:169-178. https://doi.org/10.1016/S0167-7012(97)00975-5
  3. Bunthof, C. J., Bloemen, K., Breeuwer, P., Rombouts, F. M. and Abee, T. 2001. Flow cytometric assessment of viability of lactic acid bacteria. Appl. Environ. Microbiol. 67:2326-2335. https://doi.org/10.1128/AEM.67.5.2326-2335.2001
  4. Chitarra, G. S., Breeuwer, P., Nout, M. J. R., Van Aelst, A. C., Rombouts, F. M. and Abee, T. 2003. An antifungal compound produced by Bacillus subtilis YM 10-20 inhibits germination of Penicillium roqueforti conidiospores. J. Appl. Microbiol. 94:159-166. https://doi.org/10.1046/j.1365-2672.2003.01819.x
  5. Cotty, P. J., Bayman, P., Egel, D. S. and Elis, K. S. 1994. Agriculture, aflatoxins and Aspergillus. In: The genus Aspergillus: from taxonomy and genetics to industrial applications, eds. by K. A. Powell, A. Renwick and J. F. Peberdy, pp. 1-27. Plenum Press, New York, NY, USA.
  6. Deleu, M., Paquot, M. and Nylander, T. 2005. Fengycin interaction with lipid monolayers at the air--aqueous interface--- implications for the effect of fengycin on biological membranes. J. Colloid. Interface Sci. 283:358-365. https://doi.org/10.1016/j.jcis.2004.09.036
  7. Dorner, J. W., Cole, R. J. and Blankenship, P. D. 1998. Effect of inoculum rate of biological control agents on preharvest aflatoxin contamination of peanuts. Biol. Control 12:171-176. https://doi.org/10.1006/bcon.1998.0634
  8. Dorner, J. W. 2004. Biological control of aflatoxin contamination of crops. J. Toxicol.: Toxin Rev. 23:425-450. https://doi.org/10.1081/TXR-200027877
  9. Farzaneh, M., Shi, Z. Q., Ghassempour, A., Sedaghat, N., Ahmadzadeh, M., Mirabolfathy, M. and Javan-Nikkhah, M. 2012. Aflatoxin B1 degradation by Bacillus subtilis UTBSP1 isolated from pistachio nuts of Iran. Food Control 23:100-106. https://doi.org/10.1016/j.foodcont.2011.06.018
  10. Gonzalez, G., Hinojo, M. J., Mateo, R., Medina, A. and Jimenez, M. 2005. Occurrence of mycotoxin producing fungi in bee pollen. Int. J. Food Microbiol. 105:1-9. https://doi.org/10.1016/j.ijfoodmicro.2005.05.001
  11. Heerklotz, H. and Seelig, J. 2007. Leakage and lysis of lipid membranes induced by the lipopeptide surfactin. Eur. Biophys. J. 36:305-314. https://doi.org/10.1007/s00249-006-0091-5
  12. Hosono, K. and Suzuki, H. 1983. Acylpeptides, the inhibitors of cyclic adenosine 3, 5-monophosphate phosphodiesterase I, Purification, physicochemical properties and structures of fatty acid residues. J. Antibiot. 36:667-673. https://doi.org/10.7164/antibiotics.36.667
  13. Hu, L. B., Shi, Z. Q., Zhang, T. and Yang, Z. M. 2007. Fengycin antibiotics isolated from B-FS01 culture inhibit the growth of Fusarium moniliforme Sheldon ATCC 38932. FEMS Microbiol. Lett. 272:91-98. https://doi.org/10.1111/j.1574-6968.2007.00743.x
  14. Hu, L. B., Zhang, T., Yang, Z. M. and Shi, Z. Q. 2009. Inhibition of fengycins on the production of fumonisin B1 from Fusarium verticillioides. Lett. Appl. Microbiol. 48:84-89. https://doi.org/10.1111/j.1472-765X.2008.02493.x
  15. Koumoutsi, A., Chen, X. H., Henne, A., Liesegang, H., Hitzeroth, G., Franke, P., Vater, J. and Borriss, R. 2004. Structural and functional characterization of gene clusters directing nonribosomal synthesis of bioactive cyclic lipopeptides in Bacillus amyloliquefaciens strain FZB42. J. Bacteriol. 186:1084-1096. https://doi.org/10.1128/JB.186.4.1084-1096.2004
  16. Kowall, M., Vater, J., Kluge, B., Stein, T., Franke, P. and Ziessow, D. 1998. Separation and characterization of surfactin isoforms produced by Bacillus subtilis OKB 105. J. Colloid Interface Sci. 204:1-8. https://doi.org/10.1006/jcis.1998.5558
  17. Kuroda, J., Fukai, T., Konishi, M., Uno, J., Kurusu, K. and Nomura, T. 2000. LI-F antibiotics, a family of antifungal cyclic depsipeptides produced by Bacillus polymyxa L-1129. Heterocycles 53:1533-1549. https://doi.org/10.3987/COM-00-8922
  18. Maget-Dana, R. and Ptak, M. 1990. Iturin lipopeptides: interactions of mycosubtilin with lipids in planar membranes and mixed monolayers. Biochim. Biophys. Acta 1023:34-40. https://doi.org/10.1016/0005-2736(90)90006-A
  19. Mohammadipour, M., Mousivand, M., Salehi-Jouzani, G. and Abbasalizadeh, S. 2009. Molecular and biochemical characterization of Iranian surfactin-producing Bacillus subtilis isolates and evaluation of their biocontrol potential against Aspergillus flavus and Colletotrichum gloeosporioides. Can. J. Microbiol. 55:395-404. https://doi.org/10.1139/W08-141
  20. Morikawa, M., Hirata, Y. and Imanaka, T. 2000. A study on the structure-function relationship of lipopeptide biosurfactants. Biochim. Biophys. Acta 1488:211-218. https://doi.org/10.1016/S1388-1981(00)00124-4
  21. Moyne, A. L., Shelby, R., Cleveland, T. E. and Tuzun, S. 2001. Bacillomycin D: an iturin with antifungal activity against Aspergillus flavus. J. Appl. Microbiol. 90:622-629. https://doi.org/10.1046/j.1365-2672.2001.01290.x
  22. Munimbazi, C. and Bullerman, L. B. 1998. Isolation and partial characterization of antifungal metabolites of Bacillus pumilus. J. Appl. Microbiol. 84:959-968. https://doi.org/10.1046/j.1365-2672.1998.00431.x
  23. Ongena, M., Jourdan, E., Adam, A., Paquot, M., Brans, A., Joris, B., Arpigny, J. L. and Thonart, P. 2007. Surfactin and fengycin lipopeptides of Bacillus subtilis as elicitors of induced systemic resistance in plants. Environ. Microbiol. 9:1084-1090. https://doi.org/10.1111/j.1462-2920.2006.01202.x
  24. Outtrup, H. and Jorgensen, S. T. 2002. The importance of Bacillus species in the production of industrial enzymes. In: Applications and systematics of Bacillus and relatives, eds. by R. Berkeley, M. Heyndrickx, N. Logan and P. De Vos, pp. 206-218. Wiley-Blackwell, Malden, MA, USA.
  25. Perfect, J. R., Cox, G. M., Lee, J. Y., Kauffman, C. A., De Repentigny, L., Chapman, S. W., Morrison, V. A., Pappas, P., Hiemenz, J. W. and Stevens, D. A. 2001. The impact of culture isolation of Aspergillus species: a hospital-based survey of aspergillosis. Clin. Infect. Dis. 33:1824-1833. https://doi.org/10.1086/323900
  26. Peypoux, F., Guinand, M., Michel, G., Delcambe, L., Das, B. C. and Lederer, E. 1978. Structure of iturine A, a peptidolipid antibiotic from Bacillus subtilis. Biochemistry 17:3992-3996. https://doi.org/10.1021/bi00612a018
  27. Reddy, K. R. N., Reddy, C. S. and Muralidharan, K. 2009. Potential of botanicals and biocontrol agents on growth and aflatoxin production by Aspergillus flavus infecting rice grains. Food Control 20:173-178. https://doi.org/10.1016/j.foodcont.2008.03.009
  28. Romero, D., De Vicente, A., Rakotoaly, R. H., Dufour, S. E., Veening, J. W., Arrebola, E., Cazorla, F. M., Kuipers, O. P., Paquot, M. and Perez-Garcia, A. 2007. The iturin and fengycin families of lipopeptides are key factors in antagonism of Bacillus subtilis toward Podosphaera fusca. Mol. Plant-Microbe Interact. 20:430-440. https://doi.org/10.1094/MPMI-20-4-0430
  29. Samson, R. A., Hoekstra, E. S., Frisvad, J. C. and Filtenborg, O. 1995. Introduction to food and airborne fungi. 4th ed. Centraalbureau Voor Schimmelcultures, Baarn, the Netherlands. 389 pp.
  30. Schading, R. L., Carruthers, R. I. and Mullin-Schading, B. A. 1995. Rapid determination of conidial viability for entomopathogenic hyphomycetes using fluorescence microscopy techniques. Biocontrol Sci. Technol. 5:201-208. https://doi.org/10.1080/09583159550039927
  31. Schallmey, M., Singh, A. and Ward, O. P. 2004. Developments in the use of Bacillus species for industrial production. Can. J. Microbiol. 50:1-17. https://doi.org/10.1139/w03-076
  32. Shephard, G. S. 2005. Aflatoxin and food safety: recent African perspectives. CRC Taylor & Francis, Boca Raton, FL, USA. pp. 13-28.
  33. Stein, T. 2005. Bacillus subtilis antibiotics: structures, syntheses and specific functions. Mol. Microbiol. 56:845-857. https://doi.org/10.1111/j.1365-2958.2005.04587.x
  34. Stroka, J., Anklam, E., Joerissen, U., Gilbert, J. 2001. Determination of aflatoxin B1 in baby food (infant formula) by immunoaffinity column cleanup liquid chromatography with postcolumn bromination: collaborative study. J. AOAC Int. 84:1116-1123.
  35. Sun, L., Lu, Z., Bie, X., Lu, F. and Yang, F. 2006. Isolation and characterization of a co-producer of fengycins and surfactins, endophytic Bacillus amyloliquefaciens ES-2, from Scutellaria baicalensis Georgi. World J. Microbiol. Biotechnol. 22:1259-1266. https://doi.org/10.1007/s11274-006-9170-0
  36. Vanittanakom, N., Loeffler, W., Koch, U. and Jung, G. 1986. Fengycin-a novel antifungal lipopeptide antibiotic produced by Bacillus subtilis F-29-3. J. Antibiot. 39:888-901. https://doi.org/10.7164/antibiotics.39.888
  37. Vater, J., Kablitz, B., Wilde, C., Franke, P., Mehta, N. and Cameotra, S. S. 2002. Matrix-assisted laser desorption ionization-time of flight mass spectrometry of lipopeptide biosurfactants in whole cells and culture filtrates of Bacillus subtilis C-1 isolated from petroleum sludge. Appl. Environ. Microbiol. 68:6210-6219. https://doi.org/10.1128/AEM.68.12.6210-6219.2002
  38. Zhang, T., Hu, L. B., Wang, F., Cheng, L. G. and Shi, Z. Q. 2007. Identification of B-FS06 and the antagonistic activity of its cultural productions against Aspergillus flavus. Chin. J. Biol. Control 23:160-165.

Cited by

  1. Isolation and characterization of a Bacillus subtilis strain with aflatoxin B1 biodegradation capability vol.75, 2017, https://doi.org/10.1016/j.foodcont.2016.12.036
  2. Biological Degradation of Aflatoxin B1 by Cell-Free Extracts of Bacillus velezensis DY3108 with Broad PH Stability and Excellent Thermostability vol.10, pp.8, 2018, https://doi.org/10.3390/toxins10080330