Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
권호 표지
DOI QR코드

DOI QR Code

Antimicrobial Cyclic Dipeptides from Japanese Quail (Coturnix japonica) Eggs Supplemented with Probiotic Lactobacillus plantarum

  • Sa-Ouk Kang (Laboratory of Biophysics, School of Biological Sciences, and Institute of Microbiology, Seoul National University) ;
  • Min-Kyu Kwak (Laboratory of Microbial Physiology and Biotechnology, Department of Food and Nutrition, College of Bio-Convergence, and Institute of Food and Nutrition Science, Eulji University)
  • Received : 2023.11.07
  • Accepted : 2023.12.13
  • Published : 2024.02.28
Download PDF
⟨ Previous Next ⟩

Abstract

Fifteen cyclic dipeptides (CDPs) containing proline, one cyclo(Phe-Ala) without proline, and a non-peptidyl ᴅⳑ-3-phenyllactic acid were previously identified in the culture filtrates of Lactobacillus plantarum LBP-K10, an isolate from kimchi. In this study, we used Japanese quail (Coturnix japonica) eggs to examine the effects of probiotic supplementation on the antimicrobial CDPs extracted from quail eggs (QE). Eggshell-free QE were obtained from two distinct groups of quails. The first group (K10N) comprised eggs from unsupplemented quails. The second group (K10S) comprised eggs from quails supplemented with Lb. plantarum LBP-K10. The QE samples were extracted using methylene chloride through a liquid-liquid extraction process. The resulting extract was fractionated into 16 parts using semi-preparative high-performance liquid chromatography. Two fractions, Q6 and Q9, were isolated from K10S and identified as cis-cyclo(ⳑ-Ser-ⳑ-Pro) and cis-cyclo(ⳑ-Leu-ⳑ-Pro). The Q9 fraction, containing cis-cyclo(ⳑ-Leu-ⳑ-Pro), has shown significant inhibitory properties against the proliferation of highly pathogenic multidrug-resistant bacteria, as well as human-specific and phytopathogenic fungi. Some of the ten combinations between the remaining fourteen unidentified fractions and two fractions, Q6 and Q9, containing cis-cyclo(ⳑ-Ser-ⳑ-Pro) and cis-cyclo(ⳑ-Leu-ⳑ-Pro) respectively, demonstrated a significant increase in activity against multidrug-resistant bacteria only when combined with Q9. The activity was 7.17 times higher compared to a single cis-cyclo(ⳑ-Leu-ⳑ-Pro). This study presents new findings on the efficacy of proline-containing CDPs in avian eggs. These CDPs provide antimicrobial properties when specific probiotics are supplemented.

Keywords

Acknowledgement

The authors would like to thank Dr. Chun Kang and Dr. Gi-eun Rhie from the Center for Infectious Diseases, National Institute of Health, Korea Centers for Disease Control and Prevention, Cheongwon-gun, Chungcheongbukdo, South Korea, for providing valuable information on multidrug-resistant bacteria. The authors also thank Cilic BioEngineering Sdn Bhd (CBE) in Taman Tawau, Sabah, Malaysia for providing the G. boninense isolate (GMR3). We also thank the NCIRF at Seoul National University for their support with the GC-MS experiments.

References

  1. Ji K, Jang NY, Kim YT. 2015. Isolation of lactic acid bacteria showing antioxidative and probiotic activities from Kimchi and infant feces. J. Microbiol. Biotechnol. 25: 1568-1577. 
  2. Archer AC, Halami PM. 2015. Probiotic attributes of Lactobacillus fermentum isolated from human feces and dairy products. Appl. Microbiol. Biotechnol. 99: 8113-8123. 
  3. Rouse S, van Sinderen D. 2008. Bioprotective potential of lactic acid bacteria in malting and brewing. J. Food Prot. 71: 1724-1733. 
  4. Ozogul F, Hamed I. 2017. The importance of lactic acid bacteria for the prevention of bacterial growth and their biogenic amines formation: a review. Crit. Rev. Food Sci. Nutr. 27: 1-11. 
  5. Bellezza I, Peirce MJ, Minelli A. 2014. Cyclic dipeptides: from bugs to brain. Trends Mol. Med. 20: 551-558. 
  6. Borthwick AD. 2012. 2,5-Diketopiperazines: synthesis, reactions, medicinal chemistry, and bioactive natural products. Chem. Rev. 112: 3641-3716. 
  7. Tsuruoka N, Beppu Y, Koda H, Doe N, Watanabe H, Abe K. 2012. A DKP cyclo (ᴸ-Phe-ᴸ-Phe) found in chicken essence is a dual inhibitor of the serotonin transporter and acetylcholinesterase. PLoS One 7: e50824. 
  8. Song S, Fu S, Sun X, Li P, Wu Je, Dong T, et al. 2018. Identification of cyclic dipeptides from Escherichia coli as new antimicrobial agents against Ralstonia solanacearum. Molecules 23: 214. 
  9. Elkahoui S, Abdel rahim H, Tabbene O, Shaaban M, Limam F, Laatsch H. 2013. Cyclo-(His, Leu): a new microbial diketopiperazine from a terrestrial Bacillus subtilis strain B38. Nat. Prod. Res. 27: 108-116. 
  10. Kumar SN, Mohandas C, Nambisan B, Sreerag RS, Jayaprakas CA. 2014. Cyclo(L-Pro-D-Arg): a new antibacterial and antitumour diketopiperazine from Bacillus cereus associated with a rhabditid entomopathogenic. Folia Microbiol. (Praha) 59: 197-202. 
  11. Kwon OS, Park SH, Yun B, Pyun YR, Kim C. 2000. Cyclo(dehydroala-ᴸ-Leu), an α-glucosidase inhibitor from Penicillium sp. F70614. J. Antibiot. 53: 954-958. 
  12. Nagia MMS, Shaaban M, Abdel-Aziz MS, El-Zalabani SM, Hanna AG. 2012. Secondary metabolites and bioactivity of two fungal strains. Egypt. Pharmaceut. J. 11: 16. 
  13. Uyemura K, Dhanani S, Yamaguchi DT, Song MK. 2010. Metabolism and toxicity of high doses of cyclo (His-Pro) plus zinc in healthy human subjects. J. Drug Metab. Toxicol. 1: 105. 
  14. Jung EY, Hong YH, Park C, Suh HJ. 2016. Effects of Cyclo-His-Pro-enriched yeast hydrolysate on blood glucose levels and lipid metabolism in obese diabetic ob/ob mice. Nutr. Res. Pract. 10: 154-160. 
  15. McCleland K, Milne PJ, Lucieto FR, Frost C, Brauns SC, Van De Venter M, et al. 2004. An investigation into the biological activity of the selected histidine-containing diketopiperazines cyclo(His-Phe) and cyclo(His-Tyr). J. Pharm. Pharmacol. 56: 1143-1153. 
  16. 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. 
  17. Liu R, Kim AH, 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. Front. Microbiol. 8: 761. 
  18. Ren D, Li C, Qin Y, Yin R, Du S, Ye F, et al. 2014. In vitro evaluation of the probiotic and functional potential of Lactobacillus strains isolated from fermented food and human intestine. Anaerobe 30: 1-10. 
  19. Dec M, Puchalski A, Urban-Chmiel R, Wernicki A. 2014. Screening of Lactobacillus strains of domestic goose origin against bacterial poultry pathogens for use as probiotics. Poult. Sci. 93: 2464-2472. 
  20. Hedberg M, Hasslof P, Sjostrom I, Twetman S, Stecksen-Blicks C. 2008. Sugar fermentation in probiotic bacteria-an in vitro study. Oral Microbiol. Immunol. 23: 482-485. 
  21. Borthwick AD, Da Costa NC. 2017. 2,5-diketopiperazines in food and beverages: Taste and bioactivity. Crit. Rev. Food Sci. Nutr. 57: 718-742. 
  22. Huang RM, Yi XX, Zhou Y, Su X, Peng Y, Gao CH. 2014. An update on 2,5-diketopiperazines from marine organisms. Mar. Drugs 12: 6213-6235. 
  23. Bathgate R, Maxwell WMC, Evans G. 2006. Studies on the effect of supplementing boar semen cryopreservation media with different avian egg yolk types on in vitro post-thaw sperm quality. Reprod. Domest. Anim. 41: 68-73. 
  24. Lee J, Paik H. 2019. Anticancer and immunomodulatory activity of egg proteins and peptides: a review. Poult. Sci. 98: 6505-6516. 
  25. Lokapirnasari WP, Dewi AR, Fathinah A, Hidanah S, Harijani N, Soepranianondo K, et al. 2018. Presented at the IOP Conference Series: Earth and Environmental Science. 
  26. Mine Y. 2007. Egg proteins and peptides in human health-chemistry, bioactivity and production. Curr. Pharm. Des. 13: 875-884. 
  27. Oladipo G, Oladipo M, Ibukun E, Salawu S. 2021. Quail (Coturnix japonica) egg attenuated 2-butoxyethanol-induced enzymatic dysregulation, disseminated thrombosis and hemolytic impairment in female wistar rats. J. Ethnopharmacol. 267: 113508. 
  28. Myint SL, Kinoshita K, Shimogiri T, Ibrahim HR, Tsusaki T, Tanoue T, et al. 2012. Effect of polymorphism in egg white lysozyme on muramidase and antibacterial activities as well as hatchability in the Japanese quail (Coturnix japonica). Anim. Sci. 90: 1747-1755. 
  29. Tolik D, Poawska E, Charuta A, Nowaczewski S, Cooper R. 2014. Characteristics of egg parts, chemical composition and nutritive value of Japanese quail eggs-a review. Folia Biol. (Krakow) 62: 287-292. 
  30. Trimeche A, Anton M, Renard P, Gandemer G, Tainturier D. 1997. Quail egg yolk: a novel cryoprotectant for the freeze preservation of Poitou jackass sperm. Cryobiology 34: 385-393. 
  31. Kwak MK, Liu R, Kwon JO, Kim MK, Kim AH, Kang SO. 2013. Cyclic dipeptides from lactic acid bacteria inhibit the proliferation of influenza A virus. J. Microbiol. 51: 836-843. 
  32. De Man JC, Rogosa M, Sharpe ME. 1960. A medium for the cultivation of Lactobacilli. J. Appl. Microbiol. 23: 130-135. 
  33. Pardali E, Paramithiotis S, Papadelli M, Mataragas M, Drosinos EH. 2017. Lactic acid bacteria population dynamics during spontaneous fermentation of radish (Raphanus sativus L.) roots in brine. World J. Microbiol. Biotechnol. 33: 110. 
  34. Fonzi WA, Irwin MY. 1993. Isogenic strain construction and gene mapping in Candida albicans. Genetics 134: 717-728. 
  35. Rees RW, Flood J, Hasan Y, Cooper RM. 2007. Effects of inoculum potential, shading and soil temperature on root infection of oil palm seedlings by the basal stem rot pathogen Ganoderma boninense. Plant Pathol. 56: 862-870. 
  36. Kwak MK, Liu R, Kim MK, Moon D, Song SH, Kang SO. 2014. Cyclic dipeptides from lactic acid bacteria inhibit the proliferation of pathogenic fungi. J. Microbiol. 52: 64-70. 
  37. National Research Council. 1994. Nutrient requirements of poultry: 1994. National Academies Press. 
  38. Wiegand I, Hilpert K, Hancock REW. 2008. Agar and broth dilution methods to determine the minimal inhibitory concentration (MIC) of antimicrobial substances. Nat. Protc. 3: 163-175. 
  39. Wikler MA. 2006. Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically: approved standard, pp. Ed. Clinical and laboratory standards institute. 
  40. Mine Y, D'Silva I. 2008. Bioactive components in egg white. Egg Biosci. Biotechnol. 141-184. 
  41. Dal Bello F, Clarke CI, Ryan LAM, Ulmer H, Schober TJ, Strom K, et al. 2007. Improvement of the quality and shelf life of wheat bread by fermentation with the antifungal strain Lactobacillus plantarum FST 1.7. J. Cereal Sci. 45: 309-318. 
  42. Yan PS, 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. Appl. Environ. Microbiol. 70: 7466-7473. 
  43. Rhee KH. 2002. Isolation and characterization of Streptomyces sp. KH-614 producing anti-VRE (vancomycin-resistant enterococci) antibiotics. J. Gen. Appl. Microbiol. 48: 327-331. 
  44. 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. Appl. Environ. Microbiol. 68: 4322-4327. 
  45. Wattana-Amorn P, Charoenwongsa W, Williams C, Crump MP, 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. 
  46. Rhee KH. 2004. Cyclic dipeptides exhibit synergistic, broad spectrum antimicrobial effects and have anti-mutagenic properties. Int. J. Antimicrob. Agents 24: 423-427. 
  47. Lind H, Sjogren J, Gohil S, Kenne L, Schnurer J, Broberg A. 2007. Antifungal compounds from cultures of dairy propionibacteria type strains. FEMS Microbiol. Lett. 271: 310-315. 
  48. Huang R, Zhou X, Xu T, Yang X, Liu Y. 2010. Diketopiperazines from marine organisms. Chem. Biodivers. 7: 2809-2829. 
  49. Wang JH, Quan CS, Qi XH, Li X, Fan SD. 2010. Determination of diketopiperazines of Burkholderia cepacia CF-66 by gas chromatography-mass spectrometry. Anal. Bioanal. Chem. 396: 1773-1779. 
  50. Ishikawa K, Hosoe T, Itabashi T, Wakana D, Takizawa K, Yaguchi T, et al. 2010. Novoamauromine and ent-Cycloechinulin: two new diketopiperazine derivatives from Aspergillus novofumigatus. Chem. Pharm. Bull. 58: 717-719. 
  51. Gu Q, Fu L, Wang Y, Lin J. 2013. Identification and characterization of extracellular cyclic dipeptides as quorum-sensing signal molecules from Shewanella baltica, the specific spoilage organism of Pseudosciaena crocea during 4℃ storage. J. Agr. Food Chem. 61: 11645-11652. 
  52. Silva MMD, Andrade MDS, Bauermeister A, Merfa MV, Forim MR, Fernandes JB, et al. 2017. A Simple defined medium for the production of true diketopiperazines in Xylella fastidiosa and their identification by ultra-fast liquid chromatography-electrospray ionization ion trap mass spectrometry. Molecules 22: E985. 
  53. Mayo B, van Sinderen D, Ventura M. 2008. Genome analysis of food grade lactic acid-producing bacteria: from basics to applications. Curr. Genomics 9: 169-183. 
  54. Liu CJ, Wang R, Gong FM, Liu XF, Zheng HJ, Luo YY, et al. 2015. Complete genome sequences and comparative genome analysis of Lactobacillus plantarum strain 5-2 isolated from fermented soybean. Genomics 106: 404-411. 
  55. Yang EJ, Kim YS, Chang HC. 2011. Purification and characterization of antifungal δ-dodecalactone from Lactobacillus plantarum AF1 isolated from kimchi. J. Food Prot. 74: 651-657. 
  56. Lim SM, Im DS. 2009. Screening and characterization of probiotic lactic acid bacteria isolated from Korean fermented foods. J. Microbiol. Biotechnol. 19: 178-186. 
  57. Li H, Liu L, Zhang S, Cui W, Lv J. 2012. Identification of antifungal compounds produced by Lactobacillus casei AST18. Curr. Microbiol. 65: 156-161. 
  58. Elayaraja S, Annamalai N, Mayavu P, Balasubramanian T. 2014. Production, purification and characterization of bacteriocin from Lactobacillus murinus AU06 and its broad antibacterial spectrum. Asian Pac. J. Trop. Biomed. 4(Suppl 1): S305-S311. 
  59. Singh AK, Mukherjee S, Adhikari MD, Ramesh A. 2012. Fluorescence-based comparative evaluation of bactericidal potency and food application potential of anti-listerial bacteriocin produced by lactic acid bacteria isolated from indigenous samples. Probiot. Antimicrob. Proteins 4: 122-132. 
  60. Devi SM, Halami PM. 2011. Detection and characterization of pediocin PA-1/AcH like bacteriocin producing lactic acid bacteria. Curr. Microbiol. 63: 181-185. 
  61. Rodger A, Sanders K. 2010. Biomacromolecular applications of UV-visible absorption spectroscopy, pp. 166-173. Encyclopedia of Spectroscopy and Spectrometry, Ed. Elsevier, 
  62. Mahoney WC, Hermodson MA. 1980. Separation of large denatured peptides by reverse phase high performance liquid chromatography. Trifluoroacetic acid as a peptide solvent. J. Biol. Chem. 255: 11199-11203. 
  63. Whitaker JR, Granum PE. 1980. An absolute method for protein determination based on difference in absorbance at 235 and 280 nm. Anal. Biochem. 109: 156-159. 
  64. Cleaves H, Aubrey A, Bada J. 2009. An evaluation of the critical parameters for abiotic peptide synthesis in submarine hydrothermal systems. Orig. Life Evol. Biosph. 39: 109-126. 
  65. Sweeney JA, Hennessey Jr JP. 2002. Evaluation of accuracy and precision of adenovirus absorptivity at 260 nm under conditions of complete DNA disruption. Virology 295: 284-288. 
  66. Antosiewicz JM, Shugar D. 2016. UV-Vis spectroscopy of tyrosine side-groups in studies of protein structure. Part 2: Selected applications. Biophys. Rev. 8: 163-177. 
  67. Sharma V, Sharma N, Sheikh I, Kumar V, Sehrawat N, Yadav M, et al. 2021. Probiotics and prebiotics having broad spectrum anticancer therapeutic potential: recent trends and future perspectives. Curr. Pharmacol. Rep. 7: 67-79. 
  68. McConnell JS, McConnell RM, Hossner LR. 1993. Ultraviolet spectra of acetic acid, glycine, and glyphosate. J. Arkansas Acad. Sci. 47: 73-76. 
  69. Willard M, Cowan WM, Vagelos PR. 1974. The polypeptide composition of intra-axonally transported proteins: evidence for four transport velocities. Proc. Natl. Acad. Sci. USA 71: 2183-2187. 
  70. 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. J. Org. Chem. 73: 9158-9160. 
  71. Karanam G, Arumugam MK. 2020. Reactive oxygen species generation and mitochondrial dysfunction for the initiation of apoptotic cell death in human hepatocellular carcinoma HepG2 cells by a cyclic dipeptide Cyclo (-Pro-Tyr). Mol. Biol. Rep. 47: 3347- 3359. 
  72. Nishanth SK, Nambisan B, Dileep C. 2014. Three bioactive cyclic dipeptides from the Bacillus sp. N strain associated with entomopathogenic nematode. Peptides 53: 59-69.