Food Science and Biotechnology

, Volume 25, Issue 6, pp 1789–1794 | Cite as

Biotransformation and detoxification of aflatoxin B1 by extracellular extract of Cladosporium uredinicola

  • Shuai Shao
  • Jun Cai
  • Xin Du
  • ChangGao Wang
  • JianGuo Lin
  • Jun Dai
Article

Abstract

Aflatoxin contamination of food and grain poses a serious economic and health problem globally. Aflatoxin B1 (AFB1) is extremely mutagenic and toxic as well as a potent carcinogen to both humans and livestock. In this study, the degradation of AFB1 by extracellular extract of Cladosporium uredinicola was examined using high-performance liquid chromatography (HPLC), thin-layer chromatography (TLC), and liquid chromatography mass spectrometry. Within 24 h of incubation, AFB1 was efficiently eliminated by the culture supernatant of C. uredinicola (84.5±5.7%) at 37°C; the elimination was proven to be enzymatic, and the enzyme was thermostable. The biotransformation products of AFB1 detected by HPLC and TLC were proven to be the same compound. Analysis with LCMS showed that AFB1 was bio-transformed to a structurally different compound (m/z=365 [M+Na]+), which is first reported. The cytotoxicity study to HeLa cells indicated that culture supernatant-treated AFB1 is less toxic as compared with AFB1.

Keywords

Aflatoxin B1 biotransformation Cladosporium uredinicola culture supernatant cytotoxicity 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Maragos CM. Measurement of aflatoxins using capillary electrophoresis. pp. 51–58. In: Mycotoxin Protocols. Trucksess MW, Pohland AE (eds). Food and Drug Administration, Totowa, NJ, USA (2001)Google Scholar
  2. 2.
    International Agency for Research on Cancer. Some naturally occurring substances: Food items and constituents, heterocyclic aromatic amines and mycotoxins. p. 599. In: IARC monograph on the evaluation of carcinogenic risk to humans. International Agency for Research on Cancer, Lyon, France (1993)Google Scholar
  3. 3.
    Van Rensburg SJ, Cook-Mozaffari P, Van Schalkwyk DJ, Van der Watt JJ, Vincent TJ, Purchase IF. Hepatocellular carcinoma and dietary aflatoxin in Mozambique and Transkei. Brit. J. Cancer 51: 713–726 (1985)CrossRefGoogle Scholar
  4. 4.
    Autrup H, Seremet T, Wakhisi J, Wasunna A. Aflatoxin exposure measured by urinary execretion of aflatoxin B1-guanine adduct and hepatitis B virus infection in areas with different liver cancer incidence in Kenya. Cancer Res. 47: 3430–3433 (1987)Google Scholar
  5. 5.
    Ross RK, Yu MC, Henderson BE, Yuan JM, Qian GS, Tu JT, Gao YT, Wogan GN, Groopman JD. Urinary aflatoxin biomarkers and risk of hepatocellular carcinoma. Lancet 339: 943–946 (1992)CrossRefGoogle Scholar
  6. 6.
    Bata Á, Lásztity R. Detoxification of mycotoxin-contaminated food and feed by microorganisms. Trends Food Sci. Tech. 10: 223–228 (1999)CrossRefGoogle Scholar
  7. 7.
    Line JE, Brackett RE. Factors affecting aflatoxin B1 removal by Flavobacterium aurantiacum. J. Food Protect. 58: 91–94 (1995)CrossRefGoogle Scholar
  8. 8.
    Wu Q, Jezkova A, Yuan Z, Pavlikova L, Dohnal V, Kuca K. Biological degradation of aflatoxins. Drug Metab. Rev. 41: 1–7 (2009)CrossRefGoogle Scholar
  9. 9.
    Fazeli MR, Hajimohammadali M, Moshkani A, Samadi N, Jamalifar H, Khoshayand MR, Vaghari E, Pouragahi S. Aflatoxin B1 binding capacity of autochthonous strains of lactic acid bacteria. J. Food Protect. 72: 189–192 (2009)CrossRefGoogle Scholar
  10. 10.
    Jespersen L, Shetty PH. Saccharomyces cerevisiae and lactic acid bacteria as potential mycotoxin decontaminating agents. Trends Food Sci. Tech. 17: 48–55 (2006)CrossRefGoogle Scholar
  11. 11.
    Peltonen K, El-Nezami H. Aflatoxin b1 binding by dairy strains of lactic acid bacteria and bifidobacteria. J. Dairy Sci. 84: 2152–2156 (2001)CrossRefGoogle Scholar
  12. 12.
    Detroy RW, Hesseltine CW. Aflatoxicol: Structure of a new transformation product of aflatoxin B1. Can. J. Biochem. 48: 830–832 (1970)CrossRefGoogle Scholar
  13. 13.
    Mann R, Rehm HJ. Degradation products from aflatoxin B1 by Corynebacterium rubrum, Aspergillus niger, Trichoderma viride and Mucor ambiguus. Appl. Microbiol. Biot. 2: 297–306 (1976)Google Scholar
  14. 14.
    Samuel MS, Sivaramakrishna A, Mehta A. Degradation and detoxification of aflatoxin B1 by Pseudomonas putida. Int. Biodeter. Biodegr. 86: 202–209 (2014)CrossRefGoogle Scholar
  15. 15.
    Liu DL, Yao DS, Liang R, Ma L, Cheng WQ, Gu LQ. Detoxification of aflatoxin B1 by enzymes isolated from Armillariella tabescens. Food Chem. Toxicol. 36: 563–574 (1998)CrossRefGoogle Scholar
  16. 16.
    Guan S, Ji C, Zhou T, Li J, Ma Q, Niu T. Aflatoxin B1 degradation by Stenotrophomonas maltophilia and other microbes selected using coumarin medium. Int. J. Mol. Sci. 9: 1489–1503 (2008)CrossRefGoogle Scholar
  17. 17.
    Motomura M, Toyomasu T, Mizuno K, Shinozawa T. Purification and characterization of an aflatoxin degradation enzyme from Pleurotus ostreatus. Microbiol. Res. 158: 237–242 (2003)CrossRefGoogle Scholar
  18. 18.
    Liu DL, Yao DS, Liang YQ, Zhou TH, Song YP, Zhao L, Ma L. Production, purification, and characterization of an intracellular aflatoxin-detoxifizyme from Armillariella tabescens (E-20). Food Chem. Toxicol. 39: 461–466 (2001)CrossRefGoogle Scholar
  19. 19.
    Cao H, Liu D, Mo X, Xie C, Yao D. A fungal enzyme with the ability of aflatoxin B1 conversion: Purification and ESI-MS/MS identification. Microbiol. Res. 166: 475–483 (2011)CrossRefGoogle Scholar
  20. 20.
    Zhao LH, Guan S, Gao X, Ma QG, Lei YP, Bai XM, Ji C. Preparation, purification and characteristics of an aflatoxin degradation enzyme from Myxococcus fulvus ANSM068. J. Appl. Microbiol. 110: 147–155 (2011)CrossRefGoogle Scholar
  21. 21.
    Wang J, Ogata M, Hirai H, Kawagishi H. Detoxification of aflatoxin B1 by manganese peroxidase from the white-rot fungus Phanerochaete sordida YK-624. FEMS Microbiol. Lett. 314: 164–169 (2011)CrossRefGoogle Scholar
  22. 22.
    Alberts JF, Gelderblom WCA, Botha A, Van Zyl WH. Degradation of aflatoxin B1 by fungal laccase enzymes. Int. J. Food Microbiol. 135: 47–52 (2009)CrossRefGoogle Scholar
  23. 23.
    Ehrlich KC, Cotty PJ. An isolate of Aspergillus flavus used to reduce aflatoxin contamination in cottonseed has a defective polyketide synthase gene. Appl. Microbiol. Biot. 65: 473–478 (2004)CrossRefGoogle Scholar
  24. 24.
    Zuo RY, Chang J, Yin QQ, Wang P, Yang YR, Wang X, Wang GQ, Zheng QH. Effect of the combined probiotics with aflatoxin B1-degrading enzyme on aflatoxin detoxification, broiler production performance and hepatic enzyme gene expression. Food Chem. Toxicol. 59: 470–475 (2013)CrossRefGoogle Scholar
  25. 25.
    Chen Y, Kong Q, Chi C, Shan S. Biotransformation of aflatoxin B1 and aflatoxin G1 in peanut meal by anaerobic solid fermentation of Streptococcus thermophilus and Lactobacillus delbrueckii subsp. bulgaricus. Int. J. Food Microbiol. 211: 1–5 (2015)CrossRefGoogle Scholar
  26. 26.
    Teniola, OD, Addo PA, Brost IM, Färber P, Jany KD, Alberts JF, Van Zyl WH, Steyn PS, Holzapfel WH. Degradation of aflatoxin B1 by cell-free extracts of Rhodococcus erythropolis and Mycobacterium fluoranthenivorans sp. nov. DSM44556T. Int. J. Food Microbiol. 105: 111–117 (2005)CrossRefGoogle Scholar
  27. 27.
    Smiley RD, Draughon FA. Preliminary evidence that degradation of aflatoxin B1 by flavobacterium aurantiacum is enzymatic. J. Food Protect. 63: 415–418 (2000)CrossRefGoogle Scholar
  28. 28.
    Alberts JF, Engelbrecht Y, Steyn PS, Holzapfel WH, Van Zyl WH. Biological degradation of aflatoxin B1 by Rhodococcus erythropolis cultures. Int. J. Food Microbiol. 109: 121–126 (2006)CrossRefGoogle Scholar
  29. 29.
    Lee LS, Dunn JJ, De Lucca AJ, Ciegler A. Role of lactone ring of aflatoxin B1 in toxicity and mutagenicity. Experientia 37: 16–17 (1981)CrossRefGoogle Scholar
  30. 30.
    Parker WA, Melnick D. Absence of aflatoxin from refined vegetable oils. J. Am. Oil Chem. Soc. 43: 635–638 (1966)CrossRefGoogle Scholar
  31. 31.
    Taylor MC, Jackson CJ, Tattersall DB, French N, Peat TS, Newman J, Briggs LJ, Lapalikar GV, Campbell PM, Scott C, Russell RJ, Oakeshott JG. Identification and characterization of two families of F420H2-dependent reductases from mycobacteria that catalyse aflatoxin degradation. Mol. Microbiol. 78: 561–575 (2010)CrossRefGoogle Scholar
  32. 32.
    Barros ST, Oliveira NT, Bastos STG, Maia LC. Hyperparasitism of Cladosporium uredinicola over Puccinia puta on the host Ipomoea fistulosa. Mycologist 13: 23–24 (1999)CrossRefGoogle Scholar

Copyright information

© The Korean Society of Food Science and Technology and Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  • Shuai Shao
    • 1
  • Jun Cai
    • 1
  • Xin Du
    • 1
  • ChangGao Wang
    • 1
  • JianGuo Lin
    • 1
  • Jun Dai
    • 1
  1. 1.Key Laboratory of Fermentation Engineering (Ministry of Education), Hubei Provincial Cooperative Innovation Center of Industrial FermentationHubei University of TechnologyWuhanChina

Personalised recommendations