Animal Bioscience

Asian Australasian Association of Animal Production Societies (아세아태평양축산학회)
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Antimicrobial activity of fermented Maillard reaction products, novel milk-derived material, made by whey protein and Lactobacillus rhamnosus and Lactobacillus gasseri on Clostridium perfringens

  • Kim, Yujin (Department of Food and Nutrition, Sookmyung Women's University) ;
  • Kim, Sejeong (Risk Analysis Research Center, Sookmyung Women's University) ;
  • Lee, Soomin (Risk Analysis Research Center, Sookmyung Women's University) ;
  • Ha, Jimyeong (Risk Analysis Research Center, Sookmyung Women's University) ;
  • Lee, Jeeyeon (Department of Food and Nutrition, Dong-eui University) ;
  • Choi, Yukyung (Risk Analysis Research Center, Sookmyung Women's University) ;
  • Oh, Hyemin (Department of Food and Nutrition, Sookmyung Women's University) ;
  • Lee, Yewon (Department of Food and Nutrition, Sookmyung Women's University) ;
  • Oh, Nam-su (Department of Food and Biotechnology, Korea University) ;
  • Yoon, Yohan (Department of Food and Nutrition, Sookmyung Women's University) ;
  • Lee, Heeyoung (Food Standard Research Center, Korea Food Research Institute)
  • Received : 2020.05.01
  • Accepted : 2021.02.02
  • Published : 2021.09.01
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Abstract

Objective: The objective of this study was to evaluate the antimicrobial effects of fermented Maillard reaction products made by milk proteins (FMRPs) on Clostridium perfringens (C. perfringens), and to elucidate antimicrobial modes of FMRPs on the bacteria, using physiological and morphological analyses. Methods: Antimicrobial effects of FMRPs (whey protein plus galactose fermented by Lactobacillus rhamnosus [L. rhamnosus] 4B15 [Gal-4B15] or Lactobacillus gasseri 4M13 [Gal-4M13], and whey protein plus glucose fermented by L. rhamnosus 4B15 [Glc-4B15] or L. gasseri 4M13 [Glc-4M13]) on C. perfringens were tested by examining growth responses of the pathogen. Iron chelation activity analysis, propidium iodide uptake assay, and morphological analysis with field emission scanning electron microscope (FE-SEM) were conducted to elucidate the modes of antimicrobial activities of FMRPs. Results: When C. perfringens were exposed to the FMRPs, C. perfringens cell counts were decreased (p<0.05) by the all tested FMRPs; iron chelation activities by FMRPs, except for Glc-4M13. Propidium iodide uptake assay indicate that bacterial cellular damage increased in all FMRPs-treated C. perfringens, and it was observed by FE-SEM. Conclusion: These results indicate that the FMRPs can destroy C. perfringens by iron chelation and cell membrane damage. Thus, it could be used in dairy products, and controlling intestinal C. perfringens.

Keywords

Acknowledgement

This study was supported by Korea Institute of Planning and Evaluation for Technology in Food, Agriculture, Forestry and Fisheries (IPET) through High Value-added Food Technology Development Program, funded by Ministry of Agriculture, Food and Rural Affairs (MAFRA) (115006-03).

References

  1. Scallan E, Hoekstra RM, Angulo FJ, et al. Foodborne Illness Acquired in the United States-Major Pathogens. Emerg Infect Dis 2011;17:7-15. https://doi.org/10.3201/eid1701.p11101
  2. Labbe RG, Juneja VK. Clostridium perfringens gastroenteritis. In: Morris JG, Potter ME, editors. Foodborne infections and intoxications. 4th ed. Waltham, MA, USA: Academic Press; 2013. p. 99-112.
  3. Heo S, Kim MG, Kwon M, Lee HS, Kim GB. Inhibition of Clostridium perfringens using bacteriophages and bacteriocin producing strains. Food Sci Anim Resour 2018;38:88-98. https://doi.org/10.5851/kosfa.2018.38.1.88
  4. Carman RJ, Sayeed S, Li J, et al. Clostridium perfringens toxin genotypes in the feces of healthy North Americans. Anaerobe 2008;14:102-8. https://doi.org/10.1016/j.anaerobe.2008.01.003
  5. Finegold SM, Summanen PH, Downes J, Corbett K, Komoriya T. Detection of Clostridium perfringens toxin genes in the gut microbiota of autistic children. Anaerobe 2017;45:133-7. https://doi.org/10.1016/j.anaerobe.2017.02.008
  6. Tremlett H, Bauer KC, Appel-Cresswell S, Finlay BB, Waubant E. The gut microbiome in human neurological disease: a review. Ann Neurol 2017;81:369-82. https://doi.org/10.1002/ana.24901
  7. Freedman JC, Shrestha A, McClane BA. Clostridium perfringens enterotoxin: action, genetics, and translational applications. Toxins 2016;8:73. https://doi.org/10.3390/toxins8030073
  8. Kim DH, Chun SH, Oh NS, Lee JY, Lee KW. Anti-inflammatory activities of Maillard reaction products from whey protein isolate fermented by Lactobacillus gasseri 4M13 in lipopolysaccharide-stimulated RAW264.7 cells. J Dairy Sci 2019;102: 7707-16. https://doi.org/10.3168/jds.2018-15774
  9. Pyo MC, Yang SY, Chun SH, Oh NS, Lee KW. Protective effects of Maillard reaction products of whey protein concentrate against oxidative stress through an Nrf2-dependent pathway in HepG2 cells. Biol Pharm Bull 2016;39:1437-47. https://doi.org/10.1248/bpb.b16-00029
  10. Oh NS, Kwon HS, Lee HA, et al. Preventive effect of fermented Maillard reaction products from milk proteins in cardiovascular health. J Dairy Sci 2014;97:3300-13. https://doi.org/10.3168/jds.2013-7728
  11. Oh NS, Lee JY, Lee HA, et al. Chemical characteristics and enhanced hepatoprotective activities of Maillard reaction products derived from milk protein-sugar system. J Dairy Sci 2016;99:947-58. https://doi.org/10.3168/jds.2015-10009
  12. Rufian-Henares JA, Morales FJ. Functional properties of melanoidins: in vitro antioxidant, antimicrobial and antihypertensive activities. Food Res Int 2007;40:995-1002. https://doi.org/10.1016/j.foodres.2007.05.002
  13. Rufian-Henares JA, Morales FJ. Microtiter plate-based assay for screening antimicrobial activity of melanoidins against E. coli and S. aureus. Food Chem 2008;111:1069-74. https://doi.org/10.1016/j.foodchem.2008.05.027
  14. Rurian-Henares JA, Morales FJ. Antimicrobial activity of melanoidins against Escherichia coli is mediated by a membrane-damage mechanism. J Agric Food Chem 2008,56: 2357-62. https://doi.org/10.1021/jf073300+
  15. Kim S, Lee H, Lee S, Yoon Y, Choi KH. Antimicrobial action of oleanolic acid on Listeria monocytogenes, Enterococcus faecium, and Enterococcus faecalis. PloS One 2015;10:e0118800. https://doi.org/10.1371/journal.pone.0118800
  16. Kim S, Lee S, Lee H, et al. Evaluation on antimicrobial activity of psoraleae semen extract controlling the growth of gram-positive bacteria. Food Sci Anim Resour 2017;37:502-10. https://doi.org/10.5851/kosfa.2017.37.4.502
  17. Kim JS, Lee YS. Antioxidant activity of Maillard reaction products derived from aqueous glucose/glycine, diglycine, and triglycine model systems as a function of heating time. Food Chem 2009;116:227-32. https://doi.org/10.1016/j.foodchem.2009.02.038
  18. Parrow NL, Fleming RE, Minnick MF. Sequestration and scavenging of iron in infection. Infect Immun 2013;81:3503-14. https://doi.org/10.1128/IAI.00602-13
  19. Frawley ER, Fang FC. The ins and outs of bacterial iron metabolism. Mol Microbiol 2014;93:609-16. https://doi.org/10.1111/mmi.12709
  20. Crowley LC, Scott AP, Marfell BJ, Boughaba JA, Chojnowski G, Waterhouse NJ. Measuring cell death by propidium iodide uptake and flow cytometry. Cold Spring Harb Protoc 2016; 2016:pdb-prot087163. https://doi.org/10.1101/pdb.prot087163
  21. Theolier J, Fliss I, Jean J, Hammami, R. Antimicrobial peptides of dairy proteins: from fundamental to applications. Food Rev Int 2014;30:134-54. https://doi.org/10.1080/87559129.2014.896017
  22. Justice SS, Hunstad DA, Cegelski L, Hultgren SJ. Morphological plasticity as a bacterial survival strategy. Nat Rev Microbiol 2008;6:162-8. https://doi.org/10.1038/nrmicro1820
  23. Everis L, Betts G. pH stress can cause cell elongation in Bacillus and Clostridium species: a research note. Food Control 2001; 12:53-6. https://doi.org/10.1016/S0956-7135(00)00017-7
  24. Misra G, Rojas ER, Gopinathan A, Huang KC. Mechanical consequences of cell-wall turnover in the elongation of a Gram-positive bacterium. Biophys J 2013;104:2342-52. https://doi.org/10.1016/j.bpj.2013.04.047

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