Class III bacteriocin Helveticin-M causes sublethal damage on target cells through impairment of cell wall and membrane

Journal of Industrial Microbiology and Biotechnology

Volumn 45, Issue 3, 2018, Pages 213-227

  Sun, Zhilan ^a   Wang, Xiaomeng ^a   Zhang, Xinxiao ^a   Wu, Haihong ^a   Zou, Ye ^a   Li, Pengpeng ^a   Sun, Chong ^a   Xu, Weimin ^a,b   Liu, Fang ^a   Wang, Daoying ^a  

^a INSTITUTE OF PLANT PROTECTION   (China)

^b Quality and Safety Control   (China)

Author keywords

Bacteriocin; Cytoplasmic membrane; Helveticin M; Lactobacillus crispatus; Sublethal damage

Indexed keywords

ADENOSINE TRIPHOSPHATE; ANTIBIOTIC AGENT; BACTERIOCIN; HELVETICIN M; NITRILOTRIACETIC ACID; UNCLASSIFIED DRUG; ANTIINFECTIVE AGENT;

ARTICLE; BACTERICIDAL ACTIVITY; CELL DAMAGE; CELL MEMBRANE; CELL MEMBRANE DEPOLARIZATION; CELL MEMBRANE PERMEABILITY; CELL POPULATION; CELL WALL; CONFOCAL LASER SCANNING MICROSCOPY; DRUG MECHANISM; ENTEROBACTER CLOACAE; ESCHERICHIA COLI; INNER MEMBRANE; LACTOBACILLUS CRISPATUS; MEMBRANE POTENTIAL; NONHUMAN; OUTER MEMBRANE; SCANNING ELECTRON MICROSCOPY; SEQUENCE ALIGNMENT; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS SAPROPHYTICUS; STRUCTURE ANALYSIS; TARGET CELL; TRANSMISSION ELECTRON MICROSCOPY; BIOLOGY; CYTOPLASM; DRUG EFFECT; GRAM NEGATIVE BACTERIUM; GRAM POSITIVE BACTERIUM; METABOLISM; MICROBIAL SENSITIVITY TEST; MOLECULAR CLONING;

ANTI-BACTERIAL AGENTS; BACTERIOCINS; CELL MEMBRANE; CELL MEMBRANE PERMEABILITY; CELL WALL; CLONING, MOLECULAR; COMPUTATIONAL BIOLOGY; CYTOPLASM; ENTEROBACTER CLOACAE; ESCHERICHIA COLI; GRAM-NEGATIVE BACTERIA; GRAM-POSITIVE BACTERIA; LACTOBACILLUS CRISPATUS; MICROBIAL SENSITIVITY TESTS; MICROSCOPY, ELECTRON, SCANNING; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS SAPROPHYTICUS;

EID: 85040774412     PISSN: 13675435     EISSN: 14765535     Source Type: Journal    
DOI: 10.1007/s10295-018-2008-6     Document Type: Article

References (45)

1. Agcam E, Akyildiz A, Akdemir EG (2014) Comparison of phenolic compounds of orange juice processed by pulsed electric fields (PEF) and conventional thermal pasteurisation. Food Chem 143:354–361. doi:10.1016/j.foodchem.2013.07.115
2. Baneyx F, Mujacic M (2004) Recombinant protein folding and misfolding in Escherichia coli. Nat Biotechnol 22:1399–1408
3. Chen B, Fan DQ, Zhu KX, Shan ZG, Chen FY, Hou L, Cai L, Wang KJ (2015) Mechanism study on a new antimicrobial peptide Sphistin derived from the N-terminus of crab histone H2A identified in haemolymphs of Scylla paramamosain. Fish Shellfish Immunol 47:833–846. doi:10.1016/j.fsi.2015.10.010
4. Chopra L, Singh G, Kumar JK, Sahoo DK (2015) Sonorensin: a new bacteriocin with potential of an anti-biofilm agent and a food biopreservative. Sci Rep 5:13412. doi:10.1038/srep13412
5. Cleveland J, Montville TJ, Nes IF, Chikindas ML (2001) Bacteriocins: safe, natural antimicrobials for food preservation. Int J Food Microbiol 71:1–20
6. Cotter PD, Ross RP, Hill C (2013) Bacteriocins—a viable alternative to antibiotics? Nat Rev Microbiol 11:95–105. doi:10.1038/nrmicro2937
7. Eijsink VG, Axelsson L, Diep DB, Havarstein LS, Holo H, Nes IF (2002) Production of class II bacteriocins by lactic acid bacteria; an example of biological warfare and communication. Antonie Van Leeuwenhoek 81:639–654
8. Gharsallaoui A, Oulahal N, Joly C, Degraeve P (2016) Nisin as a food preservative: part 1: physicochemical properties, antimicrobial activity, and main uses. Crit Rev Food Sci Nutr 56:1262–1274. doi:10.1080/10408398.2013.763765
9. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp 41:95–98
10. Hoffmann M, Luo Y, Monday SR, Gonzalez-Escalona N, Ottesen AR, Muruvanda T, Wang C, Kastanis G, Keys C, Janies D, Senturk IF, Catalyurek UV, Wang H, Hammack TS, Wolfgang WJ, Schoonmaker-Bopp D, Chu A, Myers R, Haendiges J, Evans PS, Meng J, Strain EA, Allard MW, Brown EW (2016) Tracing Origins of the Salmonella bareilly strain causing a food-borne outbreak in the United States. J Infect Dis 213:502–508. doi:10.1093/infdis/jiv297
11. Hultman J, Rahkila R, Ali J, Rousu J, Bjorkroth KJ (2015) Meat processing plant microbiome and contamination patterns of cold-tolerant bacteria causing food safety and spoilage risks in the manufacture of vacuum-packaged cooked sausages. Appl Environ Microbiol 81:7088–7097. doi:10.1128/AEM.02228-15
12. Hurdle JG, O’Neill AJ, Chopra I, Lee RE (2010) Targeting bacterial membrane function: an underexploited mechanism for treating persistent infections. Nat Rev Microbiol 9:62
13. Joerger MC, Klaenhammer TR (1990) Cloning, expression, and nucleotide sequence of the Lactobacillus helveticus 481 gene encoding the bacteriocin helveticin. J Bacteriol 172:6339–6347
14. Kadariya J, Smith TC, Thapaliya D (2014) Staphylococcus aureus and staphylococcal food-borne disease: an ongoing challenge in public health. Biomed Res Int 2014:827965. doi:10.1155/2014/827965
15. Lavieri NA, Sebranek JG, Cordray JC, Dickson JS, Horsch AM, Jung S, Manu DK, Mendonça AF, Stecher BB (2015) Control of Listeria monocytogenes on alternatively cured ready-to-eat ham using natural antimicrobial ingredients in combination with post-lethality interventions. Food Process Technol 6:10
16. Lazdunski CJ (1995) Colicin import and pore formation: a system for studying protein transport across membranes? Mol Microbiol 16:1059–1066
17. Lee H, Kim HY (2011) Lantibiotics, class I bacteriocins from the genus Bacillus. J Microbiol Biotechnol 21:229–235
18. Li J, Ahn J, Liu D, Chen S, Ye X, Ding T (2016) Evaluation of ultrasound-induced damage to Escherichia coli and Staphylococcus aureus by flow cytometry and transmission electron microscopy. Appl Environ Microbiol 82:1828–1837. doi:10.1128/AEM.03080-15
19. Liu G, Song Z, Yang X, Gao Y, Wang C, Sun B (2016) Antibacterial mechanism of bifidocin A, a novel broad-spectrum bacteriocin produced by Bifidobacterium animalis BB04. Food Control 62:309–316
20. Liu YG, Chen Y (2007) High-efficiency thermal asymmetric interlaced PCR for amplification of unknown flanking sequences. Biotechniques 43:649–650, 652, 654
21. Lou M, Zhu B, Muhammad I, Li B, Xie G, Wang Y, Li H, Sun G (2011) Antibacterial activity and mechanism of action of chitosan solutions against apricot fruit rot pathogen Burkholderia seminalis. Carbohyd Res 346:1294–1301. doi:10.1016/j.carres.2011.04.042
22. Lou MM, Zhu B, Muhammad I, Li B, Xie GL, Wang YL, Li HY, Sun GC (2011) Antibacterial activity and mechanism of action of chitosan solutions against apricot fruit rot pathogen Burkholderia seminalis. Carbohydr Res 346:1294–1301. doi:10.1016/j.carres.2011.04.042
23. Mercer RG, Walker BD, Yang X, McMullen LM, Ganzle MG (2017) The locus of heat resistance (LHR) mediates heat resistance in Salmonella enterica, Escherichia coli and Enterobacter cloacae. Food Microbiol 64:96–103. doi:10.1016/j.fm.2016.12.018
24. Moll GN, Konings WN, Driessen AJ (1999) Bacteriocins: mechanism of membrane insertion and pore formation. Antonie Van Leeuwenhoek 76:185–198
25. NicAogain K, O’Byrne CP (2016) The role of stress and stress adaptations in determining the fate of the bacterial pathogen Listeria monocytogenes in the food chain. Front Microbiol 7:1865. doi:10.3389/fmicb.2016.01865
26. Nigutova K, Serencova L, Piknova M, Javorsky P, Pristas P (2008) Heterologous expression of functionally active enterolysin A, class III bacteriocin from Enterococcus faecalis, in Escherichia coli. Protein Expr Purif 60:20–24. doi:10.1016/j.pep.2008.03.006
27. Nilsen T, Nes IF, Holo H (2003) Enterolysin A, a cell wall-degrading bacteriocin from Enterococcus faecalis LMG 2333. Appl Environ Microbiol 69:2975–2984
28. Oppegard C, Rogne P, Emanuelsen L, Kristiansen PE, Fimland G, Nissen-Meyer J (2007) The two-peptide class II bacteriocins: structure, production, and mode of action. J Mol Microbiol Biotechnol 13:210–219. doi:10.1159/000104750
29. 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. doi:10.1080/10408398.2016.1277972
30. Padmavathy N, Vijayaraghavan R (2008) Enhanced bioactivity of ZnO nanoparticles-an antimicrobial study. Sci Technol Adv Mater 9:35004. doi:10.1088/1468-6996/9/3/035004
31. Pillet F, Formosa-Dague C, Baaziz H, Dague E, Rols MP (2016) Cell wall as a target for bacteria inactivation by pulsed electric fields. Sci Rep 6:19778. doi:10.1038/srep19778
32. Riley MA (1993) Molecular mechanisms of colicin evolution. Mol Biol Evol 10:1380–1395
33. Schenk M, Raffellini S, Guerrero S, Blanco GA, Alzamora SM (2011) Inactivation of Escherichia coli, Listeria innocua and Saccharomyces cerevisiae by UV-C light: study of cell injury by flow cytometry. Lebensmittel-Wissenschaft und-Technologie 44:191–198
34. Sun Z, Kong J, Hu S, Kong W, Lu W, Liu W (2013) Characterization of a S-layer protein from Lactobacillus crispatus K313 and the domains responsible for binding to cell wall and adherence to collagen. Appl Microbiol Biotechnol 97:1941–1952. doi:10.1007/s00253-012-4044-x
35. Sung SY, Sin LT, Tee TT, Bee ST, Rahmat AR, Rahman WAWA, Tan AC, Vikhraman M (2013) Antimicrobial agents for food packaging applications. Trends Food Sci Tech 33:110–123
36. Hp T, Oppedijk SF, Breukink E, Martin NI (2016) New insights into Nisin’s antibacterial mechanism revealed by binding studies with synthetic lipid II analogues. Biochemistry-Us 55:232–237. doi:10.1021/acs.biochem.5b01173
37. Thompson JD, Gibson TJ, Higgins DG (2002) Multiple sequence alignment using ClustalW and ClustalX. Curr Protoc Bioinform Chapter 2:2–3. doi:10.1002/0471250953.bi0203s00
38. Thompson JK, Collins MA, Mercer WD (1996) Characterization of a proteinaceous antimicrobial produced by Lactobacillus helveticus CNRZ450. J Appl Bacteriol 80:338–348
39. Tsiraki MI, Savvaidis IN (2016) The effects of citrus extract (Citrox(c)) on the naturally occurring microflora and inoculated pathogens, Bacillus cereus and Salmonella enterica, in a model food system and the traditional Greek yogurt-based salad Tzatziki. Food Microbiol 53:150–155. doi:10.1016/j.fm.2015.09.015
40. Vaara M (1992) Agents that increase the permeability of the outer membrane. Microbiol Rev 56:395
41. Woraprayote W, Malila Y, Sorapukdee S, Swetwiwathana A, Benjakul S, Visessanguan W (2016) Bacteriocins from lactic acid bacteria and their applications in meat and meat products. Meat Sci 120:118–132. doi:10.1016/j.meatsci.2016.04.004
42. Zhang M, Wang D, Geng Z, Li P, Sun Z, Xu W (2018) Effect of heat shock protein 90 against ROS-induced phospholipid oxidation. Food Chem 240:642–647. doi:10.1016/j.foodchem.2017.08.005
43. Zhang T, Pan Y, Li B, Ou J, Zhang J, Chen Y, Peng X, Chen L (2013) Molecular cloning and antimicrobial activity of enterolysin A and helveticin J of bacteriolysins from metagenome of Chinese traditional fermented foods. Food Control 31:499–507
44. Zhao W, Yang R, Zhang HQ, Zhang W, Hua X, Tang Y (2011) Quantitative and real time detection of pulsed electric field induced damage on Escherichia coli cells and sublethally injured microbial cells using flow cytometry in combination with fluorescent techniques. Food Control 22:566–573
45. Zou Y, Bian H, Li P, Sun Z, Sun C, Zhang M, Geng Z, Xu W, Wang D (2017) Optimization and physicochemical properties of nutritional protein isolate from pork liver with ultrasound-assisted alkaline extraction. Anim Sci J. doi:10.1111/asj.12930