PLANT BIOLOGY
ANIMAL BIOLOGY
SUBSCRIPTION
E-SUBSCRIPTION
 
MAP
MAIN PAGE

 

 

 

 

doi: 10.15389/agrobiology.2022.1.141eng

UDC: 636.086.1:636.085.19

Acknowledgements:
Supported by Russian Scientific Foundation (projects No. 19-76-10031 and No. 14-16-00150)

 

FAN EFFECTIVE AFLATOXIN B1 REDUCTION IN WHEAT GRAIN CONTAMINATED BY Aspergillus flavus VIA COMBINING THE BIOLOGICAL DEGRADATION OF THE TOXIN WITH INHIBITION OF ITS BIOSYNTHESIS

T.М. Voinova, L.А. Shcherbakova, S.B. Popletayeva, V.G. Dzhavakhiya

All-Russian Research Institute of Phytopathology, 5, ul. Institute, pos. Bol’shie Vyazemy, Odintsovskii Region, Moscow Province, 143050 Russia, e-mail tatiana.voinova@bk.ru, larisavniif@yahoo.com ( corresponding author), unavil@yandex.ru, dzhavakhiya@yahoo.com

ORCID:
Voinova T.М. orсid.org/0000-0002-7162-545Х
Popletayeva S.B. orсid.org/0000-0002-0341-9611
Shcherbakova L.А. orсid.org/0000-0003-0254-379X
Dzhavakhiya V.G. orсid.org/0000-0001-8704-0512

October 27, 2021

Decontamination of forage grain polluted with mycotoxins is one of the relevant problems of the forage safety provision. In recent years, the frequency of a severe contamination of forage grain and other fodder with aflatoxin B1 (AFB1) in Russia significantly increased. The probability of the AFB1 contamination of the grass stand and forage grain produced in the central and northern regions of Russia may increase in the future due to the further expansion of Aspergillus flavus fungus, the main AFB1 producer, into these regions as a result of climate change. One of the promising approaches to decontaminate grain contaminated with AFB1 is the toxin catabolization by various microorganisms producing enzymes able to degrade AFB1. Another approach includes the treatment of grain contaminated with the AFB1 producers with compounds able to inhibit the aflatoxigenesis. In the present work, it was shown for the first time that the treatment of the cultural broth of Rhodococcus erythropolus AC-884 with the supernatant after the treatment with compactin almost completely prevents the accumulation of mycotoxin in the infected grain. The aim of the work is to evaluate the effectiveness of reducing the content of mycotoxin in wheat grain artificially contaminated with aflatoxin B1 after treatment with actinobacteria of the genus Rhodococcus or an inhibitor of aflatoxygenesis, the compactin, as well as a combination of these methods. The present study reports the results of investigation of the AFB1 destruction capability in four Rhodococcus strains (Rhodococcus sp., AC-1260, R. erythropolus AC-1269 and АС-884, and R. ruber AC-1801). Quantitative analysis of AFB1 by high performance liquid chromatography revealed that the most active mycotoxin degradation occurred in the cell-free cultural broth supernatant of АС-884 (СBS-884). Only trace amounts of AFB1 added in CBS-17 to a final concentration of 0.2 µg/ml were detected in this supernatant after 48-h incubation at 30 °C, whereas cultural broth supernatants of other studied strains contained from 15 to 50 % of the added AFB1 after its incubation under the same conditions. A 72-h treatment of wheat (Triticum aestivum L., cv. Daria) grain artificially contaminated with AFB1 (1.0, 2.5, or 5.0 mg/g) with CBS-884 removed 60 % of the toxin, while the use of cultural broth supernatants or cell suspensions of AC-1260, AC-1269 or AC-1801 strains did not result in any changes in the AFB1 content comparing to the control. Using a consecutive treatment of grain infected with a toxigenic Aspergillus flavus strain by compactin, inhibiting the AFB1 production in this fungus, and then by CBS-884, we first demonstrated that the approach based on application of AFB1 biosynthesis inhibitors followed by the toxin biodegradation allowed an efficient decontamination of grain if the use of inhibitors alone did not result in a complete suppression of the aflatoxigenesis. Grain treatment of with the supernatant of AC-884 was more effective than the treatment with a similarly obtained supernatant of another АFB1-destroiyng agent, Phoma glomerata PG-41. In our experiments, the AFB1 content in wheat grain contaminated with A. flavus А11 reduced twice compared to the control in 7 days after compactin (0.05 mg/g) application. In 24 h after the treatment of the contaminated grain with CBS-884 alone (0.25 ml/g), the AFB1 amount produced by A. flavus for six post-inoculation days was reduced almost thrice. Combination of both treatments (compactin, 0.05 mg/g, and then CBS-884, 0.25 ml/g) resulted in a more than 200-fold reduction of the AFB1 content and the achievement of almost complete grain decontamination. Therefore, an approach based on a combination of biodegradation with inhibition of aflatoxigenesis can provide effective decontamination of grain contaminated with AFB1 producers in cases where the use of inhibitors does not lead to complete suppression of mycotoxin biosynthesis.

Keywords: aflatoxin B1, forage, grain, decontamination, Aspergillus flavus, compactin, Rhodococcus erythropolus.

 

REFERENCES

  1. Borutova R., Aidinyan G. Zhivotnovodstvo Rossii, 2021, 4: 54-59 (in Russ.).
  2. Iyldyrym E.A., Il'ina L.A., Filippova V.A., Soldatova V.V., Nikonov I.N., Laptev G.Yu., Sokolova O.V., Novikova N.I. Kormoproizvodstvo, 2016, 3: 41-45 (in Russ.).
  3. Tanaseva S.A., Bosyakov I.V. Materialy Mezhdunarodnoi nauchno-prakticheskoi konferentsii, posvyashchennoi 90-letiyu so dnya rozhdeniya professora V.A. Kirshina [Proc. Int. Conf. dedicated to the 90th anniversary of the birth of Professor V.A. Kirshina]. Kazan', 2018: 191-193 (in Russ.).
  4. Sedova I.B., Zakharova L.P., Kiseleva M.G., Chalyi Z.A., Tutel'yan V.A. Nauchnye trudy SKFNTSSVV, 2018, 21: 129-137 (in Russ.).
  5. Miroshnichenko P.V., Panfilkina E.V., Okolot M.V. Sbornik nauchnykh trudov FGBNU KNTsZV, 2020, 9(2): 109-111 CrossRef (in Russ.).
  6. Kovalenko A., Soldatenko N., Fetisov L., Sukhikh E. Kombikorma, 2011, 3: 98-99 (in Russ.).
  7. Semenov E.I., Papunidi K.Kh., Tremasov M.Ya. Mikotoksikozy v APK: rasprostranenie, diagnostika, profilaktika [Mycotoxicoses in the agro-industrial complex: distribution, diagnosis, prevention]. Available: http://soyanews.info/news/mikotoksikozy_v_apk-_rasprostranenie-_diagnostika-_profilaktika.html. Accessed: 14.10.2021 (in Russ.).
  8. Aflatoxins — biochemistry and molecular biology. R.G. Guevara-González (ed.). InTech, London, 2000 CrossRef
  9. Molecular and applied aspects of oxidative drug metabolizing enzymes. E. Arinç, J.B. Schenkman, E. Hodgson (eds.). Springer, New York, 1999 CrossRef
  10. Yang C., Song G., Lim W. Effects of mycotoxin-contaminated feed on farm animals. Journal of Hazardous Materials,2020, 389: 122087 CrossRef
  11. Min L., Fink-Gremmels J., Li D., Tong X., Tang J., Nan X., Yu Z., Chen W., Wang G. An overview of aflatoxin B1 biotransformation and aflatoxin M1 secretion in lactating dairy cows. Animal Nutrition, 2020, 7(1): 42-48 CrossRef
  12. Dzhavakhiya V.G., Statsyuk N.V., Shcherbakova L.A., Popletaeva S.B. Aflatoksiny: ingibirovanie biosinteza, profilaktika zagryazneniya i dekontaminatsiya agroproduktsii [Aflatoxins: biosynthesis inhibition, pollution prevention and decontamination of agricultural products]. Moscow, 2017 (in Russ.).
  13. Sipos P., Peles F., Brassó D.L., Béri B., Pusztahelyi T., Pócsi I., Győri Z. Physical and chemical methods for reduction in aflatoxin content of feed and food. Toxins, 2021, 13(3): 204 CrossRef
  14. Lyagin I., Efremenko E. Enzymes for detoxification of various mycotoxins: origins and mechanisms of catalytic action. Molecules, 2019, 24(13): 2362 CrossRef
  15. Loi M., Fanelli F., Zucca P., Liuzzi V.C., Quintieri L., Cimmarusti M.T., Monaci L., Haidukowski M., Logrieco A.F., Sanjust E., Mulè G. Aflatoxin B1 and M1 degradation by Lac2 from Pleurotus pulmonarius and redox mediators. Toxins, 2016, 8(9): 245 CrossRef
  16. 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 Microbiology Letters, 2011, 314(2): 164-169 CrossRef
  17. 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. Microbiological Research, 2011, 166(6): 475-483 CrossRef
  18. Wu Y.Z., Lu F.P., Jiang H.L., Tan C.P., Yao D.S., Xie C.F., Liu D.L. The furofuran-ring selectivity, hydrogen peroxide-production and low Km value are the three elements for highly effective detoxification of aflatoxin oxidase. Food and Chemical Toxicology, 2015, 76: 125-131 CrossRef
  19. Krifaton C., Kriszt B., Szoboszlay S., Cserháti M., Szűcs A., Kukolya J. Analysis of aflatoxin-B1-degrading microbes by use of a combined toxicity-profiling method. Mutation Research, 2011, 726(1): 1-7 CrossRef
  20. Cserháti M., Kriszt B., Krifaton C., Szoboszlay S., Háhn J., Tóth S., Nagy I., Kukolya J. Mycotoxin-degradation profile of Rhodococcus strains. International Journal of Food Microbiology, 2013, 166(1): 176-185 CrossRef
  21. Eshelli M., Harvey L., Edrada-Ebel R., McNeil B. Metabolomics of the bio-degradation process of aflatoxin B1 by Actinomycetes at an initial pH of 6.0. Toxins, 2015, 7(2): 439-456 CrossRef
  22. Risa A., Divinyi D.M., Baka E., Krifaton C. Aflatoxin B1 detoxification by cell-free extracts of Rhodococcus strains. Acta Microbiologica et Immunologica Hungarica, 2017, 64(4): 423-438 CrossRef
  23. Prettl Z., Dési E., Lepossa A., Kriszt B., Kukolya J., Nagy E. Biological degradation of aflatoxin B1 by a Rhodococcus pyridinivorans strain in by-product of bioethanol. Animal Feed Science and Technology, 2017, 224: 104-114 CrossRef
  24. Dzhavakhiya V.G., Voinova T.M., Popletaeva S.B., Statsyuk N.V., Limantseva L.A., Shcherbakova L.A. Effect of various compounds blocking the colony pigmentation on the aflatoxin B1 production by Aspergillus flavus. Toxins, 2016, 8(11): 313 CrossRef
  25. Dudchik N.V., Drozdova E.V., Treilib V.V., Budkina E.A., Buraya V.V., Kozlova T.O., Ushkova L.L. Otsenka integral'noi toksichnosti ob"ektov okruzhayushchei sredy metodami biotestirovaniya (instruktsiya po primeneniyu) [Assessment of the integral toxicity of environmental objects by biotesting methods (instruction for use)]. Minsk, 2012 (in Russ.).
  26. Shcherbakova L.A., Statsyuk N.V., Mikityuk O.D., Nazarova T.A., Dzhavakhiya V.G. Aflatoxin B1 degradation by metabolites of Phoma glomerata PG41 isolated from natural substrate colonized by aflatoxigenic Aspergillus flavus. Jundishapur Journal of Microbiology, 2015, 8(1): e24324 CrossRef
  27. Vankayalapati V.K. Aflatoxins: properties, toxicity and detoxification. Nutrition and Food Science International Journal, 2018, 6(5): 555696 CrossRef
  28. Ukraintseva S.N., Voinova T.M., Dzhavakhiya V.G. Obtaining the highly productive mutants Penicillium citrinum producing compactin and optimization of fermentation process in shaken flasks. In: Biotechnology in biology and medicine. A.M. Egorov, G. Zaikov (eds.). Nova Science Publishers, New York, 2006.
  29. Bueno D.J., Casale C.H., Pizzolitto R.P., Salvano M.A., Oliver G. Physical adsorption of aflatoxin B1 by lactic acid bacteria and Saccharomyces cerevisiae: a theoretical model. Journal of Food Protection, 2007, 70(9): 2148-2154 CrossRef
  30. Peltonen K., El-Nezami H., Haskard C., Ahokas J., Salminen S. Aflatoxin B1 binding by dairy strains of lactic acid bacteria and bifidobacteria. Journal of Dairy Science, 2001, 84(10): 2152-2156 CrossRef
  31. Ondiek W., Wang Y., Sun L., Zhou L., On S.L., Zheng H., Ravi G. Removal of aflatoxin b1 and t-2 toxin by bacteria isolated from commercially available probiotic dairy foods. Food Science and Technology International, 2021, 28(1): 15-25 CrossRef
  32. Hahn I., Thamhesl M., Apfelthaler E., Klingenbrunner V., Hametner C., Krska R., Schatzmayr G., Moll W.-D., Berthiller F., Schwartz-Zimmermann H.E. Characterisation and determination of metabolites formed by microbial and enzymatic degradation of ergot alkaloids. World Mycotoxin Journal, 2015, 8(4): 393-404 CrossRef
  33. Alberts J.F., Engelbrecht Y., Steyn P.S., Holzapfel W.H., van Zyl W.H. Biological degradation of aflatoxin B1 by Rhodococcus erythropolis cultures. International Journal of Food Microbiology, 2006, 109(1-2): 121-126 CrossRef
  34. Rodriguez H., Reveron I., Doria F., Costantini A., De Las Rivas B., Munoz R., Garcia-Moruno E. Degradation of ochratoxin A by Brevibacterium species. Journal of Agricultural and Food Chemistry, 2011, 59(19): 10755-10760 CrossRef
  35. Mikityuk O.D., Voinova T.M., Dzhavakhiya V.G. Materialy Mezhdunarodnoi nauchnoi konferentsii «Aktual'nye voprosy organicheskoi khimii i biotekhnologii» [Proc. Conf. «Topical issues of organic chemistry and biotechnology»]. Ekaterinburg, 2020, vol. 1: 659-660 (in Russ.).

 

back

 


CONTENTS

 

 

Full article PDF (Rus)

Full article PDF (Eng)