Abstract
The present study aimed to evaluate the binding capacity and stability of ochratoxin A (10 µg/kg; OTA) by single and co-culture Lactobacillus acidophilus + Lactobacillus rhamnosus in various modes including viable, heat-, and ultrasound-inactivated cells as well as a combination of viable + heat- or ultrasound-inactivated cells. The stability of OTA binding on native and modified lactic acid bacteria (LAB) surface was conducted after washing with solvent. The highest OTA adsorption capacity and stability (μg/kg) were obtained after co-culture L. acidophilus + L. rhamnosus in the following order: ultrasound-treated (8.418 and 7.829) > viable + ultrasound-treated (8.376 and 7.204) > heat-treated (7.588 and 6.987) > viable + heat-treated (7.536 and 6.483) > viable (7.425 and 5.157). The surface hydrophobicity obtained by spectrophotometry (%) enhanced from 40.5% in viable to 71.9% and 60.6% in ultrasound and heat-treated L. acidophilus + L. rhamnosus. α-helix and β-turn structures in L. acidophilus + L. rhamnosus reduced to (20.7 and 22.6%) and (26.9 and 27.2%) further LAB inactivated by thermosensation and heating compared to α-helix and β-turn structures in viable LAB, respectively (16.1 and 26.1%). To prove that the reduction of the OTA by LAB caused a substantial reduction of their toxic performances, micronucleus (MN) experiments were carried out with human-derived hepatoma cell line cells. Indeed, a considerable decrease of OTA caused a substantial reduction of MN induction and the inhibition of the cell division rates (i.e., the decline of BNC formation) by the OTA was significantly reduced in the ultrasonicated L. acidophilus + L. rhamnosus.
Similar content being viewed by others
Data Availability
Research data are not shared.
Abbreviations
- LAV:
-
Viable L. acidophilus
- LRV:
-
Viable L. rhamnosus
- LARV:
-
Viable L. acidophilus + L. rhamnosus
- LAVH:
-
Viable + heat-treated L. acidophilus
- LRVH:
-
Viable + heat-treated L. rhamnosus
- LARVH:
-
Viable + heat-treated L. acidophilus + L. rhamnosus
- LAH:
-
Heat-treated L. acidophilus
- LRH:
-
Heat-treated L. rhamnosus
- LARH:
-
Heat-treated L. acidophilus + L. rhamnosus
- LAU:
-
Ultrasound-treated L. acidophilus
- LRU:
-
Ultrasound-treated L. rhamnosus
- LARU:
-
Ultrasound-treated L. acidophilus + L. rhamnosus
- LAVU:
-
Viable + ultrasound-treated L. acidophilus
- LRVU:
-
Viable + ultrasound-treated L. rhamnosus
- LARVU:
-
Viable + ultrasound-treated L. acidophilus + L. rhamnosus
- LAB:
-
Lactic acid bacteria
- HepG2:
-
Human-derived hepatoma cell line
- MN:
-
Micronucleus
- HPLC:
-
High-performance liquid chromatography
- PSOM:
-
Pseudo-second-order model
- PFOM:
-
Pseudo-first-order model
- IDM:
-
Weber and Morris intraparticle diffusion model
- EM:
-
Elovich model
References
Abedi, E., & Hashemi, S. M. B. (2020). Lactic acid production–producing microorganisms and substrates sources-state of art. Heliyon, 6(10), e04974.
Abrunhosa, L., Paterson, R. R. M., & Venâncio, A. (2010). Biodegradation of ochratoxin A for food and feed decontamination. Toxins, 2(5), 1078–1099.
Armando, M. R., Pizzolitto, R. P., Dogi, C. A., Cristofolini, A., Merkis, C., Poloni, V., et al. (2012). Adsorption of ochratoxin A and zearalenone by potential probiotic Saccharomyces cerevisiae strains and its relation with cell wall thickness. Journal of Applied Microbiology, 113(2), 256–264.
Arzeni, C., Martínez, K., Zema, P., Arias, A., Pérez, O. E., & Pilosof, A. M. R. (2012). Comparative study of high intensity ultrasound effects on food proteins functionality. Journal of Food Engineering, 108(3), 463–472.
Belkacem-Hanfi, N., Fhoula, I., Semmar, N., Guesmi, A., Perraud-Gaime, I., Ouzari, H.-I., et al. (2014). Lactic acid bacteria against post-harvest moulds and ochratoxin A isolated from stored wheat. Biological Control, 76, 52–59.
Belova, V., Gorin, D. A., Shchukin, D. G., & Möhwald, H. (2011). Controlled effect of ultrasonic cavitation on hydrophobic/hydrophilic surfaces. ACS Applied Materials & Interfaces, 3(2), 417–425.
Bolognesi, C., & Hayashi, M. (2011). Micronucleus assay in aquatic animals. Mutagenesis, 26(1), 205–213.
Bryła, M., Ksieniewicz-Woźniak, E., Stępniewska, S., Modrzewska, M., Waśkiewicz, A., Szymczyk, K., & Szafrańska, A. (2021). Transformation of ochratoxin A during bread-making processes. Food Control, 125, 107950. https://doi.org/10.1016/j.foodcont.2021.107950
Chen, D., Chen, P., Cheng, Y., Peng, P., Liu, J., Ma, Y., et al. (2019). Deoxynivalenol decontamination in raw and germinating barley treated by plasma-activated water and intense pulsed light. Food and Bioprocess Technology, 12(2), 246–254.
Chen, W.-Y., Huang, H.-M., Lin, C.-C., Lin, F.-Y., & Chan, Y.-C. (2003). Effect of temperature on hydrophobic interaction between proteins and hydrophobic adsorbents: Studies by isothermal titration calorimetry and the van’t Hoff equation. Langmuir, 19(22), 9395–9403.
Del Prete, V., Rodriguez, H., Carrascosa, A. V., & de las RIVAS, B., Garcia-Moruno, E., & Munoz, R. (2007). In vitro removal of ochratoxin A by wine lactic acid bacteria. Journal of Food Protection, 70(9), 2155–2160.
Duarte, S. C., Pena, A., & Lino, C. M. (2010). A review on ochratoxin A occurrence and effects of processing of cereal and cereal derived food products. Food Microbiology, 27(2), 187–198.
Ehrlich, V., Darroudi, F., Uhl, M., Steinkellner, H., Gann, M., Majer, B. J., et al. (2002). Genotoxic effects of ochratoxin A in human-derived hepatoma (HepG2) cells. Food and Chemical Toxicology, 40(8), 1085–1090.
Feizollahi, E., & Roopesh, M. S. (2021). Degradation of zearalenone by atmospheric cold plasma: Effect of selected process and product factors. Food and Bioprocess Technology, 1–13.
Fuchs, S., Sontag, G., Stidl, R., Ehrlich, V., Kundi, M., & Knasmüller, S. (2008). Detoxification of patulin and ochratoxin A, two abundant mycotoxins, by lactic acid bacteria. Food and Chemical Toxicology, 46(4), 1398–1407.
Ghofrani Tabari, D., Kermanshahi, H., Golian, A., & Majidzadeh Heravi, R. (2018). In vitro binding potentials of bentonite, yeast cell wall and lactic acid bacteria for aflatoxin B1 and ochratoxin A. Iranian Journal of Toxicology, 12(2), 7–13.
Hashemi, S. M. B., & Amiri, M. J. (2020). A comparative adsorption study of aflatoxin B1 and aflatoxin G1 in almond butter fermented by Lactobacillus fermentum and Lactobacillus delbrueckii subsp. lactis. LWT, 109500.
Hashemi, S. M. B., Shahidi, F., Mortazavi, S. A., Milani, E., & Eshaghi, Z. (2014). Potentially probiotic Lactobacillus strains from traditional Kurdish cheese. Probiotics and Antimicrobial Proteins, 6(1), 22–31.
Hathout, A. S., & Aly, S. E. (2014). Biological detoxification of mycotoxins: A review. Annals of Microbiology, 64(3), 905–919.
Khan, S. A., Zhang, M., Liu, L., Dong, L., Ma, Y., & Wei, Z., et al. (2020). Co-culture submerged fermentation by lactobacillus and yeast more effectively improved the profiles and bioaccessibility of phenolics in extruded brown rice than single-culture fermentation. Food chemistry, 326, 126985.
Khaneghah, A. M., Fakhri, Y., & Sant’Ana, A. S. (2018). Impact of unit operations during processing of cereal-based products on the levels of deoxynivalenol, total aflatoxin, ochratoxin A, and zearalenone: A systematic review and meta-analysis. Food Chemistry, 268, 611–624.
Kumar, P., Mahato, D. K., Sharma, B., Borah, R., Haque, S., & Mahmud, M. M. C., et al. (2020). Ochratoxins in food and feed: Occurrence and its impact on human health and management strategies. Toxicon, 187, 151–162. https://doi.org/10.1016/j.toxicon.2020.08.031
Mateo, E. M., Medina, Á., Mateo, F., Valle-Algarra, F. M., Pardo, I., & Jiménez, M. (2010). Ochratoxin A removal in synthetic media by living and heat-inactivated cells of Oenococcus oeni isolated from wines. Food Control, 21(1), 23–28.
Niderkorn, V., Morgavi, D. P., Aboab, B., Lemaire, M., & Boudra, H. (2009). Cell wall component and mycotoxin moieties involved in the binding of fumonisin B1 and B2 by lactic acid bacteria. Journal of Applied Microbiology, 106(3), 977–985.
Ojha, K. S., Mason, T. J., O’Donnell, C. P., Kerry, J. P., & Tiwari, B. K. (2017). Ultrasound technology for food fermentation applications. Ultrasonics Sonochemistry, 34, 410–417.
Paíga, P., Morais, S., Oliva-Teles, T., Correia, M., Delerue-Matos, C., Sousa, A. M. M., et al. (2013). Determination of ochratoxin A in bread: Evaluation of microwave-assisted extraction using an orthogonal composite design coupled with response surface methodology. Food and Bioprocess Technology, 6(9), 2466–2477.
Pakfetrat, S., Amiri, S., Radi, M., Abedi, E., & Torri, L. (2019). Reduction of phytic acid, aflatoxins and other mycotoxins in wheat during germination. Journal of the Science of Food and Agriculture, 99(10), 4695–4701.
Pawlowska, A. M., Zannini, E., Coffey, A., & Arendt, E. K. (2012). “Green preservatives”: Combating fungi in the food and feed industry by applying antifungal lactic acid bacteria. In Advances in food and nutrition research, 66, 217–238. Elsevier.
Piotrowska, M. (2014). The adsorption of ochratoxin A by Lactobacillus species. Toxins, 6(9), 2826–2839.
Piotrowska, M., & Zakowska, Z. (2005). The elimination of ochratoxin A by lactic acid bacteria strains. Polish Journal of Microbiology, 54(4), 279–286.
Rasch, C., Kumke, M., & Löhmannsröben, H.-G. (2010). Sensing of mycotoxin producing fungi in the processing of grains. Food and Bioprocess Technology, 3(6), 908–916.
Sheikh-Zeinoddin, M., & Khalesi, M. (2018). Biological detoxification of ochratoxin A in plants and plant products. Toxin Reviews.
Shi, H., Ileleji, K., Stroshine, R. L., Keener, K., & Jensen, J. L. (2017). Reduction of aflatoxin in corn by high voltage atmospheric cold plasma. Food and Bioprocess Technology, 10(6), 1042–1052.
Turbic, A., Ahokas, J. T., & Haskard, C. A. (2002). Selective in vitro binding of dietary mutagens, individually or in combination, by lactic acid bacteria. Food Additives & Contaminants, 19(2), 144–152.
Vidal, A., Marín, S., Morales, H., Ramos, A. J., & Sanchis, V. (2014). The fate of deoxynivalenol and ochratoxin A during the breadmaking process, effects of sourdough use and bran content. Food and Chemical Toxicology, 68, 53–60.
Zhu, F. (2015). Impact of ultrasound on structure, physicochemical properties, modifications, and applications of starch. Trends in Food Science & Technology, 43(1), 1–17. https://doi.org/10.1016/j.tifs.2014.12.008
Author information
Authors and Affiliations
Contributions
EA wrote the manuscript conceived and designed the research and analyzed the data. MM and SMBH conducted experiments. All the authors read and approved the manuscript.
Corresponding authors
Ethics declarations
Ethical Approval
This article does not contain any studies with human participants or animals performed by any of the authors.
Conflict of Interest
The authors declare no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Abedi, E., Mousavifard, M. & Hashemi, S.M.B. Ultrasound-Assisted Detoxification of Ochratoxin A: Comparative Study of Cell Wall Structure, Hydrophobicity, and Toxin Binding Capacity of Single and Co-culture Lactic Acid Bacteria. Food Bioprocess Technol 15, 539–560 (2022). https://doi.org/10.1007/s11947-022-02767-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11947-022-02767-7