Detoxification and anti-mycotoxigenic effect of Ochratoxin A produced by Penicillium expansum species utilizing probiotic Pichia kudriavzevii and biogenic-selenium nano-formulations

Eman Ahmed Mohamed Helmy

doi:10.7324/JAPS.2019.S101

Abstract References Article Metrics Similar Articles Request Permission Related Search Citation Alert By Google Scholar Comment On This Article

Abstract

Ochratoxins (OT) are overall spread fungal secondary metabolites combined chiefly by some toxigenic types of Aspergillus and Penicillium. A few physical, chemical, and biological techniques were found among literary reports to wipe out, inactivate, or decrease the bioavailability of mycotoxins counting ochratoxin A (OTA). The aim of this study was to evaluate the combined inhibitory capacity of selenium nanoparticles (SeNPs) and probiotic yeast Pichia kudriavzevii on OTA production by seven mycotoxigenic Penicillium expansum strains. The detoxification capability of OTA was tested using thin-layer chromatography (TLC) and high-performance liquid chromatography (HPLC) techniques. The mixture of the probiotic P. kudriavzevii and SeNPs demonstrated that most of OTA reduction rate created by P. expansum5 by a rate of (58.38%). While the least OTA removal rate was delivered by P. expansum3 by (34.47%) treated with SeNPs as it were. The ultrastructural investigations of P. expansum5 cells completed with transmission electron microscopy demonstrated among the cytoplasmic constituents of P. expansum5 cells treated with the previous mix of probiotic and SeNPs that were totally contracted and pulled back far from the cell membrane leaving a gigantic separation region of no organelles. Remarkable cytoplasmic ultra-structure’s deformations of cells were additionally recorded accompanied with a vacuolation as a survival adaptation mode of fungal cells. Conclusively, a strategy of combined probiotic yeast P. kudriavzevii and biogenic-SeNPs is useful as natural blends for detoxification, anti-mycotoxigenic, and/or reduction of OTA production by mycotoxigenic fungal species of P. expansum. This natural mixture could be recommended as food/feed preservative and as a prophylactic agent in pre- and post-harvest crops.

Keyword: OTA Detoxification Probiotic Pichia kudriavzevii Biogenic-Selenium Nano.

Citation:

Helmy EAM. Detoxification and anti-mycotoxigenic of Ochratoxin A produced by Penicillium expansum species utilizing probiotic Pichia kudriavzevii and biogenic-selenium nano-formulations. J Appl Pharm Sci, 2019; 9(S1): 001–008.

Copyright: © The Author(s). This is an open-access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

HTML Full Text

Reference

Adegoke GO, Letuma P. Strategies for the prevention and reduction of Mycotoxins in developing countries. In: Makun HA (ed.). Book chapter of mycotoxin and food safety in developing countries— Mycotoxicology. InTech Janeza Trdine 9, Rijeka, Croatia, pp 123–37, 2013.
Ammar HAM, Helmy EA. Ecophysiological conditions affecting growth and ochratoxin A production by novel Aspergillus terreusHA2 and Aspergillus fumigatusHA1 isolated from Egyptian rice grains. Egypt J Bot, 2015; 12(2):11–22.
Aniket L, Roch-Chui Y, Cheng-Chun C, Je-Ruei L, Kuan-Chen C. Protective and detoxifying effects conferred by dietary selenium and curcumin against AFB1-mediated toxicity in livestock: a review. Toxins, 2018; 10(25):1–18.
Association of Official Analytical Chemists (AOAC). Official methods of analysis 18th AOAC, Method 971.22. Published Chemists, Washington, DC, 2005.
Applegate KL, Chipley JR. Production of ochratoxin A by Aspergillus ochraceous NRRL-3174 before and after exposure with 60Co irradiation. Appl Environ Microbiol, 1976; 31:349–53.
Asmathunisha N, Kathiresan KA. Review on biosynthesis of nanoparticles by marine organisms. Colloid Surf B Biointerfaces, 2013; 103:283–7. https://doi.org/10.1016/j.colsurfb.2012.10.030
Bragulat MR, Abarca ML, Cabanes FJ. An easy screening method for fungi producing OTA in pure cultures. Int J Food Microbiol, 2001; 71:139–44. https://doi.org/10.1016/S0168-1605(01)00581-5
Dalie D, Pinson-Gadais L, Atanasova-Penichon V, Marchegay G, Barreau C, Deschamps A, Richard-Forget F. Impact of Pediococcus pentosaceus strain L006 and its metabolites on fumonisin biosynthesis by Fusarium verticillioides. Food Control, 2012; 23(2):405–11. https://doi.org/10.1016/j.foodcont.2011.08.008
Dorner JW, Cole RJ, Connick WJ, Daigle DJ, McGuire MR, Shasha BS. Evaluation of biological control formulations to reduce aflatoxin contamination in peanuts. Biocontrol, 2003; 26:318–24.
El-Desouky TA, Ammar HAM. Honey mediated silver nanoparticles and their inhibitory effect on aflatoxins and ochratoxin A. J Appl Pharm Sci, 2016; 6(06):83–90. https://doi.org/10.7324/JAPS.2016.60615
Fink-Gremmels J, Malekinejad H. Clinical effects and biochemical mechanisms associated with exposure to the mycoestrogen zearalenone. Ani Feed Sci Technol, 2007; 137:326–41. https://doi.org/10.1016/j.anifeedsci.2007.06.008
Gabriel O. Adegoke and Puleng Letuma. (2013). Strategies for the prevention and reduction of Mycotoxins in developing countries. Book chapter of mycotoxin and food safety in developing countries – Mycotoxicology, Edited by Hussaini Anthony Makun. Published by InTech Janeza Trdine 9, 51000 Rijeka, Croatia. 123-137.
Gil de los Santos D, Gil de los Santos JR, Gil-Turnes C, Gaboardi G, Fernandes Silva L, FrancËa R. Probiotic effect of pastoris X-33 produced in parboiled rice effluent and YPD medium on broiler chickens. PLoS ONE, 2018; 13(2):e0192904. https://doi.org/10.1371/journal.pone.0192904
Härdle W, Simar L. Applied multivariate statistical analysis. 2nd edition, Springer, Heidelberg, p 420, 2007.
Helmy EA. Nano-biotechnology breakthrough and food-packing industry. Microbial Biosystems, 2016; 1(1):50–69. https://doi.org/10.21608/mb.2016.5257
Helmy EA, Abdul Aziz SS. In vitro isolation and evaluation of probiotic attributes of three dairy yeast isolates against clinical and food-borne pathogens, 2018 (Unpublished Data).
Helmy EA, Mekawey AA. Envision of the microbial contact with mycosynthesized silver nanoparticles. Res J Pharm Biol Chem Sci, 2014; 5(5):344–54.
Helmy EA, Shehata RM, Abdul Aziz SS. Ecofriendly green biogenic synthesis of selenium nano spheres by Trichoderma harzianum, 2018 (Unpublished Data).
Huo S, Jin S, Ma X, Xue X, Yang K, Kumar A, Wang PC, Zhang J, Hu Z, Liang XJ. Ultrasmall gold nanoparticles as carriers for nucleus-based gene therapy due to size-dependent nuclear entry. ACS Nano J, 2014; 8(6):5852–62. https://doi.org/10.1021/nn5008572
Khalil AA, Abou-Gabal AE, Elfaramawy AM, Khaled AE, Abdellatef AA. Lactic acid bacteria as antimycotic and antimycotoxins agents against Toxigenic Fusarium species associated to maize grains stored in Egyptian markets. J Pure Appl Microbiol, 2013; 7(Spl. Edn.):93–105.
Kim JS, Kuk E, Yu KN, Kim JH, Park SJ. Antimicrobial effects of silver nanoparticles. Nanomed Nanotechnol Biol Med, 2007; 3:95–101. https://doi.org/10.1016/j.nano.2006.12.001
Koteswara RV, Aruna B, Girisham S, Madhusudhan RS. Effect of indigenous fungi on ochratoxin A produced by two species of Penicillium. Ani Nutr, 2016; 2:225–8. https://doi.org/10.1016/j.aninu.2016.04.004
Kuiper-Goodman T, Scott PM. Risk assessment of the mycotoxin ochratoxin A. Biomed Environ Sci, 1989; 2:179–248.
Leonardo P, Corbo MR, Milena S, Antonio B. Ochratoxin A removal by yeasts after exposure to simulated human gastrointestinal conditions. J Food Sci, 2016; 81(11):12–24.
Mahoney M, Molyneux RJ, Kim JH, Campbell BC, Waiss AC, Hagerman AE. Aflatoxigenesis induced in Aspergillus flavus by oxidative stress and reduction by phenolic antioxidants from tree nuts. World Mycotoxin J, 2010; 3(1):49–57. https://doi.org/10.3920/WMJ2009.1185
McCormick S. Microbial detoxification of mycotoxins. J Chem Ecol, 2013; 39:907–18. https://doi.org/10.1007/s10886-013-0321-0
Mekawey AI, Helmy EA. Elucidative physiological optimization of silver nanospheres biogenesis by molds. Int J Nanotechnol Allied Sci, 2017; 1(1):30–44.
Nido SA, Shituleni SA, Mengistu BM, Liu Y, Khan AZ, Gan F, Kumbhar S, Huang K. Effects of selenium-enriched probiotics on lipid metabolism, antioxidative status, histopathological lesions, and related gene expression in mice fed a high-fat diet. Biol Trace Elem Res, 2016; 171(2):399–409. https://doi.org/10.1007/s12011-015-0552-8
O'Brien E, Dietrich DR. Ochratoxin A: the continuing enigma. Crit Rev Toxicol, 2005; 35:33–60. https://doi.org/10.1080/10408440590905948
Parsameher N, Rezaei S, Khodavasiy S, Salari S, Hadizade S, Kord M, Ayatollahi Mousavi SA. Effect of biogenic selenium nanoparticles on ERG11 and CDR1 gene expression in both fluconazole-resistant and -susceptible Candida albicans isolates. Curr Med Mycol, 2017; 3(3):16–20. https://doi.org/10.29252/cmm.3.3.16
Paster N, Barkai-Golan R, Padova R. Effect of gamma radiation on ochratoxin production by the fungus Aspergillus ochraceus. J Sci Food Agric, 1985; 36:445–9. https://doi.org/10.1002/jsfa.2740360604
Pfohl-Leszkowicz A, Grosse Y, Castegnaro M, Nicolov IG, Chernozemsky IN, Bartsch H, Betbeder AM, Creppy EE, Dirheimer G. Ochratoxin A-related DNA adducts in urinary tract tumors of Bulgarian subjects. IARC Sci Publ, 1993; 124:141–8.
Qi L, Li Y, Luo X, Wang R, Zheng R, Wang L, Li Y, Yang D, Fang W, Chen Z. Detoxification of zearalenone and ochratoxin A by ozone and qual¬ity evaluation of ozonized corn. J Food Addit Contam 2016; 33(HYPERLINK "https://www.tandfonline.com/toc/tfac20/33/11" 11):12–24.
Saeger SD, Kris A, Siska C. Report from the 5th International Symposium on Mycotoxins and Toxigenic Moulds: Challenges and Perspectives (MYTOX) Held in Ghent, Belgium, May 2016. Toxins 2016; 8:146–83. https://doi.org/10.3390/toxins8050146
Samson RA, Hoekstra ES, Frisvad JC, Filtenborg O. Introduction to food- and airborne fungi. Centraalbureau voor Schimmelcultures-Utrecht, Utrecht, The Netherlands, 389 p, 2000.
Stoimenov PK, Klinger RL, Marchin GL, Klabunde KJ. Metal oxide nanoparticles as bactericidal agents. Langmuir, 2002; 18:6679–86. https://doi.org/10.1021/la0202374
Thalita C, Fernández-Cruzb ML, Verdec SC, Armando V, Luís A. Gamma irradiation effects on ochratoxin A: Degradation, cytotoxicity and application in food. Food Chem, 2018; 240:463–71. https://doi.org/10.1016/j.foodchem.2017.07.136
Yamazaki M, Maebayashi Y, Miyaki K. Production of Ochratoxin A by Aspergillus ochraceous isolated in Japan from moldy rice. Appl Microbiol, 1970; 20: 452–4.
Yehia RS, Ahmed OS. In vitro study of the antifungal efficacy of zinc oxide nanoparticles against Fusarium oxysporum and Penicillium expansum. Afr J Microbiol Res, 2013; 7(19):1917–23. https://doi.org/10.5897/AJMR2013.5668

Article Metrics

481 Views 92 Downloads 573 Total

Year

Month

Related Search

By author names

Helmy E A M [PubMed] [Google Scholar ]

By article title

Adegoke GO, Letuma P. Strategies for the prevention and reduction of Mycotoxins in developing countries. In: Makun HA (ed.). Book chapter of mycotoxin and food safety in developing countries— Mycotoxicology. InTech Janeza Trdine 9, Rijeka, Croatia, pp 123–37, 2013.

Ammar HAM, Helmy EA. Ecophysiological conditions affecting growth and ochratoxin A production by novel Aspergillus terreusHA2 and Aspergillus fumigatusHA1 isolated from Egyptian rice grains. Egypt J Bot, 2015; 12(2):11–22.

Aniket L, Roch-Chui Y, Cheng-Chun C, Je-Ruei L, Kuan-Chen C. Protective and detoxifying effects conferred by dietary selenium and curcumin against AFB1-mediated toxicity in livestock: a review. Toxins, 2018; 10(25):1–18.

Association of Official Analytical Chemists (AOAC). Official methods of analysis 18th AOAC, Method 971.22. Published Chemists, Washington, DC, 2005.

Applegate KL, Chipley JR. Production of ochratoxin A by Aspergillus ochraceous NRRL-3174 before and after exposure with 60Co irradiation. Appl Environ Microbiol, 1976; 31:349–53.

Asmathunisha N, Kathiresan KA. Review on biosynthesis of nanoparticles by marine organisms. Colloid Surf B Biointerfaces, 2013; 103:283–7. https://doi.org/10.1016/j.colsurfb.2012.10.030

Bragulat MR, Abarca ML, Cabanes FJ. An easy screening method for fungi producing OTA in pure cultures. Int J Food Microbiol, 2001; 71:139–44. https://doi.org/10.1016/S0168-1605(01)00581-5

Dalie D, Pinson-Gadais L, Atanasova-Penichon V, Marchegay G, Barreau C, Deschamps A, Richard-Forget F. Impact of Pediococcus pentosaceus strain L006 and its metabolites on fumonisin biosynthesis by Fusarium verticillioides. Food Control, 2012; 23(2):405–11. https://doi.org/10.1016/j.foodcont.2011.08.008

Dorner JW, Cole RJ, Connick WJ, Daigle DJ, McGuire MR, Shasha BS. Evaluation of biological control formulations to reduce aflatoxin contamination in peanuts. Biocontrol, 2003; 26:318–24.

El-Desouky TA, Ammar HAM. Honey mediated silver nanoparticles and their inhibitory effect on aflatoxins and ochratoxin A. J Appl Pharm Sci, 2016; 6(06):83–90. https://doi.org/10.7324/JAPS.2016.60615

Fink-Gremmels J, Malekinejad H. Clinical effects and biochemical mechanisms associated with exposure to the mycoestrogen zearalenone. Ani Feed Sci Technol, 2007; 137:326–41. https://doi.org/10.1016/j.anifeedsci.2007.06.008

Gabriel O. Adegoke and Puleng Letuma. (2013). Strategies for the prevention and reduction of Mycotoxins in developing countries. Book chapter of mycotoxin and food safety in developing countries – Mycotoxicology, Edited by Hussaini Anthony Makun. Published by InTech Janeza Trdine 9, 51000 Rijeka, Croatia. 123-137.

Gil de los Santos D, Gil de los Santos JR, Gil-Turnes C, Gaboardi G, Fernandes Silva L, FrancËa R. Probiotic effect of pastoris X-33 produced in parboiled rice effluent and YPD medium on broiler chickens. PLoS ONE, 2018; 13(2):e0192904. https://doi.org/10.1371/journal.pone.0192904

Härdle W, Simar L. Applied multivariate statistical analysis. 2nd edition, Springer, Heidelberg, p 420, 2007.

Helmy EA. Nano-biotechnology breakthrough and food-packing industry. Microbial Biosystems, 2016; 1(1):50–69. https://doi.org/10.21608/mb.2016.5257

Helmy EA, Abdul Aziz SS. In vitro isolation and evaluation of probiotic attributes of three dairy yeast isolates against clinical and food-borne pathogens, 2018 (Unpublished Data).

Helmy EA, Mekawey AA. Envision of the microbial contact with mycosynthesized silver nanoparticles. Res J Pharm Biol Chem Sci, 2014; 5(5):344–54.

Helmy EA, Shehata RM, Abdul Aziz SS. Ecofriendly green biogenic synthesis of selenium nano spheres by Trichoderma harzianum, 2018 (Unpublished Data).

Huo S, Jin S, Ma X, Xue X, Yang K, Kumar A, Wang PC, Zhang J, Hu Z, Liang XJ. Ultrasmall gold nanoparticles as carriers for nucleus-based gene therapy due to size-dependent nuclear entry. ACS Nano J, 2014; 8(6):5852–62. https://doi.org/10.1021/nn5008572

Khalil AA, Abou-Gabal AE, Elfaramawy AM, Khaled AE, Abdellatef AA. Lactic acid bacteria as antimycotic and antimycotoxins agents against Toxigenic Fusarium species associated to maize grains stored in Egyptian markets. J Pure Appl Microbiol, 2013; 7(Spl. Edn.):93–105.

Kim JS, Kuk E, Yu KN, Kim JH, Park SJ. Antimicrobial effects of silver nanoparticles. Nanomed Nanotechnol Biol Med, 2007; 3:95–101. https://doi.org/10.1016/j.nano.2006.12.001

Koteswara RV, Aruna B, Girisham S, Madhusudhan RS. Effect of indigenous fungi on ochratoxin A produced by two species of Penicillium. Ani Nutr, 2016; 2:225–8. https://doi.org/10.1016/j.aninu.2016.04.004

Kuiper-Goodman T, Scott PM. Risk assessment of the mycotoxin ochratoxin A. Biomed Environ Sci, 1989; 2:179–248.

Leonardo P, Corbo MR, Milena S, Antonio B. Ochratoxin A removal by yeasts after exposure to simulated human gastrointestinal conditions. J Food Sci, 2016; 81(11):12–24.

Mahoney M, Molyneux RJ, Kim JH, Campbell BC, Waiss AC, Hagerman AE. Aflatoxigenesis induced in Aspergillus flavus by oxidative stress and reduction by phenolic antioxidants from tree nuts. World Mycotoxin J, 2010; 3(1):49–57. https://doi.org/10.3920/WMJ2009.1185

McCormick S. Microbial detoxification of mycotoxins. J Chem Ecol, 2013; 39:907–18. https://doi.org/10.1007/s10886-013-0321-0

Mekawey AI, Helmy EA. Elucidative physiological optimization of silver nanospheres biogenesis by molds. Int J Nanotechnol Allied Sci, 2017; 1(1):30–44.

Nido SA, Shituleni SA, Mengistu BM, Liu Y, Khan AZ, Gan F, Kumbhar S, Huang K. Effects of selenium-enriched probiotics on lipid metabolism, antioxidative status, histopathological lesions, and related gene expression in mice fed a high-fat diet. Biol Trace Elem Res, 2016; 171(2):399–409. https://doi.org/10.1007/s12011-015-0552-8

O'Brien E, Dietrich DR. Ochratoxin A: the continuing enigma. Crit Rev Toxicol, 2005; 35:33–60. https://doi.org/10.1080/10408440590905948

Parsameher N, Rezaei S, Khodavasiy S, Salari S, Hadizade S, Kord M, Ayatollahi Mousavi SA. Effect of biogenic selenium nanoparticles on ERG11 and CDR1 gene expression in both fluconazole-resistant and -susceptible Candida albicans isolates. Curr Med Mycol, 2017; 3(3):16–20. https://doi.org/10.29252/cmm.3.3.16

Paster N, Barkai-Golan R, Padova R. Effect of gamma radiation on ochratoxin production by the fungus Aspergillus ochraceus. J Sci Food Agric, 1985; 36:445–9. https://doi.org/10.1002/jsfa.2740360604

Pfohl-Leszkowicz A, Grosse Y, Castegnaro M, Nicolov IG, Chernozemsky IN, Bartsch H, Betbeder AM, Creppy EE, Dirheimer G. Ochratoxin A-related DNA adducts in urinary tract tumors of Bulgarian subjects. IARC Sci Publ, 1993; 124:141–8.

Qi L, Li Y, Luo X, Wang R, Zheng R, Wang L, Li Y, Yang D, Fang W, Chen Z. Detoxification of zearalenone and ochratoxin A by ozone and qual¬ity evaluation of ozonized corn. J Food Addit Contam 2016; 33(HYPERLINK "https://www.tandfonline.com/toc/tfac20/33/11" 11):12–24.

Saeger SD, Kris A, Siska C. Report from the 5th International Symposium on Mycotoxins and Toxigenic Moulds: Challenges and Perspectives (MYTOX) Held in Ghent, Belgium, May 2016. Toxins 2016; 8:146–83. https://doi.org/10.3390/toxins8050146

Samson RA, Hoekstra ES, Frisvad JC, Filtenborg O. Introduction to food- and airborne fungi. Centraalbureau voor Schimmelcultures-Utrecht, Utrecht, The Netherlands, 389 p, 2000.

Stoimenov PK, Klinger RL, Marchin GL, Klabunde KJ. Metal oxide nanoparticles as bactericidal agents. Langmuir, 2002; 18:6679–86. https://doi.org/10.1021/la0202374

Thalita C, Fernández-Cruzb ML, Verdec SC, Armando V, Luís A. Gamma irradiation effects on ochratoxin A: Degradation, cytotoxicity and application in food. Food Chem, 2018; 240:463–71. https://doi.org/10.1016/j.foodchem.2017.07.136

Yamazaki M, Maebayashi Y, Miyaki K. Production of Ochratoxin A by Aspergillus ochraceous isolated in Japan from moldy rice. Appl Microbiol, 1970; 20: 452–4.

Yehia RS, Ahmed OS. In vitro study of the antifungal efficacy of zinc oxide nanoparticles against Fusarium oxysporum and Penicillium expansum. Afr J Microbiol Res, 2013; 7(19):1917–23. https://doi.org/10.5897/AJMR2013.5668