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Antimicrobial and anti-biofilm effects of probiotic Lactobacillus plantarum KU200656 isolated from kimchi

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Abstract

The probiotic properties and anti-pathogenic effects of Lactobacillus plantarum KU200656 (KU200656) isolated from Korean fermented kimchi against Staphylococcus aureus, Listeria monocytogenes, Escherichia coli, and Salmonella Typhimurium were investigated. KU200656 showed high tolerance to artificial gastric acid (99.48%) and bile salts (102.40%) and this strain was safe according to antibiotic sensitivity test; it could not produce harmful enzymes, including β-glucuronidase. KU200656 exhibited high adhesion (4.45%) to intestinal cells, HT-29 cells, with high cell surface hydrophobicity (87.31% for xylene and 81.11% for toluene). Moreover, KU200656 co-aggregated with pathogenic bacteria and exhibited antibacterial activity and anti-adhesion properties against pathogens. The cell-free supernatant (CFS) of KU200656 inhibited biofilm formation by pathogenic bacteria. In addition, half of the minimum inhibitory concentration of the KU200656 CFS downregulated the expression of biofilm-related genes, as determined by quantitative real-time PCR. Therefore, KU200656 was demonstrated to possess anti-pathogenic effects and have potential for use as probiotics in the food industry.

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References

  • Arciola CR, Campoccia D, Ravaioli S, Montanaro L. Polysaccharide intercellular adhesin in biofilm: structural and regulatory aspects. Front. Cell. Infect. Microbiol. 5: 1-10 (2015)

    Article  Google Scholar 

  • Bai JR, Zhong K, Wu YP, Elena G, Gao H. Antibiofilm activity of shikimic acid against Staphylococcus aureus. Food Control 95: 327-333 (2019)

    Article  CAS  Google Scholar 

  • Behbahani BA, Noshad M, Falah F. Inhibition of Escherichia coli adhesion to human intestinal Caco-2 cells by probiotic candidate Lactobacillus plantarum strain L15. Microb. Pathog. 136: 103677 (2019)

    Article  Google Scholar 

  • Chen X, Tian F, Liu X, Zhao J, Zhang HP, Zhang H, Chen W. In vitro screening of lactobacilli with antagonistic activity against Helicobacter pylori from traditionally fermented foods. J. Dairy Sci. 93: 5627-5634 (2010)

    Article  CAS  Google Scholar 

  • CLSI. Performance standards for antimicrobial susceptibility testing; twenty-second informational supplement. Clin. Lab. Standards Institute. 32: 1-184 (2012)

  • FAO/WHO. Joint FAO/WHO (Food and Agriculture Organization/World Health Organization) working group report on drafting guidelines for the evaluation of probiotics in food. London, Ontario, Canada (2002)

  • García-Heredia A, García S, Merino-Mascorro JA, Feng P, Heredia N. Natural plant products inhibits growth and alters the swarming motility, biofilm formation, and expression of virulence genes in enteroaggregative and enterohemorrhagic Escherichia coli. Food Microbiol. 59: 124-132 (2016)

    Article  Google Scholar 

  • Jahid IK, Mizan MFR, Ha AJ, Ha SD. Effect of salinity and incubation time of planktonic cells on biofilm formation, motility, exoprotease production, and quorum sensing of Aeromonas hydrophila. Food Microbiol. 49: 142-151 (2015)

    Article  CAS  Google Scholar 

  • Jang HJ, Lee NK, Paik HD. Probiotic characterization of Lactobacillus brevis KU15153 showing antimicrobial and antioxidant effect isolated from kimchi. Food Sci. Biotechnol. 28: 1521-1528 (2019)

    Article  CAS  Google Scholar 

  • Jeon HL, Lee NK, Yang SJ, Kim WS, Paik HD. Probiotic characterization of Bacillus subtilis P223 isolated from kimchi. Food Sci. Biotechnol. 26: 1641-1648 (2017)

    Article  CAS  Google Scholar 

  • Keersmaecker CJ, Verhoeven TLA, Desair J, Marchal K, Vanderleyden J, Nagy I. Strong antimicrobial activity of Lactobacillus rhamnosus GG against Salmonella typhimurium is due to accumulation of lactic acid. FEMS Microbiol. Lett. 259: 89-96 (2006)

    Article  Google Scholar 

  • Lau LYJ, Chye FY. Antagonistic effects of Lactobacillus plantarum 0612 on the adhesion of selected foodborne enteropathogens in various colonic environments. Food Control 91: 237-247 (2018)

    Article  CAS  Google Scholar 

  • Lee NK, Kim WS, Paik HD. Bacillus strains as human probiotics: characterization, safety, microbiome, and probiotic carrier. Food Sci. Biotechnol. 28: 1297-1305 (2019)

    Article  CAS  Google Scholar 

  • Leite AMO, Miguel MAL, Peixoto RS, Ruas-Madiedo P, Paschoalin VMF, Mayo B, Delgado S. Probiotic potential of selected lactic acid bacteria strains isolated from Brazilian kefir grains. J. Dairy Sci. 98: 3622-3632 (2015)

    Article  CAS  Google Scholar 

  • Li R, Du W, Yang J, Liu Z, Yousef AE. Control of Listeria monocytogenes biofilm by paenibacterin, a natural antimicrobial lipopeptide. Food Control 84: 529-535 (2018a)

    Article  CAS  Google Scholar 

  • Li T, Wang D, Liu N, Ma Y, Ding T, Mei Y, Li J. Inhibition of quorum sensing-controlled virulence factors and biofilm formation in Pseudomonas fluorescens by cinnamaldehyde. Int. J. Food Microbiol. 269: 98-106 (2018b)

    Article  CAS  Google Scholar 

  • Liu M, Wu X, Li J, Liu L, Zhang R, Shao D, Du X. The specific anti-biofilm effect of gallic acid on Staphylococcus aureus by regulating the expression of the ica operon. Food Control 73: 613-618 (2017a)

    Article  CAS  Google Scholar 

  • Liu Z, Zhang Z, Qiu L, Zhang F, Xu X, Wei H, Tao X. Characterization and bioactivities of the exopolysaccharide from a probiotic strain of Lactobacillus plantarum WLPL04. J. Dairy Sci. 100: 6895-6905 (2017b)

    Article  CAS  Google Scholar 

  • Merino L, Trejo FM, De Antoni G, Golowczyc MA. Lactobacillus strains inhibit biofilm formation of Salmonella sp isolates from poultry. Food Res. Int. 123: 258-265 (2019)

    Article  CAS  Google Scholar 

  • Monteagudo-Mera A, Rastall RA, Gibson GR, Charalampopoulos D, Chatzifragkou A. Adhesion mechanisms mediated by probiotics and prebiotics and their potential impact on human health. Appl. Microbiol. Biotechnol. 103: 6463-6472 (2019)

    Article  CAS  Google Scholar 

  • Moradi M, Mardani K, Tajik H. Characterization and application of postbiotics of Lactobacillus spp. on Listeria monocytogenes in vitro and in food models. LWT-Food Sci. Technol. 111: 457-464 (2019)

    Article  CAS  Google Scholar 

  • Mohammedsaeed W, McBain AJ, Cruickshank SM, O’Neill CA. Lactobacillus rhamnosus GG inhibits the toxic effects of Staphylococcus aureus on epidermal keratinocytes. Appl. Environ. Microbiol. 80: 5773-5781 (2014)

    Article  Google Scholar 

  • Muhammad Z, Ramzan R, Adelazez A, Amjad A, Afzaal M, Zhang S, Pan S. Assessment of the antimicrobial potentiality and functionality of Lactobacillus plantarum strains isolated from the conventional inner Mongolian fermented cheese against foodborne pathogens. Pathogens 8: 71 (2019)

    Article  CAS  Google Scholar 

  • Rodríguez PFP, Arévalo-Villena M, Rosa IZ, Péreza AB. Selection of potential non-Saccharomyces probiotic yeasts from food origin by a step-by-step approach. Food Res. Int. 112: 143-151 (2018)

    Article  Google Scholar 

  • Sethupathy S, Vigneshwari L, Valliammai A, Balamurugan K, Pandian SK. L-Ascorbyl 2,6-dipalmitate inhibits biofilm formation and virulence in methicillin-resistant Staphylococcus aureus and prevents triacylglyceride accumulation in Caenorhabditis elegans. RSC Adv. 7: 23392-23406 (2017)

    Article  Google Scholar 

  • Son SH, Jeon HL, Yang SJ, Sim MH, Kim YJ, Lee NK, Paik HD. Probiotic lactic acid bacteria isolated from traditional Korean fermented foods based on β-glucosidase activity. Food Sci. Biotechnol. 27: 123-129 (2018a)

    Article  CAS  Google Scholar 

  • Son SH, Yang SJ, Jeon HL, Yu HS, Lee NK, Park YS, Paik HD. Antioxidant and immunostimulatory effect of potential probiotic Lactobacillus paraplantarum SC61 isolated from Korean traditional fermented food, jangajji. Microb. Pathog. 125: 486-492 (2018b)

    Article  CAS  Google Scholar 

  • Song H, Zhang J, Qu J, Liu J, Yin P, Zhang G, Shang D. Lactobacillus rhamnosus GG microcapsules inhibit Escherichia coli biofilm formation in coculture. Biotechnol. Lett. 41: 1007-1014 (2019)

    Article  CAS  Google Scholar 

  • Sun T, Li XD, Hong J, Liu C, Zhang XL, Zheng JP, Xu YJ, Ou ZY, Zheng JL, Yu DJ. Inhibitory effect of two traditional Chinese medicine monomers, berberine and matrine, on the quorum sensing system of antimicrobial-resistant Escherichia coli. Front. Microbiol. 10: 2584 (2019)

    Article  Google Scholar 

  • Tarrah A, Duarte VS, Castilhos J, Pakroo S, Lemos WJF Jr, Luchese RH, Guerra AF, Rossi RC, Ziegler DR, Corich V, Giacomini A. Probiotic potential and biofilm inhibitory activity of Lactobacillus casei group strains isolated from infant feces. J. Funct. Foods 54: 489-497 (2019)

    Article  CAS  Google Scholar 

  • Upadhyay A, Johny AK, Amalaradjou MAR, Baskaran SA, Kim KS, Venkitanarayanan K. Plant-derived antimicrobials reduce Listeria monocytogenes virulence factors in vitro, and down-regulate expression of virulence genes. Int. J. Food Microbiol. 157: 88-94 (2012)

    Article  CAS  Google Scholar 

  • Upadhyay A, Upadhyaya I, Kollanoor-Johny A, Venkitanarayanan K. Antibiofilm effect of plant derived antimicrobials on Listeria monocytogenes. Food Microbiol. 36: 79-89 (2013)

    Article  CAS  Google Scholar 

  • Yang SJ, Lee JE, Lim SM, Kim YJ, Lee NK, Paik HD. Antioxidant and immune-enhancing effects of probiotic Lactobacillus plantarum 200655 isolated from kimchi. Food Sci. Biotechnol. 28: 491-499 (2019)

    Article  CAS  Google Scholar 

  • Yan X, Gu S, Cui X, Shi Y, Wen S, Chen H, Ge J. Antimicrobial, anti-adhesive and anti-biofilm potential of biosurfactants isolated from Pediococcus acidilactici and Lactobacillus plantarum against Staphylococcus aureus CMCC26003. Microb. Pathog. 127: 12-20 (2019)

    Article  CAS  Google Scholar 

  • Ye K, Zhang X, Huang Y, Liu J, Liu M, Zhou G. Bacteriocinogenic Enterococcus faecium inhibits the virulence property of Listeria monocytogenes. LWT-Food Sci. Technol. 89: 87-92 (2018)

    Article  CAS  Google Scholar 

  • Zhang B, Zuo F, Yu R, Zeng Z, Ma H, Chen S. Comparative genome-based identification of a cell wall-anchored protein from Lactobacillus plantarum increases adhesion of Lactococcus lactis to human epithelial cells. Sci. Rep. 5: 14109 (2015)

    Article  CAS  Google Scholar 

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Acknowledgements

This work was supported by Korea Institute of Planning and Evaluation for Technology in Food, Agriculture and Forestry (IPET) through Innovational Food Technology Development Program (#119009-3), funded by Ministry of Agriculture, Food and Rural Affairs (MAFRA).

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Correspondence to Hyun-Dong Paik.

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Lee, JE., Lee, NK. & Paik, HD. Antimicrobial and anti-biofilm effects of probiotic Lactobacillus plantarum KU200656 isolated from kimchi. Food Sci Biotechnol 30, 97–106 (2021). https://doi.org/10.1007/s10068-020-00837-0

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