Proline-based cyclic dipeptides from Korean fermented vegetable kimchi and from Leuconostoc mesenteroides LBP-Ko6 have activities against multidrug-resistant bacteria

Frontiers in Microbiology

Volumn 8, Issue MAY, 2017, Pages

  Liu, Rui ^a   Kim, Andrew H ^a   Kwak, Min Kyu ^a   Kang, Sa Ouk ^a  

^a Seoul National University   (South Korea)

Author keywords

Cyclic dipeptides; Kimchi; Korean fermented foods; Lactic acid bacteria; Leuconostoc mesenteroides LBP K06

Indexed keywords

ANTIINFECTIVE AGENT; DIPEPTIDE; PROLINE;

ANTIBACTERIAL ACTIVITY; ARTICLE; CHINESE CABBAGE; COMPARATIVE STUDY; FERMENTATION; FERMENTED PRODUCT; FRACTIONATION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; KIMCHI; LACTOBACILLUS PLANTARUM; LEUCONOSTOC MESENTEROIDES; MASS FRAGMENTOGRAPHY; MINIMUM INHIBITORY CONCENTRATION; MULTIDRUG RESISTANCE; NONHUMAN; RADISH;

EID: 85019771369     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2017.00761     Document Type: Article

References (72)

1. Amoroso, M. J., Saguir, F. M., and Manca De Nadra, M. C. (1993). Variation of nutritional requirements of Leuconostoc oenos by organic acids. J. Int. Sci. Vigne Vin. 27, 135-144. doi: 10.20870/oeno-one.1993.27.2.1170
2. Bellezza, I., Peirce, M. J., and Minelli, A. (2014). Cyclic dipeptides: from bugs to brain. Trends Mol. Med. 20, 551-558. doi: 10.1016/j.molmed.2014.08.003
3. Borthwick, A. D. (2012). 2, 5-Diketopiperazines: synthesis, reactions, medicinal chemistry, and bioactive natural products. Chem. Rev. 112, 3641-3716. doi: 10.1021/cr200398y
4. Campbell, J., Lin, Q., Geske, G. D., and Blackwell, H. E. (2009). New and unexpected insights into the modulation of LuxR-type quorum sensing by cyclic dipeptides. ACS Chem. Biol. 4, 1051-1059. doi: 10.1021/cb900165y
5. Chang, J. Y., and 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. J. Food Sci. 75, M103-M110. doi: 10.1111/j.1750-3841.2009.01486.x
6. Cheigh, H. S., and Park, K. Y. (1994). Biochemical, microbiological, and nutritional aspects of kimchi (Korean fermented vegetable products). Crit. Rev. Food Sci. Nutr. 34, 175-203. doi: 10.1080/10408399409527656
7. Ciarkowski, J. (1984). CNDO/2 quantum-mechanical calculations of the conformational flexibility of the diketopiperazine skeleton. Biopolymers 23, 397-407. doi: 10.1002/bip.360230303
8. Crowley, S., Mahony, J., and Van Sinderen, D. (2013). Current perspectives on antifungal lactic acid bacteria as natural bio-preservatives. Trends Food Sci. Technol. 33, 93-109. doi: 10.1016/j.tifs.2013.07.004
9. De Man, J. C., Rogosa, M., and Sharpe, M. E. (1960). A medium for the cultivation of Lactobacilli. J. Appl. Microbiol. 23, 130-135. doi: 10.1111/j.1365-2672.1960.tb00188.x
10. Digaitiene, A., Hansen, ç.S., Juodeikiene, G., Eidukonyte, D., and Josephsen, J. (2012). Lactic acid bacteria isolated from rye sourdoughs produce bacteriocin-like inhibitory substances active against Bacillus subtilis and fungi. J. Appl. Microbiol. 112, 732-742. doi: 10.1111/j.1365-2672.2012.05249.x
11. Dinsmore, J. C., and Beshore, D. C. (2002). Recent advances in the synthesis of diketopiperazines. Tetrahedron 58, 3297-3312. doi: 10.1016/S0040-4020(02)00239-9
12. Elli, M., Zink, R., Reniero, R., and Morelli, L. (1999). Growth requirements of Lactobacillus johnsonii in skim and UHT milk. Int. Dairy J. 9, 507-513. doi: 10.1016/S0958-6946(99)00127-2
13. Eom, H. J., Park, J. M., Seo, M. J., Kim, M. D., and Han, N. S. (2008). Monitoring of Leuconostoc mesenteroides DRC starter in fermented vegetable by random integration of chloramphenicol acetyltransferase gene. J. Ind. Microbiol. Biotechnol. 35, 953-959. doi: 10.1007/s10295-008-0369-y
14. Fernádez, M., and Zúñiga, M. (2006). Amino acid catabolic pathways of lactic acid bacteria. Crit. Rev. Microbiol. 32, 155-183. doi: 10.1080/10408410600880643
15. Foucaud, C., Francois, A., and Richard, J. (1997). Development of a chemically defined medium for the growth of Leuconostoc mesenteroides. Appl. Environ. Microbiol. 63, 301-304.
16. Foucaud, C., Hemme, D., and Desmazeaud, M. (2001). Peptide utilization by Lactococcus lactis and Leuconostoc mesenteroides. Lett. Appl. Microbiol. 32, 20-25. doi: 10.1046/j.1472-765x.2001.00852.x
17. Freitas, M., Tavan, E., Cayuela, C., Diop, L., Sapin, C., and Trugnan, G. (2003a). Host-pathogens cross-talk. Indigenous bacteria and probiotics also play the game. Biol. Cell 95, 503-506. doi: 10.1016/j.biolcel.2003.08.004
18. Freitas, M., Tavan, E., Thoreux, K., Cayuela, C., Sapin, C., and Trugnan, G. (2003b). Lactobacillus casei DN-114 001 and Bacteroides thetaitaomicrom VPI-5482 inhibit rotavirus infection by modulating apical glycosylation pattern of cultured human intestinal HT29-MTX cells. Gastroenterology 124, A475-A476. doi: 10.1016/S0016-5085(03)82406-X
19. Gänzle, M. G., Höltzel, A., Walter, J., Jung, G., and Hammes, W. P. (2000). Characterization of reutericyclin produced by Lactobacillus reuteri LTH2584. Appl. Environ. Microbiol. 66, 4325-4333. doi: 10.1128/AEM.66.10.4325-4333.2000
20. Giraffa, G., and Rossetti, L. (2004). Monitoring of the bacterial composition of dairy starter cultures by RAPD-PCR. FEMS Microbiol. Lett. 237, 133-138. doi: 10.1111/j.1574-6968.2004.tb09688.x
21. Graz, M., Hunt, A., Jamie, H., Grant, G., and Milne, P. (1999). Antimicrobial activity of selected cyclic dipeptides. Pharmazie 54, 772-775.
22. Grobben, G. J., Peters, S. W., Wisselink, H. W., Weusthuis, R. A., Hoefnagel, M. H., Hugenholtz, J., et al. (2001). Spontaneous formation of a mannitol-producing variant of Leuconostoc pseudomesenteroides grown in the presence of fructose. Appl. Environ. Microbiol. 67, 2867-2870. doi: 10.1128/AEM.67.6.2867-2870.2001
23. Ha, J. H., Hawer, W. S., Kim, Y. J., and Nam, Y. (1989). Changes of free sugars in kimchi during fermentation. Korean J. Food Sci. Technol. 21, 633-638.
24. Holden, M. T., Ram Chhabra, S., De Nys, R., Stead, P., Bainton, N. J., Hill, P. J., et al. (1999). Quorum-sensing cross talk: isolation and chemical characterization of cyclic dipeptides from Pseudomonas aeruginosa and other gram-negative bacteria. Mol. Microbiol. 33, 1254-1266. doi: 10.1046/j.1365-2958.1999.01577.x
25. Huang, R. M., Yi, X. X., Zhou, Y., Su, X., Peng, Y., and Gao, C. H. (2014). An update on 2, 5-diketopiperazines from marine organisms. Mar. Drugs 12, 6213-6235. doi: 10.3390/md12126213
26. Huang, R., Zhou, X., Xu, T., Yang, X., and Liu, Y. (2010). Diketopiperazines from marine organisms. Chem. Biodivers. 7, 2809-2829. doi: 10.1002/cbdv.200900211
27. Huys, G., D'haene, K., and Swings, J. (2002). Influence of the culture medium on antibiotic susceptibility testing of food-associated lactic acid bacteria with the agar overlay disc diffusion method. Lett. Appl. Microbiol. 34, 402-406. doi: 10.1046/j.1472-765X.2002.01109.x
28. Jagannath, A., Raju, P. S., and Bawa, A. S. (2012). A two-step controlled lactic fermentation of cabbage for improved chemical and microbiological qualities. J. Food Qual. 35, 13-20. doi: 10.1111/j.1745-4557.2011.00427.x
29. Jeong, D. W., Kim, H. R., and Lee, J. H. (2014). Genetic diversity of Staphylococcus equorum isolates from Saeu-jeotgal evaluated by multilocus sequence typing. Antonie Van Leeuwenhoek 106, 795-808. doi: 10.1007/s10482-014-0249-6
30. Jeong, S. H., Jung, J. Y., Lee, S. H., Jin, H. M., and Jeon, C. O. (2013). Microbial succession and metabolite changes during fermentation of dongchimi, traditional Korean watery kimchi. Int. J. Food Microbiol. 164, 46-53. doi: 10.1016/j.ijfoodmicro.2013.03.016
31. Ji, S.-H., Han, W.-C., Lee, J.-C., Cheong, C., Kang, S.-A., Lee, J.-H., et al. (2009). Effect of low temperature on the qualities of long-term fermented kimchi (Korean pickled cabbage). Korean J. Food Preserv. 16, 804-809.
32. Jung, J. Y., Lee, S. H., and Jeon, C. O. (2014). Kimchi microflora: history, current status, and perspectives for industrial kimchi production. Appl. Microbiol. Biotechnol. 98, 2385-2393. doi: 10.1007/s00253-014-5513-1
33. Jung, J. Y., Lee, S. H., Kim, J. M., Park, M. S., Bae, J. W., Hahn, Y., et al. (2011). Metagenomic analysis of kimchi, a traditional Korean fermented food. Appl. Environ. Microbiol. 77, 2264-2274. doi: 10.1128/AEM.02157-10
34. Jung, J. Y., Lee, S. H., Lee, H. J., Seo, H. Y., Park, W. S., and Jeon, C. O. (2012). Effects of Leuconostoc mesenteroides starter cultures on microbial communities and metabolites during kimchi fermentation. Int. J. Food Microbiol. 153, 378-387. doi: 10.1016/j.ijfoodmicro.2011.11.030
35. Kim, B. H., Lee, H. S., Jang, Y. A., Lee, J. Y., Cho, Y. J., and Kim, C.-I. (2009). Development of amino acid composition database for Korean foods. J. Food Compos. Anal. 22, 44-52. doi: 10.1016/j.jfca.2008.07.005
36. Kwak, M.-K., Liu, R., Kim, M.-K., Moon, D., Kim, A. H., Song, S.-H., et al. (2014a). Cyclic dipeptides from lactic acid bacteria inhibit the proliferation of pathogenic fungi. J. Microbiol. 52, 64-70. doi: 10.1007/s12275-014-3520-7
37. Kwak, M.-K., Liu, R., Kwon, J.-O., Kim, M.-K., Kim, A. H., and Kang, S.-O. (2013). Cyclic dipeptides from lactic acid bacteria inhibit proliferation of the influenza A virus. J. Microbiol. 51, 836-843. doi: 10.1007/s12275-013-3521-y
38. Kwak, S. H., Cho, Y. M., Noh, G. M., and Om, A. S. (2014b). Cancer preventive potential of kimchi lactic acid bacteria (Weissella cibaria, Lactobacillus plantarum). J. Cancer Prev. 19, 253-258. doi: 10.15430/JCP.2014.19.4.253
39. Kwon, O. S., Park, S. H., Yun, B., Pyun, Y. R., and Kim, C. (2000). Cyclo(dehydroala-L-Leu), an α-glucosidase inhibitor from Penicillium sp. F70614. J. Antibiot. 53, 954-958. doi: 10.7164/antibiotics.53.954
40. Lee, C.-W., Ko, C.-Y., and Ha, D.-M. (1992). Microfloral changes of the lactic acid bacteria during kimchi fermentation and identification of the isolates. Korean J. Appl. Microbiol. Biotechnol. 20, 102-109.
41. Lee, D., Kim, S., Cho, J., and Kim, J. (2008). Microbial population dynamics and temperature changes during fermentation of kimjang kimchi. J. Microbiol. 46, 590-593. doi: 10.1007/s12275-008-0156-5
42. Lee, H. J., Joo, Y. J., Park, C. S., Kim, S. H., Hwang, I. K., Ahn, J. S., et al. (1999). Purification and characterization of a bacteriocin produced by Lactococcus lactis subsp. lactis H-559 isolated from kimchi. J. Biosci. Bioeng. 88, 153-159. doi: 10.1016/S1389-1723(99)80194-7
43. Li, H., Liu, L., Zhang, S., Cui, W., and Lv, J. (2012). Identification of antifungal compounds produced by Lactobacillus casei AST18. Curr. Microbiol. 65, 156-161. doi: 10.1007/s00284-012-0135-2
44. Li, J., Wang, W., Xu, S. X., Magarvey, N. A., and Mccormick, J. K. (2011). Lactobacillus reuteri-produced cyclic dipeptides quench agr-mediated expression of toxic shock syndrome toxin-1 in staphylococci. Proc. Natl. Acad. Sci. U.S.A. 108, 3360-3365. doi: 10.1073/pnas.1017431108
45. Lind, H., Sjögren, J., Gohil, S., Kenne, L., Schnürer, J., and Broberg, A. (2007). Antifungal compounds from cultures of dairy propionibacteria type strains. FEMS Microbiol. Lett. 271, 310-315. doi: 10.1111/j.1574-6968.2007.00730.x
46. Magnusson, J., Ström, K., Roos, S., Sjögren, J., and Schnürer, J. (2003). Broad and complex antifungal activity among environmental isolates of lactic acid bacteria. FEMS Microbiol. Lett. 219, 129-135. doi: 10.1016/S0378-1097(02)01207-7
47. Mayshak, J., Yoder, O. C., Beamer, K. C., and Shelton, D. C. (1966). Inhibition and transport kinetic studies involving L-leucine, L-valine, and their dipeptides in Leuconostoc mesenteroides. Arch. Biochem. Biophys. 113, 189-194. doi: 10.1016/0003-9861(66)90173-1
48. Messens, W., and De, V. L. (2002). Inhibitory substances produced by Lactobacilli isolated from sourdoughs-a review. Int. J. Food Microbiol. 72, 31-43. doi: 10.1016/S0168-1605(01)00611-0
49. Naidu, A. S., Bidlack, W. R., and Clemens, R. A. (1999). Probiotic spectra of lactic acid bacteria (LAB). Crit. Rev. Food Sci. Nutr. 39, 13-126. doi: 10.1080/10408699991279187
50. Naz, S., Gueguen-Minerbe, M., Cretenet, M., and Vernoux, J.-P. (2013). Aromatic amino acids as precursors of antimicrobial metabolites in Geotrichum candidum. FEMS Microbiol. Lett. 344, 39-47. doi: 10.1111/1574-6968.12152
51. Niku-Paavola, M. L., Laitila, A., Mattila-Sandholm, T., and Haikara, A. (1999). New types of antimicrobial compounds produced by Lactobacillus plantarum. J. Appl. Microbiol. 86, 29-35. doi: 10.1046/j.1365-2672.1999.00632.x
52. Panda, B. P., Javed, S., and Ali, M. (2007). Fermentation process optimization. Res. J. Microbiol. 2, 201-208. doi: 10.3923/jm.2007.201.208
53. Paulo, L., Ferreira, S., Gallardo, E., Queiroz, J. A., and Domingues, F. (2010). Antimicrobial activity and effects of resveratrol on human pathogenic bacteria. World J. Microbiol. Biotechnol. 26, 1533-1538. doi: 10.1007/s11274-010-0325-7
54. Prasad, C. (1995). Bioactive cyclic dipeptides. Peptides 16, 151-164. doi: 10.1016/0196-9781(94)00017-Z
55. Rhee, K. H. (2002). Isolation and characterization of Streptomyces sp. KH-614 producing anti-VRE (vancomycin-resistant enterococci) antibiotics. J. Gen. Appl. Microbiol. 48, 327-331. doi: 10.2323/jgam.48.321
56. Ross, R. P., Morgan, S., and Hill, C. (2002). Preservation and fermentation: past, present and future. Int J Food Microbiol 79, 3-16. doi: 10.1016/S0168-1605(02)00174-5
57. Rouse, S., and Van Sinderen, D. (2008). Bioprotective potential of lactic acid bacteria in malting and brewing. J. Food Prot. 71, 1724-1733. doi: 10.4315/0362-028X-71.8.1724
58. Saguir, F. M., and Manca De Nadra, M. C. (2007). Improvement of a chemically defined medium for the sustained growth of Lactobacillus plantarum: nutritional requirements. Curr. Microbiol. 54, 414-418. doi: 10.1007/s00284-006-0456-0
59. Sarika, A. R., Lipton, A. P., Aishwarya, M. S., and Dhivya, R. S. (2012). Isolation of a bacteriocin-producing lactococcus lactis and application of its bacteriocin to manage spoilage bacteria in high-value marine fish under different storage temperatures. Appl. Biochem. Biotechnol. 167, 1280-1289. doi: 10.1007/s12010-012-9701-0
60. Sauguet, L., Moutiez, M., Li, Y., Belin, P., Seguin, J., Le Du, M. H., et al. (2011). Cyclodipeptide synthases, a family of class-I aminoacyl-tRNA synthetase-like enzymes involved in non-ribosomal peptide synthesis. Nucleic Acids Res. 39, 4475-4489. doi: 10.1093/nar/gkr027
61. Shin, D., and Jeong, D. (2015). Korean traditional fermented soybean products: Jang. J. Ethnic Foods 2, 2-7. doi: 10.1016/j.jef.2015.02.002
62. Ström, K., Sjögren, J., Broberg, A., and Schnürer, 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. Appl. Environ. Microbiol. 68, 4322-4327. doi: 10.1128/AEM.68.9.4322-4327.2002
63. Todorov, S. D., Botes, M., Guigas, C., Schillinger, U., Wiid, I., Wachsman, M. B., et al. (2008). Boza, a natural source of probiotic lactic acid bacteria. J. Appl. Microbiol. 104, 465-477. doi: 10.1111/j.1365-2672.2007.03558.x
64. Vandenbergh, P. A. (1993). Lactic acid bacteria, their metabolic products and interference with microbial growth. FEMS Microbiol. Rev. 12, 221-237. doi: 10.1111/j.1574-6976.1993.tb00020.x
65. Wang, H., Yan, Y., Wang, J., Zhang, H., and Qi, W. (2012). Production and characterization of antifungal compounds produced by Lactobacillus plantarum IMAU10014. PLoS ONE 7:e29452. doi: 10.1371/journal.pone.0029452
66. Wattana-Amorn, P., Charoenwongsa, W., Williams, C., Crump, M. P., and Apichaisataienchote, B. (2015). Antibacterial activity of cyclo(L-Pro-L-Tyr) and cyclo(D-Pro-L-Tyr) from Streptomyces sp. strain 22-4 against phytopathogenic bacteria. Nat. Prod. Res. 15, 1-4. doi: 10.1080/14786419.2015.1095747
67. Winters, D. A., Poolman, B., Hemme, D., and Konings, W. N. (1991). Branched-chain amino acid transport in cytoplasmic membranes of Leuconostoc mesenteroides subsp. dextranicum CNRZ 1273. Appl. Environ. Microbiol. 57, 3350-3354.
68. Witiak, D. T., and Wei, Y. (1990). Dioxopiperazines: chemistry and biology. Prog. Drug Res. 35, 249-363. doi: 10.1007/978-3-0348-7133-4_7
69. Yan, P.-S., Song, Y., Sakuno, E., Nakajima, H., Nakagawa, H., and Yabe, K. (2004). Cyclo(Lleucyl-L-prolyl) produced by Achromobacter xylosoxidans inhibits aflatoxin production by Aspergillus parasiticus. Appl. Environ. Microbiol. 70, 7466-7473. doi: 10.1128/AEM.70.12.7466-7473.2004
70. Yang, E. J., and Chang, H. C. (2010). Purification of a new antifungal compound produced by Lactobacillus plantarum AF1 isolated from kimchi. Int. J. Food Microbiol. 139, 56-63. doi: 10.1016/j.ijfoodmicro.2010.02.012
71. Yang, E. J., Kim, Y. S., and Chang, H. C. (2011). Purification and characterization of antifungal d-dodecalactone from Lactobacillus plantarum AF1 isolated from kimchi. J. Food Prot. 74, 651-657. doi: 10.4315/0362-028X.JFP-10-512
72. Young, J. E. (2016). Advances in chromatographic analysis of foods and beverages modern stationary phases for challenging compounds. Agro Food Ind. Hi Tech 27, 14-17.