Abstract
The present study aimed to evaluate the effects of new Lactobacillus plantarum strain isolated from dairy products as well as chitosan nanoparticles on reducing aflatoxin B1 (AFB1) toxicity In vitro. After collection and preparation of yogurt, cheese, milk, and whey products, lactic acid bacteria (LABs) were isolated and identified using biochemical and molecular methods. pH, bile, and salt tolerance tests were used to measure probiotic activity. Then, the antimicrobial activity of LABs against gastrointestinal pathogens was studied. The strain isolated from cheese (C1) was selected as the appropriate strain and antibiotic susceptibility test was performed for this strain. Then, the effect of C1 isolate and chitosan nanoparticles on reducing aflatoxin B1 (AFB1) in the medium was studied by measuring AFB1 using the enzyme-linked immunosorbent assay (ELISA) and high-performance liquid chromatography (HPLC). The results of biochemical evaluations indicated the separation of different strains of L. plantarum. Antimicrobial activity test showed extensive antimicrobial activity of C1 isolate. The results showed that this strain has good probiotic activities. This strain was shown to be resistant to erythromycin, fusidic acid, gentamicin, kanamycin, nalidixic acid, neomycin, ofloxacin, and vancomycin antibiotics. C1 strain together with chitosan nanoparticles was able to reduce AFB1 in the medium and, when both were used simultaneously, a synergistic effect was seen in reducing AFB1 from the medium. Based on the findings, it can be concluded that the new C1 L. plantarum strains together with chitosan nanoparticles had synergistic effects on reducing AFB1 toxin in food products.
Similar content being viewed by others
Data availability
All data generated or analyzed during this study are included in this published article [and its supplementary information files]. Raw sequence data on 16 s RNA gene had been submitted to the NCBI Sequence Read Archive (SRA) with the accession number SRX11028965. (https://www.ncbi.nlm.nih.gov/sra/SRX11028965).
References
Ahmad A, Yap WB, Kofli NT, Ghazali AR (2018) Probiotic potentials of Lactobacillus plantarum isolated from fermented durian (Tempoyak), a Malaysian traditional condiment. Food Sci Nutr 6:1370–1377. https://doi.org/10.1002/fsn3.672
Alishahi M, Tulaby DZ, Mohammadian T, Mesbah M (2018) Effects of two probiotics, Lactobacillus plantarum and Lactobacillus bulgaricus on growth performance and intestinal lactic acid bacteria of cyprinus carpio. Iran J Vet Med 12:207–218. https://doi.org/10.22059/ijvm.2018.235444.1004816
Alshannaq AF, Gibbons JG, Lee M-K, Han K-H, Hong S-B, Yu J-H (2018) Controlling aflatoxin contamination and propagation of Aspergillus flavus by a soy-fermenting Aspergillus oryzae strain. Sci Rep 8:1–14. https://doi.org/10.1038/s41598-018-35246-1
Azat R et al (2016) Probiotic properties of lactic acid bacteria isolated from traditionally fermented Xinjiang cheese. J Zhejiang Univ Sci B 17:597–609. https://doi.org/10.1631/jzus.B1500250
Chauhan PB, Daru D. (2016) Isolation and characterization of Lactobacillus isolated from milk, curd, and fecal sample and assigning their probiotic values. Int J Pharma Bio Sci, Issn:0975-6299
Chen YS, Yanagida F, Shinohara T (2005) Isolation and identification of lactic acid bacteria from soil using an enrichment procedure. Lett Appl Microbiol 40:195–200. https://doi.org/10.1111/j.1472-765X.2005.01653.x
Chlebicz A, Śliżewska K (2020) In vitro detoxification of aflatoxin B 1, deoxynivalenol, fumonisins, T-2 toxin and zearalenone by probiotic bacteria from genus Lactobacillus and Saccharomyces cerevisiae yeast. Probiotics Antimicro Prot 12:289–301. https://doi.org/10.1007/s12602-018-9512-x
Fakruddin M, Chowdhury A, Hossain MN, Ahmed MM (2015) Characterization of aflatoxin producing Aspergillus flavus from food and feed samples. Springerplus 4:1–6. https://doi.org/10.1186/s40064-015-0947-1
Fazeli MR et al (2009) Aflatoxin B1 binding capacity of autochthonous strains of lactic acid bacteria. J Food Protect 72:189–192. https://doi.org/10.4315/0362-028X-72.1.189
Fouad AM, Ruan D, El-Senousey HK, Chen W, Jiang S, Zheng C (2019) Harmful effects and control strategies of aflatoxin b1 produced by Aspergillus flavus and Aspergillus parasiticus strains on poultry. Toxins 11:176. https://doi.org/10.3390/toxins11030176
Gallant-Behm CL et al (2005) Comparison of in vitro disc diffusion and time kill-kinetic assays for the evaluation of antimicrobial wound dressing efficacy. Wound Repair Regen 13:412–421. https://doi.org/10.1111/j.1067-1927.2005.130409.x
Gizachew D, Chang C-H, Szonyi B, De La Torre S, W-tE T (2019) Aflatoxin B1 (AFB1) production by Aspergillus flavus and Aspergillus parasiticus on ground Nyjer seeds: the effect of water activity and temperature. Int J Food Microbiol 296:8–13. https://doi.org/10.1016/j.ijfoodmicro.2019.02.017
Gómez JV, Tarazona A, Mateo-Castro R, Gimeno-Adelantado JV, Jiménez M, Mateo EM (2018) Selected plant essential oils and their main active components, a promising approach to inhibit aflatoxigenic fungi and aflatoxin production in food. Food Addit Contam: Part A 35:1581–1595. https://doi.org/10.1080/19440049.2017.1419287
Gotcheva V, Hristozova E, Hristozova T, Guo M, Roshkova Z, Angelov A (2002) Assessment of potential probiotic properties of lactic acid bacteria and yeast strains. Food Biotechnol 16:211–225. https://doi.org/10.1081/FBT-120016668
Gratz S, Mykkänen H, El-Nezami H (2005) Aflatoxin B1 binding by a mixture of Lactobacillus and Propionibacterium: in vitro versus ex vivo. J Food Protect 68:2470–2474. https://doi.org/10.4315/0362-028X-68.11.2470
Hamid AS, Tesfamariam IG, Zhang Y, Zhang ZG (2013) Aflatoxin B1-induced hepatocellular carcinoma in developing countries: Geographical distribution, mechanism of action and prevention. Oncol Lett 5:1087–1092. https://doi.org/10.3892/ol.2013.1169
Hassan MU et al (2020) Characterisation of bacteriocins produced by Lactobacillus spp. isolated from the traditional Pakistani yoghurt and their antimicrobial activity against common foodborne pathogens. Biomed Res Int. https://doi.org/10.1155/2020/8281623
Hernandez-Mendoza A, Guzman-de-Peña D, Garcia HS (2009) Key role of teichoic acids on aflatoxin B binding by probiotic bacteria. J Appl Microbiol 107:395–403. https://doi.org/10.1111/j.1365-2672.2009.04217.x
Hoque M, Akter F, Hossain K, Rahman M, Billah M, Islam K (2010) Isolation, identification and analysis of probiotic properties of Lactobacillus spp. from selective regional yoghurts. World J Dairy Food Sci 5:39–46
Ibitoye OA, Olaniyi OO, Ogidi CO, Akinyele BJ. (2020) Lactic acid bacteria bio-detoxified aflatoxins contaminated cereals, ameliorate toxicological effects and improve haemato-histological parameters in albino rats. Toxin Rev 1-12. https://doi.org/10.1080/15569543.2020.1817088
Intanoo M et al (2018) Isolation and screening of aflatoxin-detoxifying yeast and bacteria from ruminal fluids to reduce aflatoxin B1 contamination in dairy cattle feed. J Appl Microbiol 125:1603–1613. https://doi.org/10.1111/jam.14060
Istiqomah L, Damayanti E, Julendra H, Suryani AE, Sakti AA, Anggraeni AS. (2017) Effect of methionine and lactic acid bacteria as aflatoxin binder on broiler performance. In: AIP Conference Proceedings. AIP Publishing LLC, p 020017. https://doi.org/10.1063/1.4985408
Kumara SS, Bashisht A, Venkateswaran G, Hariprasad P, Gayathri D (2019) Characterization of novel Lactobacillus fermentum from curd samples of indigenous cows from Malnad region, Karnataka, for their aflatoxin B 1 binding and probiotic properties. Probiotics Antimicro Prot 11:1100–1109. https://doi.org/10.1007/s12602-018-9479-7
Kumara SS, Gayathri D, Hariprasad P, Venkateswaran G, Swamy CT (2020) In vivo AFB1 detoxification by Lactobacillus fermentum LC5/a with chlorophyll and immunopotentiating activity in albino mice. Toxicon 187:214–222. https://doi.org/10.1016/j.toxicon.2020.09.004
Leroy F, De Vuyst L (2004) Lactic acid bacteria as functional starter cultures for the food fermentation industry. Trends Food Sci Technol 15:67–78. https://doi.org/10.1016/j.tifs.2003.09.004
Lee K, Paek K, Lee H, Park JH, Lee Y (2007) Antiobesity effect of trans‐10, cis‐12‐conjugated linoleic acid‐producing Lactobacillus plantarum PL62 on diet‐induced obese mice. Journal of Applied Microbiology 103:1140–1146. https://doi.org/10.1111/j.1365-2672.2007.03336.x
Ma Z, Garrido-Maestu A, Jeong KC (2017) Application, mode of action, and in vivo activity of chitosan and its micro-and nanoparticles as antimicrobial agents: a review. Carbohydr Polym 176:257–265. https://doi.org/10.1016/j.carbpol.2017.08.082
Man Y, Liang G, Li A, Pan L (2017) Recent advances in mycotoxin determination for food monitoring via microchip. Toxins 9:324. https://doi.org/10.3390/toxins9100324
Maragkoudakis PA, Chingwaru W, Gradisnik L, Tsakalidou E, Cencic A (2010) Lactic acid bacteria efficiently protect human and animal intestinal epithelial and immune cells from enteric virus infection. Int J Food Microbiol 141:S91–S97. https://doi.org/10.1016/j.ijfoodmicro.2009.12.024
Mekawey AAI (2018) Effects of Chitosan nanoparticles as antimicrobial activity and on mycotoxin production. Acad J Agric Res 6(5):101–106
Mohammadi F, Eshaghi M, Razavi S, Sarokhalil DD, Talebi M, Pourshafie MR (2018) Characterization of bacteriocin production in Lactobacillus spp. isolated from mother’s milk. Microb Pathog 118:242–246. https://doi.org/10.1016/j.micpath.2018.03.020
Mohammed A et al (2018) Integrated management of Aspergillus species and aflatoxin production in groundnut (Arachis hypogaea L.) through application of farm yard manure and seed treatments with fungicides and Trichoderma species. Afr J Plant Sci 12:196–207. https://doi.org/10.5897/AJPS2018.1688
Ostry V, Malir F, Toman J, Grosse Y (2017) Mycotoxins as human carcinogens-the IARC Monographs classification. Mycotoxin Res 33:65–73. https://doi.org/10.1007/s12550-016-0265-7
Perinelli DR et al (2018) Chitosan-based nanosystems and their exploited antimicrobial activity. Eur J Pharm Sci 117:8–20. https://doi.org/10.1016/j.ejps.2018.01.046
Prabhurajeshwar C, Chandrakanth K (2019) Evaluation of antimicrobial properties and their substances against pathogenic bacteria in-vitro by probiotic Lactobacilli strains isolated from commercial yoghurt. Clin Nutr Exp 23:97–115. https://doi.org/10.1016/j.yclnex.2018.10.001
Rashki S et al (2020) Chitosan-based nanoparticles against bacterial infections. Carbohydr Polym. https://doi.org/10.1016/j.carbpol.2020.117108
Shobharani P, Agrawal R (2011) A potent probiotic strain from cheddar cheese. Indian J Microbiol 51:251–258. https://doi.org/10.1007/s12088-011-0072-y
Silva CC, Silva SP, Ribeiro SC (2018) Application of bacteriocins and protective cultures in dairy food preservation. Front Microbiol 9:594. https://doi.org/10.3389/fmicb.2018.00594
Strompfová V, Lauková A, Ouwehand AC (2004) Selection of enterococci for potential canine probiotic additives. Vet Microbiol 100:107–114. https://doi.org/10.1016/j.vetmic.2004.02.002
Tajik H, Sayadi M. (2020) Effects of probiotic bacteria of Lactobacillus acidophilus and Lactobacillus casei on aflatoxin B1 detoxification within a simulated gastrointestinal tract model. Toxin Rev 1-8. https://doi.org/10.1080/15569543.2020.1843180
Tambekar D, Bhutada S (2010) An evaluation of probiotic potential of Lactobacillus sp. from milk of domestic animals and commercial available probiotic preparations in prevention of enteric bacterial infections. Recent Res Sci Technol 2:82–88
Temmerman R, Huys G, Swings J (2004) Identification of lactic acid bacteria: culture-dependent and culture-independent methods. Trends Food Sci Technol 15:348–359. https://doi.org/10.1016/j.tifs.2003.12.007
Vanniyasingam J, Kapilan R, Vasantharuba S. (2019) Isolation and characterization of potential probiotic lactic acid bacteria isolated from cow milk and milk products. J Agric Sci. https://doi.org/10.4038/agrieast.v13i1.62
Wei S, Ching YC, Chuah CH (2020) Synthesis of chitosan aerogels as promising carriers for drug delivery: a review. Carbohydr Polym 231:115744. https://doi.org/10.1016/j.carbpol.2019.115744
Xu Y et al (2020) Probiotic potential and amylolytic properties of lactic acid bacteria isolated from Chinese fermented cereal foods. Food Control 111:107057. https://doi.org/10.1016/j.foodcont.2019.107057
Yang E, Chang H (2010) Purification of a new antifungal compound produced by Lactobacillus plantarum AF1 isolated from kimchi. Int J Food Microbiol 139:56–63. https://doi.org/10.1016/j.ijfoodmicro.2010.02.012
Funding
The authors did not receive support from any organization for the submitted work.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors declared no conflicts of interest.
Additional information
Communicated by Erko Stackebrandt.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Zamani, N., Fazeli, M.R., Sepahi, A.A. et al. A new probiotic Lactobacillus plantarum strain isolated from traditional dairy together with nanochitosan particles shows the synergistic effect on aflatoxin B1 detoxification. Arch Microbiol 204, 624 (2022). https://doi.org/10.1007/s00203-022-03231-y
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00203-022-03231-y