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Detoxification of Aflatoxin B1 by Antifungal Compounds from Lactobacillus brevis and Lactobacillus paracasei, Isolated from Dairy Products

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Abstract

Aflatoxins are a large group of highly toxic, mutagenic, and carcinogenic mycotoxins produced by specific species of fungi. Potential contamination of food commodities by these compounds causes extensive damage that lead to great economic losses. This study explored the potential use of antifungal compounds, produced by Lactobacillus brevis and Lactobacillus paracasei, for growth inhibition and subsequent aflatoxin B1 production from select strains of Aspergillus flavus and Aspergillus parasiticus. Lactobacilli strains were isolated from traditional Egyptian dairy products, whereas fungal strains were isolated from infected cereal seeds. There were noticeable decreases in mycelium biomass and aflatoxin production as well. L. brevis exhibited the highest reduction of aflatoxin B1 production by A. flavus and A. parasiticus, 96.31 and 90.43%, respectively. The concentrations of amino acids of the antifungal compound produced by L. brevis were significantly higher than that produced by L. paracasei. Asparagine, glutamine, glycine, alanine, and leucine were the most concentrated amino acids for both strains. The antifungal compounds produced by L. brevis and L. paracasei were active in a wide range of pH, heat stable and inactivated by proteolytic enzymes (protease K and trypsin A). The expression of Omt-A gene that involved in the later step of aflatoxin production was evaluated by real-time PCR. There was a vigorous reduction at transcriptional level of Omt-A gene observed in A. flavus that is treated by L. brevis and L. paracasei (80 and 70%, respectively). However, the reduction of Omt-A gene observed in A. parasiticus that is treated by L. brevis and L. paracasei was 64.5 and 52%, respectively. Treating maize seeds with antifungal compounds exhibited great efficiency in controlling fungal infection and increasing seed germination. The results confirmed that lactic acid bacteria are a promising strategy to control food contamination of fermented food and dairy products.

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References

  1. Bhat R, Rai RV, Karim A (2010) Mycotoxins in food and feed: present status and future concerns. Compr Rev Food Sci Food Saf 9(1):57–81. https://doi.org/10.1111/j.1541-4337.2009.00094.x

    Article  CAS  PubMed  Google Scholar 

  2. Afsah-Hejri L, Jinap S, Hajeb P, Radu S, Shakibazadeh S (2013) A review on mycotoxins in food and feed: Malaysia case study. Compr Rev Food Sci Food Saf 12(6):629–651. https://doi.org/10.1111/1541-4337.12029

    Article  CAS  PubMed  Google Scholar 

  3. Lutfullah G, Hussain A (2012) Studies on contamination level of aflatoxins in some cereals and beans of Pakistan. Food Control 23(1):32–36. https://doi.org/10.1016/j.foodcont.2011.06.004

    Article  CAS  Google Scholar 

  4. Ostadrahimi A, Ashrafnejad F, Kazemi A, Sargheini N, Mahdavi R, Farshchian M (2014) Aflatoxin in raw and salt-roasted nuts (pistachios, peanuts and walnuts) sold in markets of Tabriz, Iran. Jundishapur J Microbiol 7(1):1–5

    Article  Google Scholar 

  5. Gacem MA, El Hadj-Khelil AO (2016) Toxicology, biosynthesis, bio-control of aflatoxin and new methods of detection. Asian Pac J Trop Biomed 6(9):808–814. https://doi.org/10.1016/j.apjtb.2016.07.012

    Article  Google Scholar 

  6. Enyiukwu DN, Awurum AN, Nwaneri JA (2014) Efficacy of plant-derived pesticides in the control of mycoinduced postharvest and storage rots of tubers and agricultural products: a review. Neth J Agric Sci 2(1):30–46

    Google Scholar 

  7. Tsitsigiannis DI, Dimakopoulou M, Antoniou PP, Tjamos EC (2012) Biological control strategies of mycotoxigenic fungi and associated mycotoxins in Mediterranean basin crops. Phytopathol Mediterr 51(1):158–174

    CAS  Google Scholar 

  8. Franz CM, Cho G, Holzapfel WH, Gálvez A (2010) Safety of lactic acid bacteria. In: Mozzi F, Raya R, Vignolo G (eds) Biotechnology of lactic acid bacteria novel applications. Wiley-Blackwell, Iowa. Organisation/Makerere Univ, p 27. https://doi.org/10.1002/9780813820866.ch19

    Chapter  Google Scholar 

  9. Vignolo G, Saavedra L, Sesma F, Raya R (2012) Food bioprotection: lactic acid bacteria as natural preservatives. In: Bhat R, Alias AK, Paliyath G (eds) Progress in food preservation. Wiley-Blackwell, Oxford. https://doi.org/10.1002/9781119962045.ch22

    Chapter  Google Scholar 

  10. Pedro MO, Emanuele Z, Elke KA (2014) Cereal fungal infection, mycotoxins, and lactic acid bacteria mediated bioprotection: from crop farming to cereal products. Food Microbiol 37:78–95

    Article  CAS  Google Scholar 

  11. Ghazvini RD, Kouhsari E, Zibafar E, Hashemi SJ, Amini A, Niknejad F (2016) Antifungal activity and aflatoxin degradation of Bifidobacterium bifidum and Lactobacillus fermentum against toxigenic Aspergillus Parasiticus. Open Microbiol J 10(1):197–201. https://doi.org/10.2174/1874285801610010197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Unnevehr L, Grace D (2013) Aflatoxins: finding solutions for improved food safety. Int Food Policy Res Inst 20:1–62

    Google Scholar 

  13. Jahanshiri Z, Shams-Ghahfarokhi M, Allameh A, Razzaghi-Abyaneh M (2015) Inhibitory effect of eugenol on aflatoxin B1 production in Aspergillus parasiticus by down regulating the expression of major genes in the toxin biosynthetic pathway. World J Microbiol Biotechnol 31(7):1071–1078. https://doi.org/10.1007/s11274-015-1857-7

    Article  CAS  PubMed  Google Scholar 

  14. Price MS, Yu J, Nierman WC, Kim HS, Pritchard B, Jacobus CA, Bhatnagar D, Cleveland TE, Payne GA (2006) The aflatoxin pathway regulator AflR induces gene transcription inside and outside of the aflatoxin biosynthetic cluster. FEMS Microbiol Lett 255(2):275–279. https://doi.org/10.1111/j.1574-6968.2005.00084.x

    Article  CAS  PubMed  Google Scholar 

  15. Yu J, Chang P, Ehrlich KC, Cary JW, Bhatnagar D, Cleveland TE, Payne GA, Linz JE, Woloshuk CP, Bennett JW (2004) Clustered pathway genes in aflatoxin biosynthesis. Appl Environ Microbiol 70(3):1253–1262. https://doi.org/10.1128/AEM.70.3.1253-1262.2004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Sicuia OA, Roming FI, Ciobotariu O, Materi A, Zamfir M, Ciuc M, Cornea CP (2014) Antifungal action of lactic acid bacteria isolated from plant materials against mycotoxigenic fungi. Sci Bull Ser F Biotechnol 18:234–240

    Google Scholar 

  17. Jaimez Ordaz J, Fente CA, Vázquez BI, Franco CM, Cepeda A (2003) Development of a method for direct visual determination of aflatoxin production by colonies of the Aspergillus flavus group. Int J Food Microbiol 83(2):219–225. https://doi.org/10.1016/S0168-1605(02)00362-8

    Article  CAS  PubMed  Google Scholar 

  18. Yazdani D, Zainal MA, Tan YH, Kamaruzaman S (2010) Evaluation of the detection techniques of toxigenic Aspergillus isolates. Afr J Biotechnol 9(45):7654–7659

    CAS  Google Scholar 

  19. Domsch KH, Gams W, Anderson TH (2007) Compendium of soil fungi. 2nd Edition IHW-Verlag Eching pp. 1–672

  20. Rushdy AA, Gomaa EZ (2013) Antimicrobial compounds produced by probiotic Lactobacillus brevis isolated from dairy products. Ann Microbiol 63(1):81–90. https://doi.org/10.1007/s13213-012-0447-2

    Article  CAS  Google Scholar 

  21. Daba H, Pandian S, Gosselin JF, Simard RE, Huang J, Lacroix C (1991) Detection and activity of bacteriocin produced by Leuconostoc mesenteriodes. Appl Environ Microbiol 57(12):3450–3455

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Oliver JD (2005) The viable but nonculturable state in bacteria. J Microbiol 43:93–100

    PubMed  Google Scholar 

  23. Rajaram G, Manivasagan P, Thilagavathi B, Saravanakumar A (2010) Purification and characterization of a bacteriocin produced by Lactobacillus lactis isolated from marine environment. Adv J Food Sci Technol 2:138–144

    CAS  Google Scholar 

  24. Rochelle PA, Will JAK, Fry JC, Jenkins GJS, Parkes RJ, Turley CM, Weightman AJ (1995) In: Trevors JT, van Elsas JD (eds) Nucleic acids in the environment. Springer, Berlin

    Google Scholar 

  25. Altschul SF, Thomas LM, Alejandro AS, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25(17):3389–3402. https://doi.org/10.1093/nar/25.17.3389

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. AOAC (1990) Official methods of analysis, 15th edn. Association of Official Analytical Chemists, Washington, DC, pp 252–483

    Google Scholar 

  27. Kim JG, Lee YW, Kim PG, Roh WS, Shintani H (2003) Reduction of aflatoxins by Korean soybean paste and its effect on cytotoxicity and reproductive toxicity—part 3. Inhibitory effects of Korean soybean paste (doen-jang) on aflatoxin toxicity in laying hens and aflatoxin accumulation in their eggs. J Food Prot 66(5):866–873. https://doi.org/10.4315/0362-028X-66.5.866

    Article  CAS  PubMed  Google Scholar 

  28. Ponce AG, Moreira MR, del Valle CE, Roura SI (2008) Preliminary characterization of bacteriocin-like substances from lactic acid bacteria isolated from organic leafy vegetables. Food Sci Technol 41:432–441

    CAS  Google Scholar 

  29. Csomós E, Simon-Sarkadi L (2002) Determination of biologically active compounds in Hungarian wines. Period Polytech Ser Chem Eng 46:73–81

    Google Scholar 

  30. Rodríguez A, Rodríguez M, Luque MI, Martín A, Córdoba JJ (2012) Real-time PCR assays for detection and quantification of aflatoxin-producing molds in foods. Food Microbiol 31(1):89–99. https://doi.org/10.1016/j.fm.2012.02.009

    Article  CAS  PubMed  Google Scholar 

  31. Mayer Z, Bagnara A, Färber P, Geisen R (2003) Quantification of the copy number of nor-1, a gene of the aflatoxin biosynthetic pathway by real-time PCR, and its correlation to the CFU of Aspergillus flavus in foods. Int J Food Microbiol 82(2):143–151. https://doi.org/10.1016/S0168-1605(02)00250-7

    Article  CAS  PubMed  Google Scholar 

  32. 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. Microbiology 153(8):2774–2780. https://doi.org/10.1099/mic.0.2006/005629-0

    Article  PubMed  Google Scholar 

  33. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:45–48

    Article  Google Scholar 

  34. Kurtar ES (2012) Modelling the effect of temperature on seed germination in some cucurbits. Afr J Biotechnol 9:1343–1353

    Google Scholar 

  35. 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 7:1–10

    Article  Google Scholar 

  36. Arasu MV, Al-Dhabi NA, Rejinieman TS, Lee KD, Huxley VAJ, Kim DH, Duraipandiyan V, Karuppiah P, Choi KC (2015) Identification and characterization of Lactobacillus brevis p68 with antifungal, antioxidant and probiotic functional properties. Indian J Microbiol 55(1):19–28. https://doi.org/10.1007/s12088-014-0495-3

    Article  CAS  Google Scholar 

  37. Asurmendi P, García MJ, Ruíz F, Dalcero A, Pascual L, Barberis L (2016) Biological control of AFB1-producing Aspergillus section Flavi strains isolated from brewer’s grains, alternative feed intended for swine production in Argentina. J Environ Sci Health B 51(7):477–481. https://doi.org/10.1080/03601234.2016.1159460

    Article  CAS  PubMed  Google Scholar 

  38. Gong HS, Meng XC, Wang H (2010) Plantaricin MG active against gram-negative bacteria produced by Lactobacillus plantarum KLDS1.0391 isolated from “Jiaoke”, a traditional fermented cream from China. Food Control 21(1):89–96. https://doi.org/10.1016/j.foodcont.2009.04.005

    Article  CAS  Google Scholar 

  39. Peltonen K, El-Nezami H, Haskard C, Ahokas J, Salminen S (2001) Aflatoxin B1 binding by dairy strains of lactic acid bacteria an d bifidobacteria. J Dairy Sci 84(10):2152–2156. https://doi.org/10.3168/jds.S0022-0302(01)74660-7

    Article  CAS  PubMed  Google Scholar 

  40. Haskard CA, El-Nezami HS, Kankaanpää PE, Salminen S, Ahokas JT (2001) Surface binding of aflatoxin B(1) by lactic acid bacteria. Appl Environ Microbiol 67(7):3086–3091. https://doi.org/10.1128/AEM.67.7.3086-3091.2001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Elsanhoty RM, Salam SA, Ramadan MF, Badr FH (2014) Detoxification of aflatoxin M1 in yoghurt using probiotics and lactic acid bacteria. Food Control 43:129–134. https://doi.org/10.1016/j.foodcont.2014.03.002

    Article  CAS  Google Scholar 

  42. Champe PC, Harvey RA (2012) Biochemistry, 2nd edn. Lippincott, New York, Illustrated Reviews, pp 2–11

    Google Scholar 

  43. Oluwafemi F, Kumar M, Bandyopadhyay R, Ogunbanwo T, Kayode B (2010) Bio-detoxification of aflatoxin B1 in artificially contaminated maize grains using lactic acid bacteria. Toxin Rev 29(3–4):115–122. https://doi.org/10.3109/15569543.2010.512556

    Article  CAS  Google Scholar 

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Acknowledgements

The authors would like to express their special thanks to Dr. Shafik Ibrahim, Agricultural Genetic Engineering Research Institute (AGERI), Agricultural Research Center (ARC), Giza, Egypt.

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Authors and Affiliations

  1. Department of Biological and Geological Sciences, Faculty of Education, Ain Shams University, Cairo, Egypt

    Eman Zakaria Gomaa & Omima Mohammed El-Mahdy

  2. Department of Microbial Molecular Biology, Agricultural Genetic Engineering Research Institute (AGERI), Agricultural Research Center (ARC), Giza, Egypt

    Manal Farouk Abdelall

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  1. Eman Zakaria Gomaa
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Correspondence to Eman Zakaria Gomaa.

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Gomaa, E.Z., Abdelall, M.F. & El-Mahdy, O.M. Detoxification of Aflatoxin B1 by Antifungal Compounds from Lactobacillus brevis and Lactobacillus paracasei, Isolated from Dairy Products. Probiotics & Antimicro. Prot. 10, 201–209 (2018). https://doi.org/10.1007/s12602-017-9350-2

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