The Korean Journal of Food & Health Convergence (식품보건융합연구)

Korea Food & Health Convergence Association (한국식품보건융합학회)
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The Antibacterial Properties of Filtrates from Chinese Cabbage Kimchi

  • Seong-Soo CHA (Dept. of Food Science and Service, College of Bio-Convergence, Eulji University) ;
  • JeungSun LEE (Dept. of Mortuary Science, College of Bio Convergence, Eulji University) ;
  • Min-Kyu KWAK (Laboratory of Microbial Physiology and Biotechnology, Dept. of Food and Nutrition, College of Bio-Convergence, and Institute of Food and Nutrition Science, Eulji University)
  • Received : 2023.11.21
  • Accepted : 2023.12.25
  • Published : 2023.12.30
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Abstract

Lactobacillus plantarum and Leuconostoc mesenteroides are crucial functional starters and predominant isolates in a wide range of fermented foods, particularly kimchi, whose constituents exhibit bioactive properties. We previously developed a methodology using anion exchange resins to purify peptidyl compounds from Lb. plantarum LBP-K10. Antibacterial cultures of Lb. plantarum LBP-K10 were obtained from the respective cultures' supernatants and filtrates. However, conclusive evidence of the efficacy of kimchi filtrates in eradicating pathogenic bacteria is lacking. We aimed to simulate the potential effects of antibacterial filtrates that contained antibacterial compounds which were derived from cultures of Lb. plantarum LBP-K10. We acquired the kimchi filtrates using a combination of centrifugation and filtration methodologies, without the requirement for inoculation. The filtered liquid from Chinese cabbage kimchi, inoculated with Lb. plantarum LBP-K10 as a starter culture, and the non-inoculated liquid from Chinese cabbage kimchi (referred to as CCK and CCKRef, respectively) were were examined. CCK demonstrated greater inhibitory activity and a more significant bactericidal effect against the bacterial indicator strains. The minimum inhibitory concentration demonstrated comparable outcomes in tests against both Gram-positive and Gram-negative bacteria. This research offers a groundbreaking examination that displays the effectiveness of profiling peptidyl compounds within kimchi filtrates for curing bacterial infections.

Keywords

Acknowledgement

The authors would like to thank Dr. Chun Kang and Dr. Gieun Rhie (Center for Infectious Diseases, National Institute of Health, Korea Centers for Disease Control and Prevention, Cheongwon-gun, Chungcheongbukdo, South Korea) for helpful information on the multidrug-resistant bacteria.

References

  1. Archer, A. C., & Halami, P. M. (2015). Probiotic attributes of Lactobacillus fermentum isolated from human feces and dairy products. Applied Microbiology and Biotechnology, 99, 8113-8123. https://doi.org/10.1007/s00253-015-6679-x
  2. Bellezza, I., Peirce, M. J., & Minelli, A. (2014). Cyclic dipeptides: from bugs to brain. Trends in Molecular Medicine, 20, 551-558. https://doi.org/10.1016/j.molmed.2014.08.003
  3. Bhushan, R., & Dixit, S. (2012). HPLC enantioresolution of (R,S)-baclofen using three newly synthesized dichloro-s-triazine reagents having amines and five others having amino acids as chiral auxiliaries. Biomedical Chromatography, 26, 743-748. https://doi.org/10.1002/bmc.1723
  4. Bobbitt, J., & Betts, R. (1992). The removal of bacteria from solutions by membrane filtration. Journal of Microbiological Methods, 16(3), 215-220. https://doi.org/10.1016/0167-7012(92)90006-P
  5. Borthwick, A. D. (2012). 2,5-Diketopiperazines: synthesis, reactions, medicinal chemistry, and bioactive natural products. Chemical Reviews, 112, 3641-3716. https://doi.org/10.1021/cr200398y
  6. Bruckner, C., Fahr, A., Imhof, D., & Scriba, G. K. (2012). Degradation kinetics of an aspartyl-tripeptide-derived diketopiperazine under forced conditions. Journal of Pharmaceutical Sciences, 101, 4178-4190. https://doi.org/10.1002/jps.23272
  7. Chang, J. Y., & Chang, H. C. (2010). Improvements in the quality and shelf life of kimchi by fermentation with the induced bacteriocin-producing strain, Leuconostoc citreum GJ7 as a starter. Journal of Food Science, 75, M103-M110. https://doi.org/10.1111/j.1750-3841.2009.01486.x
  8. Cheigh, H. S., & Park, K. Y. (1994). Biochemical, microbiological, and nutritional aspects of kimchi (Korean fermented vegetable products). Critical Reviews in Food Science and Nutrition, 34, 175-203. https://doi.org/10.1080/10408399409527656
  9. Dal Bello, F., Clarke, C. I., Ryan, L. A. M., Ulmer, H., Schober, T. J., Strom, K., . . . Arendt, E. K. (2007). Improvement of the quality and shelf life of wheat bread by fermentation with the antifungal strain Lactobacillus plantarum FST 1.7. Journal of Cereal Science, 45, 309-318. https://doi.org/10.1016/j.jcs.2006.09.004
  10. De Man, J. C., Rogosa, M., & Sharpe, M. E. (1960). A medium for the cultivation of Lactobacilli. Journal of Applied Microbiology, 23, 130-135.
  11. Deepa, I., Kumar, S. N., Sreerag, R. S., Nath, V. S., & Mohandas, C. (2015). Purification and synergistic antibacterial activity of arginine derived cyclic dipeptides, from Achromobacter sp. associated with a rhabditid entomopathogenic nematode against major clinically relevant biofilm forming wound bacteria. Frontiers in Microbiology, 6, 876.
  12. Eom, H. J., Park, J. M., Seo, M. J., Kim, M. D., & Han, N. S. (2008). Monitoring of Leuconostoc mesenteroides DRC starter in fermented vegetable by random integration of chloramphenicol acetyltransferase gene. Journal of Industrial Microbiology and Biotechnology, 35, 953-959. https://doi.org/10.1007/s10295-008-0369-y
  13. Funasaki, N., Hada, S., & Neya, S. (1993). Conformational effects in reversed-phase liquid chromatographic separation of diastereomers of cyclic dipeptides. Analytical Chemistry, 65, 1861-1867. https://doi.org/10.1021/ac00062a010
  14. Ha, J. H., Hawer, W. S., Kim, Y. J., & Nam, Y. (1989). Changes of free sugars in kimchi during fermentation. Korean Journal of Food Science and Technology, 21, 633-638.
  15. Ishikawa, K., Hosoe, T., Itabashi, T., Wakana, D., Takizawa, K., Yaguchi, T., & Kawai, K. (2010). Novoamauromine and ent-Cycloechinulin: two new diketopiperazine derivatives from Aspergillus novofumigatus. Chemical and Pharmaceutical Bulletin, 58, 717-719. https://doi.org/10.1248/cpb.58.717
  16. Jeong, S. H., Jung, J. Y., Lee, S. H., Jin, H. M., & Jeon, C. O. (2013). Microbial succession and metabolite changes during fermentation of dongchimi, traditional Korean watery kimchi. International Journal of Food Microbiology, 164, 46-53. https://doi.org/10.1016/j.ijfoodmicro.2013.03.016
  17. Ji, K., Jang, N. Y., & Kim, Y. T. (2015). Isolation of Lactic Acid Bacteria Showing Antioxidative and Probiotic Activities from Kimchi and Infant Feces. Journal of Microbiology and Biotechnology, 25, 1568-1577. https://doi.org/10.4014/jmb.1501.01077
  18. Jung, J. Y., Lee, S. H., & Jeon, C. O. (2014). Kimchi microflora: history, current status, and perspectives for industrial kimchi production. Applied Microbiology and Biotechnology, 98, 2385-2393. https://doi.org/10.1007/s00253-014-5513-1
  19. Jung, J. Y., Lee, S. H., Kim, J. M., Park, M. S., Bae, J. W., Hahn, Y., Jeon, C. O. (2011). Metagenomic analysis of kimchi, a traditional Korean fermented food. Applied and Environmental Microbiology, 77, 2264-2274. https://doi.org/10.1128/AEM.02157-10
  20. Jung, J. Y., Lee, S. H., Lee, H. J., Seo, H. Y., Park, W. S., & Jeon, C. O. (2012). Effects of Leuconostoc mesenteroides starter cultures on microbial communities and metabolites during kimchi fermentation. International Journal of Food Microbiology, 153, 378-387. https://doi.org/10.1016/j.ijfoodmicro.2011.11.030
  21. Kumar, S. N., Lankalapalli, R. S., & Kumar, B. S. (2014). In vitro antibacterial screening of six proline-based cyclic dipeptides in combination with β-lactam antibiotics against medically important bacteria. Applied Biochemistry and Biotechnology, 173, 116-128. https://doi.org/10.1007/s12010-014-0808-3
  22. Kwak, M.-K., Liu, R., & Kang, S.-O. (2018). Antimicrobial activity of cyclic dipeptides produced by Lactobacillus plantarum LBP-K10 against multidrug-resistant bacteria, pathogenic fungi, and influenza A virus. Food Control, 85, 223-234. https://doi.org/10.1016/j.foodcont.2017.10.001
  23. Kwak, M.-K., Liu, R., Kim, M.-K., Moon, D., Kim, A. H., Song, S.-H., & Kang, S.-O. (2014). Cyclic dipeptides from lactic acid bacteria inhibit the proliferation of pathogenic fungi. Journal of Microbiology, 52, 64-70. doi:10.1007/s12275-014-3520-7
  24. Kwak, M.-K., Liu, R., Kwon, J.-O., Kim, M.-K., Kim, A. H., & Kang, S.-O. (2013). Cyclic dipeptides from lactic acid bacteria inhibit proliferation of the influenza A virus. Journal of Microbiology, 51, 836-843. doi:10.1007/s12275-013-3521-y
  25. Lee, D., Kim, S., Cho, J., & Kim, J. (2008). Microbial population dynamics and temperature changes during fermentation of kimjang kimchi. Journal of Microbiology, 46, 590-593. https://doi.org/10.1007/s12275-008-0156-5
  26. Lesma, G., Cecchi, R., Crippa, S., Giovanelli, P., Meneghetti, F., Musolino, M., Silvani, A. (2012). Ugi 4-CR/Pictet-Spengler reaction as a short route to tryptophan-derived peptidomimetics. Organic & Biomolecular Chemistry, 10, 9004-9012. https://doi.org/10.1039/c2ob26301g
  27. Li, H., Liu, L., Zhang, S., Cui, W., & Lv, J. (2012). Identification of antifungal compounds produced by Lactobacillus casei AST18. Current Microbiology, 65, 156-161. https://doi.org/10.1007/s00284-012-0135-2
  28. Lim, S. M., & Im, D. S. (2009). Screening and characterization of probiotic lactic acid bacteria isolated from Korean fermented foods. Journal of Microbiology and Biotechnology, 19, 178-186. https://doi.org/10.4014/jmb.0804.269
  29. Liu, C. J., Wang, R., Gong, F. M., Liu, X. F., Zheng, H. J., Luo, Y. Y., & Li, X. R. (2015). Complete genome sequences and comparative genome analysis of Lactobacillus plantarum strain 5-2 isolated from fermented soybean. Genomics, 106, 404-411. https://doi.org/10.1016/j.ygeno.2015.07.007
  30. Liu, R., Kim, A., Kwak, M.-K., & Kang, S.-O. (2017). Proline-Based Cyclic Dipeptides from Korean Fermented Vegetable Kimchi and from Leuconostoc mesenteroides LBP-K06 Have Activities against Multidrug-Resistant Bacteria. Frontiers in Microbiology, 8, 761.
  31. Lukaszewicz, R., & Meltzer, T. (1979). Concerning filter validation. Journal of the Parenteral Drug Association, 33(4), 187-194.
  32. Lukaszewicz, R., Tanny, G., & Meltzer, T. (1978). Membrane filter characterizations and their implications for particulate retention. Pharmaceutical Technology, 2(11), 77-83.
  33. Mayo, B., van Sinderen, D., & Ventura, M. (2008). Genome analysis of food grade lactic acid-producing bacteria: from basics to applications. Current Genomics, 9, 169-183. https://doi.org/10.2174/138920208784340731
  34. Michael, J., Barth, A., Kloft, C., & Derendorf, H. (2014). Pharmacodynamic in vitro models to determine the effect of antibiotics. Fundamentals of Antimicrobial Pharmacokinetics and Pharmacodynamics, 81-112.
  35. Osumi, M., Yamada, N., & Toya, M. (1996). Bacterial retention mechanisms of membrane filters. PDA Journal of Pharmaceutical Science and Technology, 50(1), 30-34.
  36. Ozogul, F., & Hamed, I. (2017). The importance of lactic acid bacteria for the prevention of bacterial growth and their biogenic amines formation: A review. Critical Reviews in Food Science and Nutrition, 27, 1-11.
  37. Perzborn, M., Syldatk, C., & Rudat, J. (2013). Separation of cyclic dipeptides (diketopiperazines) from their corresponding linear dDipeptides by RP-HPLC and method validation. Chromatography Research International, 2013, 1-8. https://doi.org/10.1155/2013/310269
  38. Pillai, S., Moellering, R., Eliopoulos, G., & Lorian, V. (2005). Antibiotics in laboratory medicine. Antibiotics in Laboratory Medicine. 5th ed. Baltimore, MD: Lippincott Williams & Wilkins, 365-440.
  39. Powers, T., Varma, K., & Powers, J. (1984). Selecting therapeutic concentrations: minimum inhibitory concentrations vs subminimum or supraminimum inhibitory concentrations. Journal of the American veterinary medical association, 185(10), 1062-1067.
  40. Ren, D., Li, C., Qin, Y., Yin, R., Du, S., Ye, F., . . . Jin, N. (2014). In vitro evaluation of the probiotic and functional potential of Lactobacillus strains isolated from fermented food and human intestine. Anaerobe, 30, 1-10. https://doi.org/10.1016/j.anaerobe.2014.07.004
  41. Rhee, K. H. (2002). Isolation and characterization of Streptomyces sp. KH-614 producing anti-VRE (vancomycin-resistant enterococci) antibiotics. The Journal of General and Applied Microbiology, 48, 327-331.
  42. Rhee, K. H. (2004). Cyclic dipeptides exhibit synergistic, broad spectrum antimicrobial effects and have anti-mutagenic properties. International Journal of Antimicrobial Agents, 24, 423-427. https://doi.org/10.1016/j.ijantimicag.2004.05.005
  43. Schmidt, S., Barbour, A., Sahre, M., Rand, K. H., & Derendorf, H. (2008). PK/PD: new insights for antibacterial and antiviral applications. Current opinion in pharmacology, 8(5), 549-556. https://doi.org/10.1016/j.coph.2008.06.010
  44. Shan, Z., Xiong, Y., Yi, J., & Hu, X. (2008). Heterocomplexation of a chiral dipeptide and quantitative enantiomeric enrichment of nonracemic 1,1'-bi-2-naphthol. The Journal of Organic Chemistry, 73, 9158-9160. https://doi.org/10.1021/jo801547j
  45. Strom, K., Sjogren, J., Broberg, A., & Schnurer, J. (2002). Lactobacillus plantarum MiLAB 393 produces the antifungal cyclic dipeptides cyclo(L-Phe-L-Pro) and cyclo(L-Phe-trans-4-OH-L-Pro) and 3-phenyllactic acid. Applied and Environmental Microbiology, 68, 4322-4327. https://doi.org/10.1128/AEM.68.9.4322-4327.2002
  46. Swadesh, J. K. (2000). HPLC: Practical and Industrial Applications. CRC Press, Second Edition, 167-169.
  47. Sy, S. K., & Derendorf, H. (2014). Pharmacometrics in bacterial infections. Applied pharmacometrics, 229-258.
  48. Thakur, M., & Belwal, T. (2022). Bioactive Components: A Sustainable System for Good Health and Well-Being: Springer Nature.
  49. Todd, R., & Kerr, T. (1972). Scanning electron microscopy of microbial cells on membrane filters. Applied Microbiology, 23(6), 1160-1162. https://doi.org/10.1128/am.23.6.1160-1162.1972
  50. Velkov, T., Bergen, P. J., Lora-Tamayo, J., Landersdorfer, C. B., & Li, J. (2013). PK/PD models in antibacterial development. Current opinion in microbiology, 16(5), 573-579. https://doi.org/10.1016/j.mib.2013.06.010
  51. Wiegand, I., Hilpert, K., & Hancock, R. E. W. (2008). Agar and broth dilution methods to determine the minimal inhibitory concentration (MIC) of antimicrobial substances. Nature Protocols, 3, 163-175. https://doi.org/10.1038/nprot.2007.521
  52. Wikler, M. A. (2006). Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically: approved standard: Clinical and laboratory standards institute. 26, M7-A7.
  53. Yan, P.-S., Song, Y., Sakuno, E., Nakajima, H., Nakagawa, H., & Yabe, K. (2004). Cyclo(Lleucyl-L-prolyl) produced by Achromobacter xylosoxidans inhibits aflatoxin production by Aspergillus parasiticus. Applied and Environmental Microbiology, 70, 7466-7473. https://doi.org/10.1128/AEM.70.12.7466-7473.2004
  54. Yang, E. J., Kim, Y. S., & Chang, H. C. (2011). Purification and characterization of antifungal δ-dodecalactone from Lactobacillus plantarum AF1 isolated from kimchi. Journal of Food Protection, 74, 651-657. https://doi.org/10.4315/0362-028X.JFP-10-512
  55. Young, J. E. (2016). Advances in chromatographic analysis of foods and beverages modern stationary phases for challenging compounds. Agro Food Industry Hi Tech, 27, 14-17.