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Isolation and Characterization of an Anti-listerial Bacteriocin from Leuconostoc lactis SD501

  • Hwang, In-Chan (Department of Animal Resource Science, Dankook University) ;
  • Oh, Ju Kyoung (Department of Animal Resource Science, Dankook University) ;
  • Kim, Sang Hoon (Department of Animal Resource Science, Dankook University) ;
  • Oh, Sejong (Department of Animal Science, Chonnam National University) ;
  • Kang, Dae-Kyung (Department of Animal Resource Science, Dankook University)
  • Received : 2018.05.17
  • Accepted : 2018.08.09
  • Published : 2018.10.31

Abstract

Although bacteriocins with anti-listerial activity have been isolated from a wide variety of lactic acid bacteria, little is known about those from Leuconostoc lactis, a heterofermentative bacterium that produces diacetyl and exopolysaccharides in dairy foods. In this study, an anti-listerial bacteriocin was isolated from Leuc. lactis SD501 and characterized. It was particularly potent against Listeria monocytogenes and also inhibited Enterococcus faecalis. Anti-listerial activity reached a maximum during the early stationary phase and then decreased gradually. The anti-listerial substance was sensitive to proteinase K and ${\alpha}$-chymotrypsin, confirming its proteinaceous nature. Its activity remained stable at pH values ranging from 1 to 10. In addition, it was strongly resistant to high temperatures, retaining its activity even after incubation for 15 min at $121^{\circ}C$. The apparent molecular mass of the partially purified anti-listerial bacteriocin was approximately 7 kDa. The characteristics of the SD501 bacteriocin, including its small molecular size (<10 kDa), strong anti-listerial activity, wide pH stability and good thermostability, indicate its classification as a Class IIa bacteriocin.

Keywords

References

  1. Abriouel H, Valdivia E, Galvez A, Maqueda M. 2001. Influence of physico-chemical factors on the oligomerization and biological activity of bacteriocin AS-48. Curr Microbiol 42:89-95.
  2. Alvarez-Cisneros YM, Fernandez FJ, Wacher-Rodarte C, Aguilar MB, Sainz Espunes Tdel R, Ponce-Alquicira E. 2010. Biochemical characterization of a bacteriocin-like inhibitory substance produced by Enterococcus faecium MXVK29, isolated from Mexican traditional sausage. J Sci Food Agric 90:2475-2481. https://doi.org/10.1002/jsfa.4109
  3. Alvarez-Sieiro P, Montalban-Lopez M, Mu D, Kuipers OP. 2016. Bacteriocins of lactic acid bacteria: Extending the family. Appl Microbiol Biotechnol 100:2939-2951. https://doi.org/10.1007/s00253-016-7343-9
  4. Arakawa K, Yoshida S, Aikawa H, Hano C, Bolormaa T, Burenjargal S, Miyamoto T. 2016. Production of a bacteriocin-like inhibitory substance by Leuconostoc mesenteroides subsp. dextranicum 213M0 isolated from Mongolian fermented mare milk, airag. Anim Sci J 87:449-456. https://doi.org/10.1111/asj.12445
  5. Balay DR, Dangeti RV, Kaur K, McMullen LM. 2017. Purification of leucocin A for use on wieners to inhibit Listeria monocytogenes in the presence of spoilage organisms. Int J Food Microbiol 255:25-31. https://doi.org/10.1016/j.ijfoodmicro.2017.05.016
  6. Balciunasa EM, Martineza FAC, Todorovb SD, de Melo Francob BDG, de Souza Oliveira ACRP. 2013. Novel biotechnological applications of bacteriocins: A review. Food Control 32:134-142. https://doi.org/10.1016/j.foodcont.2012.11.025
  7. Barmpalia IM, Koutsoumanis KP, Geornaras I, Belk KE, Scanga JA, Kendall PA, Smith GC, Sofos JN. 2005. Effect of antimicrobials as ingredients of pork bologna for Listeria monocytogenes control during storage at 4 or $10^{\circ}C$. Food Microbiol 22:205-211. https://doi.org/10.1016/j.fm.2004.08.003
  8. Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254. https://doi.org/10.1016/0003-2697(76)90527-3
  9. Byelashov OA, Kendall PA, Belk KE, Scanga JA, Sofos JN. 2008. Control of Listeria monocytogenes on vacuum-packaged frankfurters sprayed with lactic acid alone or in combination with sodium lauryl sulfate. J Food Prot 71:728-734. https://doi.org/10.4315/0362-028X-71.4.728
  10. Chen YS, Wu HC, Kuo CY, Chen YW, Ho S, Yanagida F. 2018. Leucocin C-607, a novel bacteriocin from the multiplebacteriocin- producing Leuconostoc pseudomesenteroides 607 isolated from persimmon. Probiotics Antimicrob Proteins 10:148-156. https://doi.org/10.1007/s12602-017-9359-6
  11. Chumchalova J, Josephsen J, Plockova M. 1995. Characterization of acidocin CH5, a saccharolytic sensitive bacteriocin of Lactobacillus acidophilus CH5. Chem Mikrobiol Techonl Lebensm 17:145-150.
  12. Cholakov R, Tumbarski Y, Yanakieva V, Dobrev I, Salim Y, Denkova Z. 2017. Antimicrobial activity of Leuconostoc lactis strain BT17, isolated from a spontaneously fermented cereal beverage (Boza). J Microbiol Biotechnol Food Sci 7:47-49. https://doi.org/10.15414/jmbfs.2017.7.1.47-49
  13. Felix JV, Papathanasopoulos MA, Smith AA, von Holy A, Hastings JW. 1994. Characterization of leucocin B-Ta11a: A bacteriocin from Leuconostoc carnosum Ta11a isolated from meat. Curr Microbiol 29:207-212. https://doi.org/10.1007/BF01570155
  14. Feng G, Guron GK, Churey JJ, Worobo RW. 2009. Characterization of mundticin L, a class IIa anti-Listeria bacteriocin from Enterococcus mundtii CUGF08. Appl Environ Microbiol 75:5708-5713. https://doi.org/10.1128/AEM.00752-09
  15. Ghalfi H, Kouakou P, Duroy M, Daoudi A, Benkerroum N, Thonart P. 2006. Antilisterial bacteriocin-producing strain of Lactobacillus curvatus CWBI-B28 as a preservative culture in bacon meat and influence of fat and nitrites on bacteriocins production and activity. Food Sci Technol Int 12:325-333. https://doi.org/10.1177/1082013206067380
  16. Halimi B, Dortu C, Arguelles-Arias A, Thonart P, Joris B, Fickers P. 2010. Antilisterial activity on poultry meat of amylolysin, a bacteriocin from Bacillus amyloliquefaciens GA1. Probiotics Antimicrob Proteins 2:120-125. https://doi.org/10.1007/s12602-010-9040-9
  17. Han KS, Kim Y, Kim SH, Oh S. 2007. Characterization and purification of acidocin 1B, a bacteriocin produced by Lactobacillus acidophilus GP1B. J Microbiol Biotechnol 17:774-783.
  18. Heng NC, Burtenshaw GA, Jack RW, Tagg JR. 2007. Ubericin A, a class IIa bacteriocin produced by Streptococcus uberis. Appl Environ Microbiol 73:7763-7766. https://doi.org/10.1128/AEM.01818-07
  19. Kanatani K, Oshimura M, Sano K. 1995. Isolation and characterization of acidocin A and cloning of the bacteriocin gene from Lactobacillus acidophilus. Appl Environ Microbiol 61:1061-1067.
  20. Kim S, Lee H, Lee S, Yoon Y, Choi KH. 2015. Antimicrobial action of oleanolic acid on Listeria monocytogenes, Enterococcus faecium, and Enterococcus faecalis. PLoS One 10: e0118800. https://doi.org/10.1371/journal.pone.0118800
  21. Koch J, Dworak R, Prager R, Becker B, Brockmann S, Wicke A, Wichmann-Schauer H, Hof H, Werber D, Stark K. 2010. Large listeriosis outbreak linked to cheese made from pasteurized milk, Germany, 2006-2007. Foodborne Pathog Dis 7:1581-1584. https://doi.org/10.1089/fpd.2010.0631
  22. Larsen AG, Vogensen FK, Josephsen J. 1993. Antimicrobial activity of lactic acid bacteria isolated from sour doughs: Purification and characterization of bavaricin A, a bacteriocin produced by Lactobacillus bavaricus MI401. J Appl Bacteriol 75:113-122. https://doi.org/10.1111/j.1365-2672.1993.tb02755.x
  23. Latorre AA, Van Kessel JS, Karns JS, Zurakowski MJ, Pradhan AK, Boor KJ, Jayarao BM, Houser BA, Daugherty CS, Schukken YH. 2010. Biofilm in milking equipment on a dairy farm as a potential source of bulk tank milk contamination with Listeria monocytogenes. J Dairy Sci 93:2792-2802. https://doi.org/10.3168/jds.2009-2717
  24. Lecompte JY, Kondjoyan A, Sarter S, Portanguen S, Collignan A. 2008. Effects of steam and lactic acid treatments on inactivation of Listeria innocua surface-inoculated on chicken skins. Int J Food Microbiol 127:155-161. https://doi.org/10.1016/j.ijfoodmicro.2008.06.033
  25. Lee J, Gwak E, Lee H, Ha J, Lee S, Kim S, Oh MH, Park BY, Choi KH, Yoon Y. 2017. Effects of low $NaNO_{2}$ and NaCl concentrations on Listeria monocytogenes growth in emulsion-type sausage. Asian-Australas J Anim Sci 30:432-438.
  26. Lim KB, Balolong MP, Kim SH, Oh JK, Lee JY, Kang DK. 2016. Isolation and characterization of a broad spectrum bacteriocin from Bacillus amyloliquefaciens RX7. Biomed Res Int 2016:8521476.
  27. Low JC, Donachie W. 1997. A review of Listeria monocytogenes and listeriosis. Vet J 153:9-29. https://doi.org/10.1016/S1090-0233(97)80005-6
  28. Makhloufi KM, Carre-Mlouka A, Peduzzi J, Lombard C, van Reenen CA, Dicks LM, Rebuffat S. 2013. Characterization of leucocin B-KM432Bz from Leuconostoc pseudomesenteroides isolated from boza, and comparison of its efficiency to pediocin PA-1. PLoS One 8:e70484. https://doi.org/10.1371/journal.pone.0070484
  29. Marques JL, Funck GD, Dannenberg GDS, Cruxen CEDS, Halal SLME, Dias ARG, Fiorentini AM, Silva WPD. 2017. Bacteriocin-like substances of Lactobacillus curvatus P99: Characterization and application in biodegradable films for control of Listeria monocytogenes in cheese. Food Microbiol 63:159-163. https://doi.org/10.1016/j.fm.2016.11.008
  30. Massa S, Cesaroni D, Poda G, Trovatelli LD. 1990. The incidence of Listeria spp. in soft cheeses, butter and raw milk in the province of Bologna. J Appl Bacteriol 68:153-156. https://doi.org/10.1111/j.1365-2672.1990.tb02560.x
  31. Mathur H, Field D, Rea MC, Cotter PD, Hill C, Ross RP. 2017. Bacteriocin-antimicrobial synergy: A medical and food perspective. Front Microbiol 8:1205. https://doi.org/10.3389/fmicb.2017.01205
  32. Meyer-Broseta S, Diot A, Bastian S, Riviere J, Cerf O. 2003. Estimation of low bacterial concentration: Listeria monocytogenes in raw milk. Int J Food Microbiol 80:1-15. https://doi.org/10.1016/S0168-1605(02)00117-4
  33. Pak SI, Spahr U, Jemmi T, Salman MD. 2002. Risk factors for L. monocytogenes contamination of dairy products in Switzerland, 1990-1999. Prev Vet Med 53:55-65. https://doi.org/10.1016/S0167-5877(01)00274-4
  34. Papagianni M, Papamichae EM. 2011. Purification, amino acid sequence and characterization of the class IIa bacteriocin weissellin A, produced by Weissella paramesenteroides DX. Bioresour Technol 102:6730-6734. https://doi.org/10.1016/j.biortech.2011.03.106
  35. Pavlova SI, Kilic AO, Kilic SS, So JS, Nader-Macias ME, Simoes JA, Tao L. 2002. Genetic diversity of vaginal lactobacilli from women in different countries based on 16S rRNA gene sequences. J Appl Microbiol 92:451-459. https://doi.org/10.1046/j.1365-2672.2002.01547.x
  36. Pintado CMBS, Oliveirab A, Pampulhab ME, Ferreira MASS. 2005. Prevalence and characterization of Listeria monocytogenes isolated from soft cheese. Food Microbiol 22: 79-85. https://doi.org/10.1016/j.fm.2004.04.004
  37. Porto MC, Kuniyoshi TM, Azevedo PO, Vitolo M, Oliveira RP. 2017. Pediococcus spp.: An important genus of lactic acid bacteria and pediocin producers. Biotechnol Adv 35:361-374. https://doi.org/10.1016/j.biotechadv.2017.03.004
  38. Ryser ET, Arimi SM, Bunduki MM, Donnelly CW. 1996. Recovery of different Listeria ribotypes from naturally contaminated, raw refrigerated meat and poultry products with two primary enrichment media. Appl Environ Microbiol 62:1781-1787.
  39. Saravanan C, Shetty PK. 2016. Isolation and characterization of exopolysaccharide from Leuconostoc lactis KC117496 isolated from idli batter. Int J Biol Macromol 90:100-106. https://doi.org/10.1016/j.ijbiomac.2015.02.007
  40. Schagger H, von Jagow G. 1987. Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal Biochem 166:368-379. https://doi.org/10.1016/0003-2697(87)90587-2
  41. Schuppler M, Loessner MJ. 2010. The opportunistic pathogen Listeria monocytogenes: Pathogenicity and interaction with the mucosal immune system. Int J Inflam 2010:704321.
  42. Seo SH, Jung M, Kim WJ. 2014. Antilisterial and amylase-sensitive bacteriocin producing Enterococcus faecium SH01 from Mukeunji, a Korean over-ripened Kimchi. Food Sci Biotechnol 23:1177-1184. https://doi.org/10.1007/s10068-014-0161-x
  43. Simon L, Fremaux C, Cenatiempo Y, Berjeaud JM. 2002. Sakacin G, a new type of antilisterial bacteriocin. Appl Environ Microbiol 68:6416-6420. https://doi.org/10.1128/AEM.68.12.6416-6420.2002
  44. Todorov SD, Dicks LM. 2004. Characterization of mesentericin ST99, a bacteriocin produced by Leuconostoc mesenteroides subsp. dextranicum ST99 isolated from boza. J Ind Microbiol Biotechnol 31:323-329. https://doi.org/10.1007/s10295-004-0153-6
  45. Tuncer Y, Ozden B. 2010. Partial biochemical characterization of nisin-like bacteriocin produced by Lactococcus lactis subsp. lactis YBD11 isolated from boza, a traditional fermented Turkish beverage. Rom Biotechnol Lett 15:4940-4948.
  46. Wulijideligen, Asahina T, Hara K, Arakawa K, Nakano H, Miyamoto T. 2012. Production of bacteriocin by Leuconostoc mesenteroides 406 isolated from Mongolian fermented mare's milk, airag. Anim Sci J 83:704-711. https://doi.org/10.1111/j.1740-0929.2012.01010.x
  47. Xiraphi N, Georgalaki M, Driessche GV, Devreese B, Beeumen JV, Tsakalidou E, Metaxopoulos J, Drosinos EH. 2006. Purification and characterization of curvaticin L442, a bacteriocin produced by Lactobacillus curvatus L442. Antonie Van Leeuwenhoek 89:19-26. https://doi.org/10.1007/s10482-005-9004-3
  48. Yehia HM, Ghanem S, Elobeid T, Mosilhey SH, Savvaidis IN. 2017. In vitro characterization of a vancomycin-resistant strain of Leuconostoc lactis isolated from chicken carcasses and its activity against some foodborne pathogens. African J Food Sci 11:337-345. https://doi.org/10.5897/AJFS2017.1627
  49. Yoon Y, Kendall PA, Belk KE, Scanga JA, Smith GC, Sofos JN. 2009. Modeling the growth/no-growth boundaries of postprocessing Listeria monocytogenes contamination on frankfurters and bologna treated with lactic acid. Appl Environ Microbiol 75:353-358. https://doi.org/10.1128/AEM.00640-08
  50. Zamfir M, Stefan IR, Stancu MM, Grosu-Tudor SS. 2016. Production, mode of action and sequencing of the corresponding gene of a bacteriocin produced by Lactococcus lactis 19.3. Int J Food Sci Technol 51:2164-2170. https://doi.org/10.1111/ijfs.13196

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