Inhibition of Clostridium botulinum and its toxins by probiotic bacteria and their metabolites: An update review

Main Article Content

Adel Mirza Alizadeh
Fataneh Hashempour-Baltork
Mahmood Alizadeh-Sani
Mohammad Maleki
Maryam Azizi-Lalabadi
Kianoush Khosravi-Darani

Keywords

bacteriocins, decontamination, prevention, probiotic bacteria

Abstract

Clostridium (C.) botulinum is the causative agent of foodborne poisoning such as botulism, which includes high mortality rates in animals and humans. Probiotic bacteria play critically functional roles in food matrices, as well as agricultural, clinical and nutritional fields. In this review, potentials of various probiotic bacteria and their metabolites to prevent C. botulinum toxicity are reviewed. For this purpose, an introduction about C. botulinum and its mechanisms of action is provided. After a short introduction of probiotic bacteria and their beneficial health effects on humans, the bacterial mechanisms of their action are reviewed. Then bacteriocin production by probiotic bacteria is described. After description of C. botulinum and its neurotoxins, effects of probiotic bacteria on C. botulinum are reviewed with a special focus on effects of the bacterial bacteriocins on this pathogen. Furthermore, physicochemical factors, which show great effects on potential of nisin to prevent growth and toxin production of the bacteria, are introduced. This study has shown that probiotic bacteria and their bacteriocins can be effective on growth, toxin formation and toxicity of C. botulinum. In conclusion, probiotic use in food safety studies can be effective in preventing or treating toxicity of C. botulinum.

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References

Alahakoon, A.U., Jayasena, D.D., Ramachandra, S. and Jo, C., 2015. Alternatives to nitrite in processed meat: up to date. Trends in Food Science & Technology 45: 37–49. 10.1016/j.tifs.2015.05.008

Bäckhed, F., Fraser, C.M., Ringel, Y., Sanders, M.E., Sartor, R.B., Sherman, P.M., et al., 2012. Defining a healthy human gut microbiome: current concepts, future directions, and clinical applications. Cell Host & Microbe 12: 611–622. 10.1016/j.chom.2012.10.012

Batra, V., Ghosh, M. and Ganguli, A., 2019. A simple fermentative process for ensuring safety and nutrition of legume and legume wheat based sourdoughs. Quality Assurance and Safety of Crops & Foods 11: 639–645. 10.3920/QAS2018.1421

Belkaid, Y. and Hand, T.W., 2014. Role of the microbiota in immunity and inflammation. Cell 157(1), 121–141. 10.1016/j.cell.2014.03.011

Bhakta, J., Ohnishi, K., Munekage, Y., Iwasaki, K. and Wei, M., 2012. Characterization of lactic acid bacteria-based probiotics as potential heavy metal sorbents. Journal of Applied Microbiology 112: 1193–1206. 10.1111/j.1365-2672.2012.05284.x

Bintsis, T., 2018. Lactic acid bacteria: their applications in foods. Journal of Bacteriology & Mycology 6: 89–94. 10.15406/jbmoa.2018.06.00182

Bonsaglia, E., Silva, N., Júnior, A.F., Júnior, J.A., Tsunemi, M. and Rall, V., 2014. Production of biofilm by Listeria monocytogenes in different materials and temperatures. Food Control 35: 386–391. 10.1016/j.foodcont.2013.07.023

Breukink, E. and de Kruijff, B., 2006. Lipid II as a target for antibiotics. Nature Reviews Drug Discovery 5: 321. 10.1038/nrd2004

Butel, M.-J., 2014. Probiotics, gut microbiota and health. Médecine et maladies infectieuses 44: 1–8. 10.1016/j.medmal.2013.10.002

Chapman, C., Gibson, G.R. and Rowland, I., 2011. Health benefits of probiotics: are mixtures more effective than single strains? European Journal of Nutrition 50: 1–17. 10.1007/s00394-010-0166-z

Chikindas, M.L., Weeks, R., Drider, D., Chistyakov, V.A. and Dicks, L.M., 2018. Functions and emerging applications of bacteriocins. Current Opinion in Biotechnology 49: 23–28. 10.1016/j.copbio.2017.07.011

Chugh, B. and Kamal-Eldin, A., 2020. Bioactive compounds produced by probiotics in food products. Current Opinion in Food Science 32: 76–82. 10.3746/jfn.2007.12.4.259

Chung, Y.K. and Yousef, A.E., 2007. Effect of nisin against Clostridium botulinum during spore-to-cell transformation. Preventive Nutrition and Food Science 12(4): 259–266.

Cizeikiene, D., Juodeikiene, G., Paskevicius, A. and Bartkiene, E., 2013. Antimicrobial activity of lactic acid bacteria against pathogenic and spoilage microorganism isolated from food and their control in wheat bread. Food Control 31: 539–545. 10.1016/j.foodcont.2012.12.004

Corcoran, B., Ross, R., Fitzgerald, G., Dockery, P. and Stanton, C., 2006. Enhanced survival of GroESL-overproducing Lactobacillus paracasei NFBC 338 under stressful conditions induced by drying. Applied and Environmental Microbiology 72: 5104–5107. 10.1128/AEM.02626-05

Dalié, D., Deschamps, A. and Richard-Forget, F., 2010. Lactic acid bacteria–potential for control of mould growth and mycotoxins: a review. Food Control 21: 370–380. 10.1016/j.foodcont.2009.07.011

Dang, Y., Reinhardt, J.D., Zhou, X. and Zhang, G., 2014. The effect of probiotics supplementation on Helicobacter pylori eradication rates and side effects during eradication therapy: a meta-analysis. PLoS One 9: e111030. 10.1371/journal.pone.0111030

Dethlefsen, L., Eckburg, P.B., Bik, E.M. and Relman, D.A., 2006. Assembly of the human intestinal microbiota. Trends in Ecology & Evolution 21: 517–523. 10.1016/j.tree.2006.06.013

Dobson, A., Cotter, P.D., Ross, R.P. and Hill, C., 2012. Bacteriocin production: a probiotic trait? Applied and Environmental Microbiology 78: 1–6. 10.1128/AEM.05576-11

Donaldson, G.P., Lee, S.M. and Mazmanian, S.K., 2016. Gut biogeography of the bacterial microbiota. Nature Reviews Microbiology 14: 20. 10.1038/nrmicro3552

Durlu-Özkaya, F. and Özkaya, M.T., 2011. Oleuropein using as an additive for feed and products used for humans. Journal of Food Processing and Technology 2(3): 113. 10.4172/2157-7110.1000113

Eslami, P., Forootan, K., Davarpanah, L. and Vahabzadeh, F., 2020. Incorporation of Lactobacillus casei into the inner phase of the water-in-oil-in-water (W1/O/W2) emulsion prepared with β-cyclodextrin and bacterial survival in a model gastric environment. Applied Food Biotechnology 7: 171–182.

Fernández-Pérez, R., Sáenz, Y., Rojo-Bezares, B., Zarazaga, M., Rodríguez, J.M., Torres, C., et al., 2018. Production and antimicrobial activity of nisin under enological conditions. Frontiers in Microbiology 9: 1918. 10.3389/fmicb.2018.01918

Fijan, S., 2014. Microorganisms with claimed probiotic properties: an overview of recent literature. International Journal of Environmental Research and Public Health 11: 4745–4767. 10.3390/ijerph110504745

Fooda, 2018. Food poisoning with Clostridium botulinum. http://fooda.ir.

Gálvez, A., Abriouel, H., Benomar, N. and Lucas, R., 2010. Microbial antagonists to food-borne pathogens and biocontrol. Current Opinion in Biotechnology 21: 142–148. 10.1016/j.copbio.2010.01.005

Gao, Y.L. and Ju, X.R., 2008. Exploiting the combined effects of high pressure and moderate heat with nisin on inactivation of Clostridium botulinum spores. Journal of Microbiological Methods 72(1): 20–28. 10.1016/j.mimet.2007.11.003

Gezginc, Y. and Kara, Ü., 2019. The effect of exopolysaccharide producing Lactobacillus plantarum strain addition on sourdough and wheat bread quality. Quality Assurance and Safety of Crops & Foods 11: 95–106. 10.3920/QAS2018.1361

Gharsallaoui, A., Oulahal, N., Joly, C. and Degraeve, P., 2016. Nisin as a food preservative: part 1: physicochemical properties, antimicrobial activity, and main uses. Critical Reviews in Food Science and Nutrition 56(8): 1262–1274. 10.1080/10408398.2013.763765

Gioacchini, G., Lombardo, F., Merrifield, D., Silvi, S., Cresci, A., Avella, M. et al., 2011. Effects of probiotics on Zebrafish reproduction. Journal of Aquaculture Research and Development S1-S6. 10.4172/2155-9546.S1-002

Gonzalez-Escalona, N., Thirunavukkarasu, N., Singh, A., Toro, M., Brown, E.W., Zink, D., Rummel, A. et al., 2014. Draft genome sequence of bivalent Clostridium botulinum strain IBCA10-7060, encoding botulinum neurotoxin B and a new FA mosaic type. Genome Announcements 2: e01275–01214. 10.1128/genomeA.01275-14

Guo, P., Zhang, K., Ma, X. and He, P., 2020. Clostridium species as probiotics: potentials and challenges. Journal of Animal Science and Biotechnology 11(1): 1–10. 10.1186/s40104-019-0402-1

Han, J., Chen, D., Li, S., Li, X., Zhou, W.-W., Zhang, B., et al., 2015. Antibiotic susceptibility of potentially probiotic Lactobacillus strains. Italian Journal of Food Science 27: 282–289.

Hashempour-Baltork, F., Hosseini, H., Shojaee-Aliabadi, S., Torbati, M., Alizadeh, A.M. and Alizadeh, M., 2019. Drug resistance and the prevention strategies in food Borne bacteria: an update review. Advanced Pharmaceutical Bulletin 9: 335. 10.15171/apb.2019.041

Hayta, M. and Ertop, M.H., 2019. Physicochemical, textural and microbiological properties of optimised wheat bread formulations as affected by differently fermented sourdough. Quality Assurance and Safet y of Crops & Foods 11: 283–293. 10.3920/QAS2018.1387

Hemarajata, P. and Versalovic, J., 2013. Effects of probiotics on gut microbiota: mechanisms of intestinal immunomodulation and neuromodulation. Therapeutic Advances in Gastroenterology 6(1), 39–51. 10.1177/1756283X12459294

Jay, J.M., Loessner, M.J. and Golden, D.A., 2005. Modern food microbiology. Springer US, New York, 790 pp.

Kasalica, A., Vuković, V., Vranješ, A., and Memiši, N., 2011. Listeria monocytogenes in milk and dairy products. Biotechnology in Animal Husbandry 27 (3). Doi:10.2298/BAH1103067K

Kechagia, M., Basoulis, D., Konstantopoulou, S., Dimitriadi, D., Gyftopoulou, K., Skarmoutsou, N., et al., 2013. Health benefits of probiotics: a review. ISRN Nutrition 2013. 10.5402/2013/481651

Khaneghah, A.M., Abhari, K., Eş, I., Soares, M.B., Oliveira, R.B., Hosseini, H., et al., 2020. Interactions between probiotics and pathogenic microorganisms in hosts and foods: a review. Trends in Food Science & Technology 95: 205–218. 10.1016/j.tifs.2019.11.022

Khezri, S., Dehghan, P., Mahmoudi, R. and Jafarlou, M., 2016. Fig juice fermented with lactic acid bacteria as a nutraceutical product. Pharmaceutical Sciences 22: 260–266. 10.15171/PS.2016.40

Khezri, S., Mahmoudi, R. and Dehghan, P., 2018. Fig juice fortified with inulin and Lactobacillus Delbrueckii: a promising functional food. Applied Food Biotechnology 5: 97–106.

Lam, T.I., Tam, C.C., Stanker, L.H. and Cheng, L.W., 2016. Probiotic microorganisms inhibit epithelial cell internalization of botulinum neurotoxin serotype A. Toxins 8: 377. 10.3390/toxins8120377

Marhamatizadeh, M.H. and Goosheh, S.R., 2016. The combined effect of Thymus vulgaris extract and probiotic bacteria (Lactobacillus acidophyllus and Bifidubacterium bifidum) on aflatoxin m1 concentration in kefir beverage. Italian Journal of Food Science 28: 517.

Markowiak, P. and Śliżewska, K., 2017. Effects of probiotics, prebiotics, and synbiotics on human health. Nutrients 9(9): 1021. 10.3390/nu9091021

Mills, S., Stanton, C., Fitzgerald, G.F. and Ross, R., 2011. Enhancing the stress responses of probiotics for a lifestyle from gut to product and back again, Microbial cell factories. BioMed Central S19. 10.1186/1475-2859-10-S1-S19

Moayyedi, P., Ford, A.C., Talley, N.J., Cremonini, F., Foxx-Orenstein, A.E., et al., 2010. The efficacy of probiotics in the treatment of irritable bowel syndrome: a systematic review. Gut 59: 325–332. 10.1136/gut.2008.167270

Nadjafi, M. and Hamzeh, P.S., 2017. Botulinum neurotoxins, a real bioterrorism threat: a classic review. Nurse and Physician Within War 13.

Nishant, T., Sathish, K., Arun, K., Hima, B. and Raviteja, Y., 2011. Bacteriocin producing probiotic lactic acid bacteria. Journal of Microbial and Biochemical Technology 3: 5.

Noordiana, N., Fatimah, A. and Mun, A., 2013. Antibacterial agents produced by lactic acid bacteria isolated from Threadfin Salmon and Grass Shrimp. International Food Research Journal 20(1): 117–124.

Oelschlaeger, T.A., 2010. Mechanisms of probiotic actions—a review. International Journal of Medical Microbiology 300: 57–62. 10.1016/j.ijmm.2009.08.005

Plaza-Diaz, J., Ruiz-Ojeda, F.J., Gil-Campos, M. and Gil, A., 2019. Mechanisms of action of probiotics. Advances in Nutrition 10: S49–S66. 10.1093/advances/nmy063

Postollec, F., Falentin, H., Pavan, S., Combrisson, J. and Sohier, D., 2011. Recent advances in quantitative PCR (qPCR) applications in food microbiology. Food Microbiology 28: 848–861. 10.1016/j.fm.2011.02.008

Raybaudi-Massilia, R.M., Mosqueda-Melgar, J., Soliva-Fortuny, R. and Martín-Belloso, O., 2009. Control of pathogenic and spoilage microorganisms in fresh-cut fruits and fruit juices by traditional and alternative natural antimicrobials. Comprehensive Reviews in Food Science and Food Safety 8: 157–180. 10.1111/j.1541-4337.2009.00076.x

Reis, J., Paula, A., Casarotti, S. and Penna, A., 2012. Lactic acid bacteria antimicrobial compounds: characteristics and applications. Food Engineering Reviews 4: 124–140. 10.1007/s12393-012-9051-2

Rossetto, O., Pirazzini, M. and Montecucco, C., 2014. Botulinum neurotoxins: genetic, structural and mechanistic insights. Nature Reviews Microbiology 12: 535. 10.1038/nrmicro3295

Rummel, A., 2015. The long journey of botulinum neurotoxins into the synapse. Toxicon 107: 9–24. 10.1016/j.toxicon.2015.09.009

Sadrizadeh, N., Khezri, S., Dehghan, P. and Mahmoudi, R., 2018. Antibacterial effect of Teucrium polium essential oil and Lactobacillus casei probiotic on Escherichia coli O157: H7 in Kishk. Applied Food Biotechnology 5: 131–140.

Salminen, S., Nybom, S., Meriluoto, J., Collado, M.C., Vesterlund, S. and El-Nezami, H., 2010. Interaction of probiotics and pathogens—benefits to human health? Current Opinion in Biotechnology 21: 157–167. 10.1016/j.copbio.2010.03.016

Sánchez, B., Delgado, S., Blanco-Míguez, A., Lourenço, A., Gueimonde, M. and Margolles, A., 2017. Probiotics, gut microbiota, and their influence on host health and disease. Molecular Nutrition & Food Research 61: 1600240. 10.1002/mnfr.201600240

Savage, D.C., 1977. Microbial ecology of the gastrointestinal tract. Annual Reviews in Microbiology 31: 107–133. 10.1146/annurev.mi.31.100177.000543

Shetty, P.H. and Jespersen, L., 2006. Saccharomyces cerevisiae and lactic acid bacteria as potential mycotoxin decontaminating agents. Trends in Food Science and Technology 17: 48–55. 10.1016/j.tifs.2005.10.004

Soccol, C.R., de Souza Vandenberghe, L.P., Spier, M.R., Medeiros, A.P., Yamaguishi, C.T., De Dea Lindner, J., et al., 2010. The potential of probiotics: a review. Food Technology and Biotechnology 48: 413–434.

Tighe, A.P. and Schiavo, G., 2013. Botulinum neurotoxins: mechanism of action. Toxicon 67: 87–93. 10.1016/j.toxicon.2012.11.011

Verschuere, L., Rombaut, G., Sorgeloos, P. and Verstraete, W., 2000. Probiotic bacteria as biological control agents in aquaculture. Microbiology and Molecular Biology Reviews 64: 655–671. 10.1128/MMBR.64.4.655-671.2000

Zendeboodi, F., Khorshidian, N., Mortazavian, A.M. and da Cruz, A.G., 2020. Probiotic: conceptualization from a new approach. Current Opinion in Food Science. 32: 103–123. 10.1016/j.cofs.2020.03.009

Zhou, H., Fang, J., Tian, Y. and Lu, X.Y., 2014. Mechanisms of nisin resistance in Gram-positive bacteria. Annals of Microbiology 64: 413–420. 10.1007/s13213-013-0679-9

Zhou, L., van Heel, A.J. and Kuipers, O.P., 2015. The length of a lantibiotic hinge region has profound influence on antimicrobial activity and host specificity. Frontiers in Microbiology 6: 11. 10.3389/fmicb.2015.00011

Zoghi, A., Khosravi-Darani, K. and Sohrabvandi, S., 2014. Surface binding of toxins and heavy metals by probiotics. Mini Reviews in Medicinal Chemistry 14: 84–98. 10.2174/1389557513666131211105554