1887

Abstract

A soil bacterium, designated strain no. 27, was found to produce aflatoxin-production inhibitors. The strain was identified as a species of the genus , and was found to be closely related to Two diketopiperazines, cyclo(-Ala–-Pro) and cyclo(-Val–-Pro), were isolated from the bacterial culture filtrate as main active components. These compounds inhibited aflatoxin production of and in liquid medium at concentrations of several hundred µM without affecting fungal growth. Both inhibitors inhibited production of norsorolinic acid, a biosynthetic intermediate involved in an early step of the aflatoxin biosynthetic pathway, and reduced the mRNA level of , which is a gene encoding a key regulatory protein necessary for the expression of aflatoxin-biosynthetic enzymes. These results indicated that the inhibitors targets are present in early regulatory steps leading to AflR expression. Co-culture of strain no. 27 with aflatoxigenic fungi in liquid medium effectively suppressed aflatoxin production of the fungus without affecting fungal growth. Furthermore, application of the bacterial cells to peanuts in laboratory experiments and at a farmer’s warehouse in Thailand by dipping peanuts in the bacterial cell suspension strongly inhibited aflatoxin accumulation. The inhibitory effect was dependent on bacterial cell numbers. These results indicated that strain no. 27 may be a practically effective biocontrol agent for aflatoxin control.

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2013-05-01
2020-08-08
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References

  1. Abbas H. K., Wilkinson J. R., Zablotowicz R. M., Accinelli C., Abel C. A., Bruns H. A., Weaver M. A.. ( 2009;). Ecology of Aspergillus flavus, regulation of aflatoxin production, and management strategies to reduce aflatoxin contamination of corn. Toxin Rev28:142–153 [CrossRef]
    [Google Scholar]
  2. Abbas H. K., Weaver M. A., Horn B. W., Carbone I., Monacell J. T., Shier W. T.. ( 2011;). Selection of Aspergillus flavus isolates for biological control of aflatoxins in corn. Toxin Rev30:59–70[CrossRef]
    [Google Scholar]
  3. Bianchini A., Bullerman L. B.. ( 2010;). Biological control of molds and mycotoxins in foods. Mycotoxin Prevention and Control in Agriculture1–16ACS symposium series Appell M., Kendra D., Trucksess M.. Washington, DC: American Chemical Society; [CrossRef]
    [Google Scholar]
  4. Brown R. L., Cotty P. J., Cleveland T. E.. ( 1991;). Reduction in aflatoxin content of maize by atoxigenic strains of Aspergillus flavus . J Food Prot54:623–626
    [Google Scholar]
  5. Campbell J., Lin Q., Geske G. D., Blackwell H. E.. ( 2009;). New and unexpected insights into the modulation of LuxR-type quorum sensing by cyclic dipeptides. ACS Chem Biol4:1051–1059 [CrossRef][PubMed]
    [Google Scholar]
  6. Cary J. W., Rajasekaran K., Brown R. L., Luo M., Chen Z. Y., Bhatnagar D.. ( 2011;). Developing resistance to aflatoxin in maize and cottonseed. Toxins (Basel) 3:678–696 [CrossRef][PubMed]
    [Google Scholar]
  7. Cotty, P. J. (1992).Aspergillus flavus
  8. Cotty P. J.. ( 1994;). Influence of field application of an atoxigenic strain of Aspergillus flavus on the populations of A. flavus infecting cotton bolls and on the aflatoxin content of cottonseed. Phytopathology84:1270–1277 [CrossRef]
    [Google Scholar]
  9. Dorner J. W., Cole R. J.. ( 2002;). Effect of application of nontoxigenic strains of Aspergillus flavus and A. parasiticus on subsequent aflatoxin contamination of peanuts in storage. J Stored Prod Res38:329–339 [CrossRef]
    [Google Scholar]
  10. Duangpatra, J. & Pumdeeying, N. (2002).The Proceedings of the Sixteenth Thailand National Peanut Meeting 2002, May 1–3, 2002,
  11. Duangpatra, J., Chompreeda, P., Chinaputhi, A. & Promchote, P. (2005).Summary International Peanut Conference 2005, Prospects and Emerging Opportunities for Peanut Quality and Utilization Technology January 9–12, 2005,
  12. Ehrlich K. C., Kobbeman K., Montalbano B. G., Cotty P. J.. ( 2007;). Aflatoxin-producing Aspergillus species from Thailand. Int J Food Microbiol114:153–159 [CrossRef][PubMed]
    [Google Scholar]
  13. Gautschi M., Schmid J. P., Peppard T. L., Ryan T. P., Tuorto R. M., Yang X.. ( 1997;). Chemical characterization of diketopiperazines in beer. J Agric Food Chem45:3183–3189 [CrossRef]
    [Google Scholar]
  14. Guan S., Ji C., Zhou T., Li J., Ma Q., Niu T.. ( 2008;). Aflatoxin B1 degradation by Stenotrophomonas maltophilia and other microbes selected using coumarin medium. Int J Mol Sci9:1489–1503 [CrossRef][PubMed]
    [Google Scholar]
  15. Haskard C. A., Binnion C., Ahokas J.. ( 2000;). Factors affecting the sequestration of aflatoxin by Lactobacillus rhamnosus strain GG. Chem Biol Interact128:39–49 [CrossRef][PubMed]
    [Google Scholar]
  16. Haskard C. A., El-Nezami H. S., Kankaanpää P. E., Salminen S., Ahokas J. T.. ( 2001;). Surface binding of aflatoxin B1 by lactic acid bacteria. Appl Environ Microbiol67:3086–3091 [CrossRef][PubMed]
    [Google Scholar]
  17. Holden M. T. G., Ram Chhabra S., de Nys R., Stead P., Bainton N. J., Hill P. J., Manefield M., Kumar N., Labatte M. et al. ( 1999;). Quorum-sensing cross talk: isolation and chemical characterization of cyclic dipeptides from Pseudomonas aeruginosa and other Gram-negative bacteria. Mol Microbiol33:1254–1266 [CrossRef][PubMed]
    [Google Scholar]
  18. Holmes R. A., Boston R. S., Payne G. A.. ( 2008;). Diverse inhibitors of aflatoxin biosynthesis. Appl Microbiol Biotechnol78:559–572 [CrossRef][PubMed]
    [Google Scholar]
  19. Hua S. S. T., Baker J. L., Flores-Espiritu M.. ( 1999;). Interactions of saprophytic yeasts with a nor mutant of Aspergillus flavus . Appl Environ Microbiol65:2738–2740[PubMed]
    [Google Scholar]
  20. Jayashree T., Subramanyam C.. ( 1999;). Antiaflatoxigenic activity of eugenol is due to inhibition of lipid peroxidation. Lett Appl Microbiol28:189–193 [CrossRef][PubMed]
    [Google Scholar]
  21. Jermnak U., Yoshinari T., Sugiyama Y., Tsuyuki R., Nagasawa H., Sakuda S.. ( 2012;). Isolation of methyl syringate as a specific aflatoxin production inhibitor from the essential oil of Betula alba and aflatoxin production inhibitory activities of its related compounds. Int J Food Microbiol153:339–344 [CrossRef][PubMed]
    [Google Scholar]
  22. Kodaira Y.. ( 1962;). Toxic substances to insects, produced by Aspergillus ochraceus and Oospra destructor . Agric Biol Chem25:261–262[CrossRef]
    [Google Scholar]
  23. Li X., Dobretsov S., Xu Y., Xiao X., Hung O. S., Qian P. Y.. ( 2006;). Antifouling diketopiperazines produced by deep-sea bacterium, Streptomyces fungicidicus . Biofouling22:187–194 [CrossRef][PubMed]
    [Google Scholar]
  24. Liu Y., Wu F.. ( 2010;). Global burden of aflatoxin-induced hepatocellular carcinoma: a risk assessment. Environ Health Perspect118:818–824 [CrossRef][PubMed]
    [Google Scholar]
  25. Liu C., Yang X. Q., Ding Z. T., Zhao L. X., Cao Y. R., Xu L. H., Yang Y. B.. ( 2011;). Cyclodipeptides from the secondary metabolites of two novel Actinomycetes. Chin J Nat Med9:78–80
    [Google Scholar]
  26. Mahoney N., Molyneux R. J.. ( 2004;). Phytochemical inhibition of aflatoxigenicity in Aspergillus flavus by constituents of walnut (Juglans regia). J Agric Food Chem52:1882–1889 [CrossRef][PubMed]
    [Google Scholar]
  27. Munimbazi C., Bullerman L. B.. ( 1997;). Inhibition of aflatoxin production of Aspergillus parasiticus NRRL 2999 by Bacillus pumilus . Mycopathologia140:163–169 [CrossRef]
    [Google Scholar]
  28. Norton N. R.. ( 1997;). Effect of carotenoids on aflatoxin B1 synthesis by Aspergillus flavus . Phytopathology87:814–821 [CrossRef]
    [Google Scholar]
  29. Oliveira C. M., Silva G. H., Regasini L. O., Zanardi L. M., Evangelista A. H., Young M. C., Bolzani V. S., Araujo A. R.. ( 2009;). Bioactive metabolites produced by Penicillium sp. 1 and sp. 2, two endophytes associated with Alibertia macrophylla (Rubiaceae). Z Naturforsch C64:824–830[PubMed][CrossRef]
    [Google Scholar]
  30. Ortiz-Castro R., Díaz-Pérez C., Martínez-Trujillo M., del Río R. E., Campos-García J., López-Bucio J.. ( 2011;). Transkingdom signaling based on bacterial cyclodipeptides with auxin activity in plants. Proc Natl Acad Sci U S A108:7253–7258 [CrossRef][PubMed]
    [Google Scholar]
  31. Palumbo J. D., Baker J. L., Mahoney N. E.. ( 2006;). Isolation of bacterial antagonists of Aspergillus flavus from almonds. Microb Ecol52:45–52 [CrossRef][PubMed]
    [Google Scholar]
  32. Palumbo J. D., O’keeffe T. L., Abbas H. K.. ( 2008;). Microbial interactions with mycotoxigenic fungi and mycotoxins. Toxin Rev27:261–285 [CrossRef]
    [Google Scholar]
  33. Paster N., Droby S., Chalutz E., Menasherov M., Nitzan R., Wilson C. L.. ( 1993;). Evaluation of potential of the yeast Pichia guilliermondii as a biocontrol agent against Aspergillus flavus and fungi of stored soya beans. Mycol Res97:1201–1206 [CrossRef]
    [Google Scholar]
  34. Peltonen K., el-Nezami H., Haskard C., Ahokas J., Salminen S.. ( 2001;). Aflatoxin B1 binding by dairy strains of lactic acid bacteria and bifidobacteria. J Dairy Sci84:2152–2156 [CrossRef][PubMed]
    [Google Scholar]
  35. Pickenhagen W., Dietrich P., Keil B., Polonsky J., Nouaille F., Lederer E.. ( 1975;). Identification of the bitter principle of cocoa. Helv Chim Acta58:1078–1086 [CrossRef][PubMed]
    [Google Scholar]
  36. Qi S. H., Xu Y., Gao J., Qian P. Y., Zhang S.. ( 2009;). Antibacterial and antilarval compounds from marine bacterium Pseudomonas rhizosphaerae . Ann Microbiol59:229–233 [CrossRef]
    [Google Scholar]
  37. Reddy K. R. N., Reddy C. S., Muralidharan K.. ( 2009;). Potential of botanicals and biocontrol agents on growth and aflatoxin production by Aspergillus flavus infecting rice grains. Food Contr20:173–178 [CrossRef]
    [Google Scholar]
  38. Reddy K. R. N., Farhana N. I., Salleh B., Oliveira C. A. F.. ( 2010;). Microbiological control of mycotoxins: present status and future concerns. Current Research, Technology and Education Topics in Applied Microbiology and Microbial Biotechnologyvol. 21078–1086 Mendez-Vilas A.. Badajoz: Formatex;
    [Google Scholar]
  39. Ryan R. P., Monchy S., Cardinale M., Taghavi S., Crossman L., Avison M. B., Berg G., van der Lelie D., Dow J. M.. ( 2009;). The versatility and adaptation of bacteria from the genus Sternotrophomonas . Nat Rev Microbiol7:514–525 [CrossRef][PubMed]
    [Google Scholar]
  40. Sakuda S.. ( 2010;). Mycotoxin production inhibitors from natural products. Mycotoxins60:79–86 [CrossRef]
    [Google Scholar]
  41. Schmidtz F. J., Vanderah D. J., Hollenbeak K. H., Enwall C. E. L., Gopichand Y., SenGupta P. K., Hossain M. B., Van der Helm D.. ( 1983;). Metabolites from the marine sponge Tedania ignis. A new atisanediol and several known diketopiperazines. J Org Chem48:3941–3945 [CrossRef]
    [Google Scholar]
  42. Sukharomana S., Dobkuntod B.. ( 2003;). Peanut in the Thai food system: a macro perspective. Peanut in local and global food systems series report No. 8127 Rhoades R. E., Nazarea V.. Athens, Georgia: University of Georgia;
    [Google Scholar]
  43. Taylor W. J., Draughon F. A.. ( 2001;). Nannocystis exedens: a potential biocompetitive agent against Aspergillus flavus and Aspergillus parasiticus . J Food Prot64:1030–1034[PubMed]
    [Google Scholar]
  44. Ten L. N., Stepanichenko N. N., Mukhamedzhanov S. Z., Khotyanovich A. V.. ( 1983;). Action of tricyclazole on the biosynthesis of melanin in some fungi of the genus Verticillium . Chem Nat Compd19:384–385 [CrossRef]
    [Google Scholar]
  45. Teniola O. D., Addo P. A., Brost I. M., Farber P., Jany K. D., Alberts J. F., Vanzyl W. H., Steyn P. S., Holzapfel W. H.. ( 2005;). Degradation of aflatoxin B1 by cell-free extracts of Rhodococcus erythropolis and Mycobacterium fluoranthenivorans sp. nov. DSM44556T . Int J Food Microbiol105:111–117 [CrossRef][PubMed]
    [Google Scholar]
  46. Thajudeen H., Park K., Moon S. S., Hong I. S.. ( 2010;). An efficient green synthesis of proline-based cyclic dipeptides under water-mediated catalyst-free conditions. Tetrahedron Lett51:1303–1305 [CrossRef]
    [Google Scholar]
  47. Thasnakorn P.. ( 1976;). Detection of aflatoxin in ground roast peanut. Siriraj Hosp Gaz28:375–382
    [Google Scholar]
  48. Trigos A., Reyna S., Galindo G., Ramos J. M.. ( 1996;). Diketopiperazines from cultures of fungus Pestalotia palmarum . Nat Prod Lett8:199–205 [CrossRef]
    [Google Scholar]
  49. van der Greef J., Tas A. C., Nijssen L. M., Jetten J., Höhn M.. ( 1987;). Identification and quantitation of diketopiperazines by liquid chromatography-mass spectrometry, using a moving belt interface. Chromatography394:77–88 [CrossRef]
    [Google Scholar]
  50. Waenlor W., Wiwanitkit V.. ( 2003;). Aflatoxin contamination of food and food products in Thailand: an overview. Southeast Asian J Trop Med Public Health34:Suppl. 2184–190[PubMed]
    [Google Scholar]
  51. Wang J. H., Quan C. S., Qi X. H., Li X., Fan S. D.. ( 2010;). Determination of diketopiperazines of Burkholderia cepacia CF-66 by gas chromatography-mass spectrometry. Anal Bioanal Chem396:1773–1779 [CrossRef][PubMed]
    [Google Scholar]
  52. Wild C. P., Turner P. C.. ( 2002;). The toxicology of aflatoxins as a basis for public health decisions. Mutagenesis17:471–481 [CrossRef][PubMed]
    [Google Scholar]
  53. Woloshuk C. P., Foutz K. R., Brewer J. F., Bhatnagar D., Cleveland T. E., Payne G. A.. ( 1994;). Molecular characterization of aflR, a regulatory locus for aflatoxin biosynthesis. Appl Environ Microbiol60:2408–2414[PubMed]
    [Google Scholar]
  54. Wu F., Khlangwiset P.. ( 2010;). Health economic impacts and cost-effectiveness of aflatoxin-reduction strategies in Africa: case studies in biocontrol and post-harvest interventions. Food Addit Contam Part A Chem Anal Control Expo Risk Assess27:496–509 [CrossRef][PubMed]
    [Google Scholar]
  55. Wu Q., Jezkova A., Yuan Z., Pavlikova L., Dohnal V., Kuca K.. ( 2009;). Biological degradation of aflatoxins. Drug Metab Rev41:1–7 [CrossRef][PubMed]
    [Google Scholar]
  56. Yan P. S., Song Y., Sakuno E., Nakajima H., Nakagawa H., Yabe K.. ( 2004;). Cyclo(l-leucyl–l-prolyl) produced by Achromobacter xylosoxidans inhibits aflatoxin production by Aspergillus parasiticus . Appl Environ Microbiol70:7466–7473 [CrossRef][PubMed]
    [Google Scholar]
  57. Yin Y. N., Yan L. Y., Jiang J. H., Ma Z. H.. ( 2008;). Biological control of aflatoxin contamination of crops. J Zhejiang Univ Sci B9:787–792 [CrossRef][PubMed]
    [Google Scholar]
  58. Yoshinari T., Akiyama T., Nakamura K., Kondo T., Takahashi Y., Muraoka Y., Nonomura Y., Nagasawa H., Sakuda S.. ( 2007;). Dioctatin A is a strong inhibitor of aflatoxin production by Aspergillus parasiticus . Microbiology153:2774–2780 [CrossRef][PubMed]
    [Google Scholar]
  59. Yu J., Chang P. K., Ehrlich K. C., Cary J. W., Bhatnagar D., Cleveland T. E., Payne G. A., Linz J. E., Woloshuk C. P., Bennett J. W.. ( 2004;). Clustered pathways genes in aflatoxin biosynthesis. Appl Microbiol70:1253–1262 [CrossRef]
    [Google Scholar]
  60. Zhao L. H., Guan S., Gao X., Ma Q. G., Lei Y. P., Bai X. M., Ji C.. ( 2011;). Preparation, purification and characteristics of an aflatoxin degradation enzyme from Myxococcus fulvus ANSM068. J Appl Microbiol110:147–155 [CrossRef][PubMed]
    [Google Scholar]
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