Antimicrobial potential of bacteriocins: in therapy, agriculture and food preservation

International Journal of Antimicrobial Agents

Volumn 49, Issue 1, 2017, Pages 1-11

  Ahmad, Varish ^a   Khan, Mohd Sajid ^a   Jamal, Qazi Mohammad Sajid ^b   Alzohairy, Mohammad A ^c   Al Karaawi, Mohammad A ^b   Siddiqui, Mughees Uddin ^b  

^a INTEGRAL UNIVERSITY   (India)

^b Buraydah Private Colleges   (Saudi Arabia)

^c QASSIM UNIVERSITY   (Saudi Arabia)

Author keywords

Antimicrobial; Bacteriocin; Diagnostic; Preservation

Indexed keywords

AMOXICILLIN; AMPICILLIN; BACTERIOCIN; BETA LACTAM ANTIBIOTIC; CEFOTAXIME; CEFTRIAXONE; CLINDAMYCIN PHOSPHATE; COLICIN A; COLISTIN; EDETIC ACID; FOOD ADDITIVE; LACTICIN 3147; METRONIDAZOLE; NISIN; NISIN Z; PEDIOCIN; PENICILLIN DERIVATIVE; POLYLYSINE; POLYMYXIN B; RIFAMPICIN; STREPTOMYCIN; SUBTILOSIN A; TETRACYCLINE; THYMOL; UNCLASSIFIED DRUG; ANTIINFECTIVE AGENT;

AGRICULTURE; ANTIMICROBIAL THERAPY; BACILLUS SUBTILIS; BACTERIAL CELL WALL; BACTERICIDAL ACTIVITY; BIOLOGICAL CONTROL AGENT; BIOSYNTHESIS; CRONOBACTER; DRUG POTENTIATION; ESCHERICHIA COLI; FOOD PRESERVATION; GENETIC ENGINEERING; GRAM NEGATIVE BACTERIUM; GRAM POSITIVE BACTERIUM; HOSPITAL INFECTION; HUMAN; LACTIC ACID BACTERIUM; LISTERIA MONOCYTOGENES; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; MICROORGANISM DETECTION; MINIMUM INHIBITORY CONCENTRATION; MULTIDRUG RESISTANCE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; PROTON MOTIVE FORCE; RESPIRATORY TRACT INFECTION; REVIEW; SEA FOOD; SKIN DISEASE; TOOTH INFECTION; VAGINITIS; VANCOMYCIN RESISTANT ENTEROCOCCUS; VETERINARY MEDICINE; ANIMAL; BACTERIAL INFECTIONS; METABOLISM; PROCEDURES; VETERINARY;

AGRICULTURE; ANIMALS; ANTI-BACTERIAL AGENTS; BACTERIAL INFECTIONS; BACTERIOCINS; FOOD PRESERVATION; HUMANS;

EID: 85006987266     PISSN: 09248579     EISSN: 18727913     Source Type: Journal    
DOI: 10.1016/j.ijantimicag.2016.08.016     Document Type: Review

References (178)

1. [1] Szkaradkiewicz, A.K., Karpinski, T.M., Probiotics and probiotics. J Biol Earth Sci 3 (2013), 42–47.
2. [2] Klaenhammer, T.R., Bacteriocins of lactic acid bacteria. Biochimie 70 (1988), 337–349.
3. [3] Desriac, F., Defer, D., Bourgougnon, N., Brillet, B., Le Chevalier, P., Fleury, Y., Bacteriocin as weapons in the marine animal-associated bacteria warfare: inventory and potential applications as an aquaculture probiotic. Mar Drugs 8 (2010), 1153–1177.
4. [4] Cintas, L.M., Casaus, M.P., Herranz, C., Nes, I.F., Hernández, P.E., Review: bacteriocins of lactic acid bacteria. Food Sci Technol Int 7 (2001), 281–305.
5. [5] Nagao, J.C., Properties and applications of lantibiotics, a class of bacteriocin produced by Gram positive bacteria. J Oral Biosci 51 (2009), 158–164.
6. [6] Cotter, P.D., Ross, R.P., Hill, C., Bacteriocins—a viable alternative to antibiotics. Nat Rev Microbiol 11 (2013), 95–105.
7. [7] Ray, B., Hoover, D.G., Pediocins. Hoover, D.G., Steenson, L.R., (eds.) Bacteriocins of lactic acid bacteria, 1993, Academic Press, Millbrae (CA), 181–206.
8. [8] Rea, M.C., Clayton, E., O'Connor, P.M., Shanahan, F., Kiely, B., Ross, R.P., et al. Antimicrobial activity of lacticin 3147 against clinical Clostridium difficile strains. J Med Microbiol 56 (2007), 940–946.
9. [9] Piper, C., Draper, L.A., Cotter, P.D., Ross, R.P., Hill, C., A comparison of the activities of lacticin 3147 and nisin against drug-resistant Staphylococcus aureus and Enterococcus species. J Antimicrob Chemother 64 (2009), 546–551.
10. [10] Piper, C., Hill, C., Cotter, P.D., Ross, R.P., Bioengineering of a nisin A-producing Lactococcus lactis to create isogenic strains producing the natural variants nisin F, Q and Z. Microb Biotechnol 4 (2011), 375–382.
11. [11] Mandell, L.A., Wunderink, R.G., Anzueto, A., Bartlett, J.G., Campbell, G.D., Dean, N.C., et al. Infectious Diseases Society of America/American Thoracic Society consensus guidelines on the management of community-acquired pneumonia in adults. Clin Infect Dis 44:Suppl. 2 (2007), S27–72.
12. [12] Manosroi, A., Khanrin, P., Lohcharoenkal, W., Werner, R.G., Götz, F., Manosroi, W., et al. Transdermal absorption enhancement through rat skin of gallidermin loaded in niosomes. Int J Pharm 392 (2010), 304–310.
13. [13] Morgan, S.M., O'Connor, P.M., Cotter, P.D., Ross, R.P., Hill, C., Sequential actions of the two component peptides of the lantibiotic lacticin 3147 explain its antimicrobial activity at nanomolar concentrations. Antimicrob Agents Chemother 49 (2005), 2606–2611.
14. [14] Papagianni, M., Ribosomally synthesized peptides with antimicrobial properties: biosynthesis, structure, function, and applications. Biotechnol Adv 21 (2003), 465–499.
15. [15] Van Heel, A.J., Montalban-Lopez, M., Kuipers, O.P., Evaluating the feasibility of lantibiotics as an alternative therapy against bacterial infections in humans. Exp Opin Drug Metabol Toxicol 7 (2011), 675–680.
16. [16] Van Staden, A.D., Brand, A.M., Dicks, L.M.T., Nisin F-loaded brushite bone cement prevented the growth of Staphylococcus aureus in vivo. J Appl Microbiol 112 (2012), 831–840.
17. [17] Chatterjee, S., Chatterjee, D.K., Jani, R.H., Blumbach, J., Ganguli, B.N., Klesel, N., et al. Mersacidin, a new antibiotic from Bacillus. In vitro and in vivo antibacterial activity. J Antibiot (Tokyo) 45 (1992), 839–845.
18. [18] Abee, T., Klaenhammer, T.R., Letellier, L., Kinetic studies of the action of lactacin F, a bacteriocin produced by Lactobacillus johnsonii that forms poration complexes in the cytoplasmic membrane. Appl Environ Microbiol 60 (1994), 1006–1013.
19. [19] Bierbaum, G., Sahl, H.G., Lantibiotics: mode of action, biosynthesis and bioengineering. Curr Pharm Biotechnol 10 (2009), 2–18.
20. [20] Bonelli, R., Wiedemann, R.I., Sahl, H.G., Lantibiotics. Kastin, A., (eds.) Handbook of biologically active peptides, 2006, Elsevier, New York (NY), 379–392.
21. [21] González-Martínez, B.E., Gómez-Treviño, M., Jiménez-Salas, Z., Bacteriocinas de probióticos. Rev Salud Pública y Nutrición. 2003, 4.
22. [22] Sahl, H.G., Bierbaum, G., Lantibiotics: biosynthesis and biological activities of uniquely modified peptides from Gram-positive bacteria. Annu Rev Microbiol 52 (1998), 41–79.
23. [23] Chatterjee, C., Paul, M., Xie, L., van der Donk, W.A., Biosynthesis and mode of action of lantibiotics. Chem Rev 105 (2005), 633–684.
24. [24] McAuliffe, O., Ross, R.P., Hill, C., Lantibiotics: structure, biosynthesis and mode of action. FEMS Microbiol Rev 25 (2001), 285–308.
25. [25] Deegan, L.H., Cotter, P.D., Hill, C., Ross, P., Bacteriocins: biological tools for bio-preservation and shelf-life extension. Int Dairy J 16 (2006), 1058–1071.
26. [26] Drider, D., Fimland, G., Hechard, Y., McMullen, L.M., Prevost, H., The continuing story of class IIa bacteriocins. Microbiol Mol Biol Rev 70 (2006), 564–582.
27. [27] Sparo, M.D., Castro, M.S., Andino, P.J., Lavigne, M.V., Ceriani, C., Gutiérrez, G.L., et al. Partial characterization of enterocin MR99 from a corn silage isolate of Enterococcus faecalis. J Appl Microbiol 100 (2006), 123–134.
28. [28] Van Belkum, M.J., Worobo, R.W., Stiles, M.E., Double-glycine-type leader peptides direct secretion of bacteriocins by ABC transporters: colicin V secretion in Lactococcus lactis. Mol Microbiol 23 (1997), 1293–1301.
29. [29] Cintas, L.M., Casaus, P., Havarstein, L.S., Hernandez, P.E., Nes, I.F., Biochemical and genetic characterization of enterocin P, a novel sec-dependent bacteriocin from Enterococcus faecium P13 with a broad antimicrobial spectrum. Appl Environ Microbiol 63 (1997), 4321–4330.
30. [30] Ennahar, S., Sashihara, T., Sonomoto, K., Ishizaki, A., Class IIa bacteriocins: biosynthesis, structure and activity. FEMS Microbiol Rev 24 (2000), 85–106.
31. [31] Venema, K., Chikindas, M.L., Seegers, J.F.M.L., Haandrikman, A.J., Leenhouts, K.J., Venema, G., et al. Rapid and efficient purification methods for small, hydrophobic, cationic bacteriocins: purification of lactococcin B and pediocin PA-1. Appl Environ Microbiol 63 (1997), 305–309.
32. [32] Gong, H.S., Meng, X.C., Wang, H., Plantaricin MG active against Gram-negative bacteria produced by Lactobacillus plantarum KLDS1.0391 isolated from ‘Jiaoke’, a traditional fermented cream from China. Food Control 21 (2009), 89–96.
33. [33] Joerger, M.C., Klaenhammer, T.R., Characterization and purification of helveticin J and evidence for a chromosomally determined bacteriocin produced by Lactobacillus helveticus 481. J Bacteriol 167 (1986), 439–446.
34. [34] Vaughan, E.E., Daly, C., Fitzgerald, G.F., Identification and characterization of helveticin V-1829, a bacteriocin produced by Lactobacillus helveticus 1829. J Appl Bacteriol 73 (1992), 299–308.
35. [35] Lewus, C.B., Montville, T.J., Detection of bacteriocins produced by lactic acid bacteria. J Microbiol Methods 13 (1991), 145–150.
36. [36] Wirawan, R.E., Swanson, K.M., Kleffmann, T., Jack, R.W., Tagg, J.R., Uberolysin: a novel cyclic bacteriocin produced by Streptococcus uberis. Microbiology 153 (2007), 1619–1630.
37. [37] Zouhir, A., Hammami, R., Fliss, I., Hamida, J.B., A new structure-based classification of Gram-positive bacteriocins. Protein J 29 (2010), 432–439.
38. [38] Jack, R.W., Tagg, J.R., Ray, B., Bacteriocins of Gram-positive bacteria. Microbiol Rev 59 (1995), 171–200.
39. [39] Nes, I.F., Diep, D.B., Havarstein, L.S., Brurberg, M.B., Eijsink, V., Holo, H., Biosynthesis of bacteriocins in lactic acid bacteria. Antonie Van Leeuwenhoek 70 (1996), 113–128.
40. [40] Hurst, A., Nisin. Laskin, D., (eds.) Advances in applied microbiology, 1981, Academic Press, New York (NY), 27.
41. [41] Kozak, W., Bardowski, J., Dobrzanski, W.T., Lactostrepcins—acid bacteriocins produced by lactic streptococci. J Dairy Res 45 (1978), 247–257.
42. [42] Gonzalez, B., Arca, P., Mayo, B., Suarez, J., Detection, purification and partial characterization of plantaricin C, a bacteriocin produced by a Lactobacillus plantarum strain of dairy origin. Appl Environ Microbiol 6 (1994), 2158–2163.
43. [43] Parente, E., Hill, C., A comparison of factors affecting the production of two bacteriocins from lactic acid bacteria. J Appl Bacteriol 73 (1992), 290–298.
44. [44] Tam, J.P., Lu, Y., Yang, J., Antimicrobial dendrimeric peptides. Eur J Biochem 269 (2002), 923–932.
45. [45] Bracci, L., Falciani, C., Lelli, B., Lozzi, L., Runci, Y., Pini, A., Synthetic peptides in the form of dendrimers become resistant to protease activity. J Biol Chem 278 (2003), 46590–46595.
46. [46] Nigama, A., Gupta, D., Sharma, A., Treatment of infectious disease: beyond antibiotics. Microbiol Res 169 (2014), 643–651.
47. [47] Cascales, E., Buchanan, S.K., Duché, D., Kleanthous, C., Lloubès, R., Postle, K., et al. Colicin biology. Microbiol Mol Biol Rev 71 (2007), 158–229.
48. [48] Stevens, K.A., Sheldon, B.W., Klapes, N.A., Klaenhammer, T.R., Nisin treatment for inactivation of Salmonella species and other Gram-negative bacteria. Appl Environ Microbiol 57 (1991), 3613–3615.
49. [49] Chikindas, M.L., García-Garcerá, M.J., Driessen, A.J.M., Ledeboer, A.M., Nissen-Meyer, J., Nes, I.F., et al. Pediocin PA-1, a bacteriocin from Pediococcus acidilactici PAC1.0, forms hydrophilic pores in the cytoplasmic membrane of target cells. Appl Environ Microbiol 59 (1993), 3577–3584.
50. [50] Montville, T.J., Chen, Y., Mechanistic action of pediocin and nisin: recent progress and unresolved questions. Appl Microbiol Biotechnol 50 (1998), 511–519.
51. [51] Clardy, J., Fischbach, M.A., Walsh, C.T., New antibiotics from bacterial natural products. Nat Biotechnol 24 (2006), 1541–1550.
52. 2+ ions on the activity of lantibiotics containing a mersacidin-like lipid II binding motif. Appl Environ Microbiol 75 (2009), 4427–4434.
53. [53] Gründling, A., Schneewind, O., Cross-linked peptidoglycan mediates lysostaphin binding to the cell wall envelope of Staphylococcus aureus. J Bacteriol 188 (2006), 2463–2472.
54. [54] Kjos, M., Nes, I.F., Diep, D.B., Class II one-peptide bacteriocins target a phylogenetically defined subgroup of mannose phosphotransferase systems on sensitive cells. Microbiology 155 (2009), 2949–2961.
55. [55] Hammami, R., Fernandez, B., Lacroix, C., Fliss, I., Anti-infective properties of bacteriocins: an update. Cell Mol Life Sci 70 (2009), 2947–2967.
56. [56] Fimland, G., Blingsmo, O.R., Sletten, K., Jung, G., Nes, I.F., Nissen-Meyer, J., New biologically active hybrid bacteriocins constructed by combining regions from various pediocin-like bacteriocins: the C-terminal region is important for determining specificity. Appl Environ Microbiol 62 (1996), 3313–3318.
57. [57] Brogden, K.A., Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria?. Nat Rev Microbiol 3 (2005), 238–250.
58. [58] Ettayebi, K., El Yamani, J., Rossi-Hassani, B., Synergistic effect of nisin and thymol on antimicrobial activities in Listeria monocytogenes and Bacillus subtilis. FEMS Microbiol Lett 183 (2000), 191–195.
59. [59] Sivarooban, T., Hettiarachchy, N.S., Johnson, M.G., Transmission electron microscopy study of Listeria monocytogenes treated with nisin in combination with either grape seed or green tea seed. J Food Prot 71 (2008), 2105–2109.
60. [60] O'Flaherty, S., Coffey, A., Meaney, W., Fitzgerald, G.F., Ross, R.P., Recombinant phage lysin LysK has a broad spectrum of lytic activity against clinically relevant staphylococci, including methicillin-resistant Staphylococcus aureus. J Bacteriol 187 (2005), 7161–7164.
61. [61] Dajcs, J.J., Hume, E.B., Moreau, J.M., Caballero, A.R., Cannon, B.M., O'Callaghan, R.J., Lysostaphin treatment of methicillin-resistant Staphylococcus aureus keratitis in the rabbit. Am J Ophtalmol, 130, 2000, 544.
62. [62] Becker, S.C., Foster-Frey, J., Donovan, D.M., Phage K lytic enzyme LysK and lysostaphin act synergistically to kill MRSA. FEMS Microbiol Lett 287 (2008), 185–191.
63. [63] Nascimento, J.G., Guerreiro-Pereira, M.D., Costa, S.F., Sao-José, C., Santos, M.A., Nisin-triggered activity of Lys44, the secreted endolysin from Oenococcus oeni phage fOg44. J Bacteriol 190 (2008), 457–461.
64. [64] Havarstein, L.S., Holo, H., Nes, I.F., The leader peptide of colicin V shares consensus sequences with leader peptides that are common amongst peptide bacteriocins produced by Gram-positive bacteria. Microbiology 140 (1994), 2383–2389.
65. [65] Ramakrishnan, V., Narayan, B., Halami, P.M., Combined effect of enterocin and lipase from Enterococcus faecium NCIM5363 against food borne pathogens: mode of action studies. Curr Microbiol 65 (2012), 4095–4099.
66. [66] Lebel, G., Piché, F., Frenette, M., Gottschalk, M., Grenier, D., Antimicrobial activity of nisin against the swine pathogen Streptococcus suis and its synergistic interaction with antibiotics. Peptides 50 (2013), 19–23.
67. [67] Singh, A.P., Prabha, V., Rishi, P., Value addition in the efficacy of conventional antibiotics by nisin against Salmonella. PLoS ONE, 8, 2013, e76844.
68. [68] Naghmouchi, K., Baah, J., Hober, D., Jouy, E., Rubrecht, C., Sané, F., et al. Synergistic effect between colistin and bacteriocins in controlling Gram-negative pathogens and their potential to reduce antibiotic toxicity in mammalian epithelial cells. Antimicrob Agents Chemother 57 (2013), 2719–2725.
69. [69] Worobo, R.W., VanBelkum, M.J., Sailer, M., Roy, K.L., Vederas, J.C., Stiles, M.E., A signal peptide secretion-dependent bacteriocin from Carnobacterium divergens. J Bacteriol 177 (1995), 3143–3149.
70. [70] Havarstein, L.S., Diep, B.D., Nes, I.F., A family of bacteriocin ABC transporters carry out proteolytic processing of their substrates concomitant with export. Mol Microbiol 16 (1995), 229–240.
71. [71] Nakayama, K., Takashima, K., Ishihara, H., Shinomiya, T., Kageyama, M., Kanaya, S., et al. The R-type pyocin of Pseudomonas aeruginosa is related to P2 phage, and the F-type is related to lambda phage. Mol Microbiol 38 (2000), 213–231.
72. [72] Matsui, H., Sano, Y., Ishihara, H., Shinomiya, T., Regulation of pyocin genes in Pseudomonas aeruginosa by positive (prtN) and negative (prtR) regulatory genes. J Bacteriol 175 (1993), 1257–1263.
73. [73] Michel-Briand, Y., Baysse, C., The pyocins of Pseudomonas aeruginosa. Biochimie 84 (2002), 499–510.
74. [74] Eijsink, V.G., Axelsson, L., Diep, D.B., Havarstein, L.S., Holo, H., Nes, I.F., Production of class II bacteriocins by lactic acid bacteria; an example of biological warfare and communication. Antonie Van Leeuwenhoek 81 (2002), 639–654.
75. [75] Moreno, I., Lerayer, A.S.L., Leitão, M.F.F., Detection and characterization of bacteriocin producing Lactococcus lactis strains. Rev Microbiol 30 (1999), 130–136.
76. [76] Messi, P., Bondi, M., Sabia, C., Battini, R., Manicardi, G., Detection and preliminary characterization of a bacteriocin plantaricin 35d, produced by a Lactobacillus plantarum strain. Int J Food Microbiol 64 (2001), 193–198.
77. [77] Torodov, S.D., Dicks, L.M.T., Lactobacillus plantarum isolated from molasses produces bacteriocins active against Gram-negative bacteria. Enzyme Microb Tech 36 (2005), 318–326.
78. [78] Lade, H.S., Chitanand, M.P., Gyananath, G., Kadam, T.A., Studies on some properties of bacteriocins produced by Lactobacillus species isolated from agro-based waste. Internet J Microbiol, 2, 2006 https://ispub.com/IJMB/2/1/13427 accessed 15.09.16.
79. [79] Ivanova, I., Kabadjova, P., Pantev, A., Danova, S., Dousset, X., Detection, purification and partial characterization of a novel bacteriocin substance produced by Lactococcus lactis subsp. lactis B14 isolated from Boza-Bulgarian traditional cereal beverage. Biocatalysis 41 (2000), 47–53.
80. [80] Lohans, C.T., Vederas, J.C., Development of class IIa bacteriocins as therapeutic agents. Int J Microbiol, 13, 2012, 386410.
81. [81] Collins, B., Guinane, C.M., Cotter, P.D., Hill, C., Ross, R.P., Assessing the contributions of the LiaS histidine kinase to the innate resistance of Listeria monocytogenes to nisin, cephalosporins, and disinfectants. Appl Environ Microbiol 78 (2012), 2923–2929.
82. [82] Gravesen, A., Ramnath, M., Rechinger, K.B., Andersen, N., Jänsch, L., Héchard, Y., et al. High-level resistance to class IIa bacteriocins is associated with one general mechanism in Listeria monocytogenes. Microbiology 148 (2002), 2361–2369.
83. [83] Katla, T., Naterstad, K., Vancanneyt, M., Swings, J., Axelsson, L., Differences in susceptibility of Listeria monocytogenes strains to sakacin P, sakacin A, pediocin PA-1, and nisin. Appl Environ Microbiol 69 (2003), 4431–4437.
84. [84] Tessema, G.T., Møretrø, T., Kohler, A., Axelsson, L., Naterstad, K., Complex phenotypic and genotypic responses of Listeria monocytogenes strains exposed to the class IIa bacteriocin sakacin P. Appl Environ Microbiol 75 (2009), 6973–6980.
85. [85] Jarvis, B., Farr, J., Partial purification, specificity and mechanism of action of the nisin-inactivating enzyme from Bacillus cereus. Biochim Biophys Acta 227 (1971), 232–240.
86. [86] Bastos, M.C.F., Ceotto, H., Coelho, M.L.V., Nascimento, J.S., Staphylococcal antimicrobial peptides: relevant properties and potential biotechnological applications. Curr Pharm Biotechnol 10 (2009), 38–61.
87. [87] Svetoch, E.A., Eruslanov, B.V., Kovalev, Y.N., Mitsevich, E.V., Mitsevich, I.P., Levchuk, V.P., et al. Antimicrobial activities of bacteriocins E 50–52 and B 602 against antibiotic-resistant strains involved in nosocomial infections. Probiotics Antimicrob Proteins, 1, 2009, 136.
88. [88] Ghodhbane, H., Elaidi, S., Sabatier, J.M., Achour, S., Benhmida, J., Regaya, I., Bacteriocins active against multi-resistant gram negative bacteria implicated in nosocomial infections. Infect Disord Drug Targets 15 (2015), 2–12.
89. [89] Michalet, S., Cartier, G., David, B., Mariotte, A.M., Dijoux-franca, M.G., Kaatz, G.W., et al. N-caffeoylphenalkylamide derivatives as bacterial efflux pump inhibitors. Bioorg Med Chem Lett 17 (2007), 1755–1758.
90. [90] Piper, C., Casey, P.G., Hill, C., Cotter, P.D., Ross, R.P., The lantibiotic lacticin 3147 prevents systemic spread of Staphylococcus aureus in a murine infection model. Int J Microbiol, 2012, 2012, 806230.
91. [91] Van Staden, D.A., Brand, A.M., Endo, A., Dicks, L.M.T., Nisin F, intraperitoneally injected, may have a stabilizing effect on the bacterial population in the gastro-intestinal tract, as determined in a preliminary study with mice as model. Lett Appl Microbiol 53 (2011), 198–201.
92. [92] Oman, T.J., van der Donk, W.A., Insights into the mode of action of the two-peptide lantibiotic haloduracin. ACS Chem Biol 4 (2009), 865–874.
93. [93] Aunpad, R., Na-Bangchang, K., Pumilicin 4, a novel bacteriocin with anti-MRSA and anti-VRE activity produced by newly isolated bacteria Bacillus pumilus strain WAPB4. Curr Microbiol 55 (2007), 308–313.
94. [94] Jabés, D., Brunati, C., Candiani, G., Riva, S., Romanó, G., Donadio, S., Efficacy of the new lantibiotic NAI-107 in experimental infections induced by multidrug-resistant Gram-positive pathogens. Antimicrob Agents Chemother 55 (2011), 1671–1676.
95. [95] Mota-Meira, M., Morency, H., Lavoie, M.C., In vivo activity of mutacin B-Ny266. J Antimicrob Chemother 56 (2005), 869–871.
96. [96] Pascual, L., Daniele, M., Giordano, W., Pajaro, M., Barberis, I., Purification and partial characterization of novel bacteriocin L23 produced by Lactobacillus fermentum L23. Curr Microbiol 56 (2008), 397–402.
97. [97] Ghobrial, O.G., Derendorf, H., Hillman, J.D., Pharmacodynamic activity of the lantibiotic MU1140. Int J Antimicrob Agents 33 (2009), 70–74.
98. [98] Knoetze, H., Todorov, S.D., Dicks, L.M.T., A class IIa peptide from Enterococcus mundtii inhibits bacteria associated with otitis media. Int J Antimicrob Agents 31 (2008), 228–234.
99. [99] Kruszewska, D., Sahl, H.G., Bierbaum, G., Pag, U., Hynes, S.O., Ljungh, A., Mersacidin eradicates methicillin-resistant Staphylococcus aureus (MRSA) in a mouse rhinitis model. J Antimicrob Chemother 54 (2004), 648–653.
100. [100] De Kwaadsteniet, M., Doeschate, K.T., Dicks, L.M.T., Nisin F in the treatment of respiratory tract infections caused by Staphylococcus aureus. Lett Appl Microbiol 48 (2009), 65–70.
101. [101] Carroll, J., Draper, L.A., O'Connor, P.M., Coffey, A., Hill, C., Ross, R.P., et al. Comparison of the activities of the lantibiotics nisin and lacticin 3147 against clinically significant mycobacteria. Int J Antimicrob Agents 36 (2010), 132–136.
102. [102] Steiner, I., Errhalt, P., Kubesch, K., Hubner, M., Holy, M., Bauer, M., et al. Pulmonary pharmacokinetics and safety of nebulized duramycin in healthy male volunteers. Naunyn Schmiedebergs Arch Pharmacol 378 (2008), 323–333.
103. [103] Sosunov, V., Mischenko, V., Eruslanov, B., Svetoch, E., Shakina, Y., Stern, N., et al. Antimycobacterial activity of bacteriocins and their complexes with liposomes. J Antimicrob Chemother 59 (2007), 919–925.
104. [104] De Kwaadsteniet, M., van Reenen, C., Dicks, L., Evaluation of nisin F in the treatment of subcutaneous skin infections, as monitored by using a bioluminescent strain of Staphylococcus aureus. Probiotics Antimicrob Proteins 2 (2010), 61–65.
105. [105] Bowe, W.P., Filip, J.C., Di Rienzo, J.M., Volgina, A., Margolis, D.J., Inhibition of Propionibacterium acnes by bacteriocin-like inhibitory substances (BLIS) produced by Streptococcus salivarius. J Drugs Dermatol 5 (2006), 868–870.
106. [106] Kang, B., Seo, J.G., Lee, G.S., Kim, J.H., Kim, S., Han, Y., et al. Antimicrobial activity of enterocins from Enterococcus faecalis SL-5 against Propionibacterium acnes, the causative agent in acne vulgaris, and its therapeutic effect. J Microbiol 47 (2009), 101–109.
107. [107] Izquierdo, E., Wagner, C., Marchioni, E., Aoude-Werner, D., Ennahar, S., Enterocin 96, a novel class II bacteriocin produced by Enterococcus faecalis WHE 96, isolated from Munster cheese. Appl Environ Microbiol 75 (2009), 4273–4276.
108. [108] Sanchez, J., Diep, D.B., Herranz, C., Nes, I.F., Cintas, L.M., Hernandez, P.E., Amino acid and nucleotide sequence, adjacent genes, and heterologous expression of hiracin JM79, a sec-dependent bacteriocin produced by Enterococcus hirae DCH5, isolated from Mallard ducks (Anas platyrhynchos). FEMS Microbiol Lett 270 (2007), 227–236.
109. [109] Sawa, N., Zendo, T., Kiyofuji, J., Fujita, K., Himeno, K., Nakayama, J., et al. Identification and characterization of lactocyclicin Q, a novel cyclic bacteriocin produced by Lactococcus sp. strain QU 12. Appl Environ Microbiol 75 (2009), 1552–1558.
110. [110] Wu, S., Jia, S., Sun, D., Chen, M., Chen, X., Zhong, J., et al. Purification and characterization of two novel antimicrobial peptides subpeptin JM4-A and subpeptin JM4-B produced by Bacillus subtilis JM4. Curr Microbiol 51 (2005), 292–296.
111. [111] Shelburne, C.E., An, F.Y., Dholpe, V., Ramamoorthy, A., Lopatin, D.E., Lantz, M.S., The spectrum of antimicrobial activity of the bacteriocin subtilosin A. J Antimicrob Chemother 59 (2007), 297–300.
112. [112] Siegers, K., Entian, K.D., Genes involved in immunity to the lantibiotic nisin produced by Lactococcus lactis 6F3. Appl Environ Microbiol 61 (1995), 1082–1089.
113. [113] Hammami, R., Zouhir, A., Le Lay, C., Ben Hamida, J., Fliss, I., Database mining for bacteriocin discovery. 2011, CABI Publishing, Wallingford, UK.
114. [114] Howell, T.H., Fiorellini, J.P., Blackburn, P., Projan, S.J., de la Harpe, J., Williams, R.C., The effect of a mouthrinse based on nisin, a bacteriocin, on developing plaque and gingivitis in beagle dogs. J Clin Periodontol 20 (1993), 335–339.
115. [115] Tagg, J.R., Prevention of streptococcal pharyngitis by anti-Streptococcus pyogenes bacteriocin-like inhibitory substances (BLIS) produced by Streptococcus salivarius. Indian J Med Res 119 (2014), 13–16.
116. [116] Lazzarini, A., Gastaldo, L., Candiani, G., Ciciliato, I., Losi, D., Marinelli, F., et al. Antibiotic 107891, its factors A1 and A2, pharmaceutically acceptable salts and compositions, and use thereof. US Patent #07351687, 2008.
117. [117] Miyauchi, E., O'Callaghan, J., Buttó, L.F., Hurley, G., Melgar, S., Tanabe, S., et al. Mechanism of protection of transepithelial barrier function by Lactobacillus salivarius: strain dependence and attenuation by bacteriocin production. Am J Physiol Gastrointest Liver Physiol 1 (2013), 1029–1041.
118. [118] Dover, S.E., Aroutcheva, A.A., Faro, S., Chikindas, M.L., Safety study of an antimicrobial peptide lactocin 160, produced by the vaginal Lactobacillus rhamnosus. Infect Dis Obstet Gynecol, 2007, 2007, 78248.
119. [119] Sutyak, K.E., Wirawan, R.E., Aroutcheva, A.A., Chikindas, M.L., Isolation of the Bacillus subtilis antimicrobial peptide subtilosin from the dairy product-derived Bacillus amyloliquefaciens. J Appl Microbiol 104 (2008), 1067–1074.
120. [120] Kaewnopparat, S., Dangmanee, N., Kaewnopparat, N., Srichana, T., Chulasiri, M., Settharaksa, S., In vitro probiotic properties of Lactobacillus fermentum SK5 isolated from vagina of a healthy woman. Anaerobe 22 (2013), 6–13.
121. [121] Reddy, K.V.R., Aranha, C., Gupta, S.M., Yedery, R.D., Evaluation of antimicrobial peptide nisin as a safe vaginal contraceptive agent in rabbits: in vitro and in vivo studies. Reproduction 128 (2004), 117–126.
122. [122] Kaur, B., Balgir, P.P., Mittu, B., Kumar, B., Garg, N., Biomedical applications of fermenticin HV6b isolated from Lactobacillus fermentum HV6b MTCC10770. Biomed Res Int, 2013, 2013, 168438.
123. [123] Lange-Starke, A., Petereit, A., Truyen, U., Braun, P.G., Fehlhaber, K., Albert, T., Antiviral potential of selected starter cultures, bacteriocins and D,L-lactic acid. Food Environ Virol 6 (2014), 42–47.
124. [124] Torres, N.I., Noll, K.S., Xu, S., Li, J., Huang, Q., Sinko, P.J., et al. Safety, formulation, and in vitro antiviral activity of the antimicrobial peptide subtilosin against herpes simplex virus type 1. Probiotics Antimicrob Proteins 5 (2013), 26–35.
125. [125] Varella, C.M.L., Santos Nascimento, J.D., Fagundes, P.C., Madureira, D.J., Oliveira, S.S.D., Vasconcelos de Paiva Brito, M.A., et al. Activity of staphylococcal bacteriocins against Staphylococcus aureus and Streptococcus agalactiae involved in bovine mastitis. Res Microbiol 158 (2007), 625–630.
126. [126] Crispie, F., Flynn, J., Ross, R.P., Hill, C., Meaney, W., Update on the development of a novel dry cow therapy using a bismuth-based intramammary teat seal in combination with the bacteriocin lacticin 3147. Ir Vet J 57 (2004), 652–656.
127. [127] Crispie, F., Twomey, D., Flynn, J., Hill, C., Ross, P., Meaney, W., The lantibiotic lacticin 3147 produced in a milk-based medium improves the efficacy of a bismuth-based teat seal in cattle deliberately infected with Staphylococcus aureus. J Dairy Res 72 (2005), 159–167.
128. [128] Klostermann, K., Crispie, F., Flynn, J., Meaney, W.J., Paul, R.R., Hill, C., Efficacy of a teat dip containing the bacteriocin lacticin 3147 to eliminate Gram-positive pathogens associated with bovine mastitis. J Dairy Res 77 (2010), 231–238.
129. [129] Kim, S.Y., Shin, H., Koo, H.C., Youn, J.H., Paik, H.D., Park, Y.H., In vitro antimicrobial effect and in vivo preventive and therapeutic effects of partially purified lantibiotic lacticin NK34 against infection by Staphylococcus species isolated from bovine mastitis. J Dairy Sci 93 (2010), 3610–3615.
130. [130] Rea, M.C., Sit, C.S., Clayton, E., O'Connor, P.M., Whittal, R.M., Zheng, J., et al. Thuricin CD, a posttranslationally modified bacteriocin with a narrow spectrum of activity against Clostridium difficile. Proc Natl Acad Sci USA 107 (2010), 9352–9357.
131. [131] Wirawan, R.E., Klesse, N.A., Jack, R.W., Tagg, J.R., Molecular and genetic characterization of a novel nisin variant produced by Streptococcus uberis. Appl Environ Microbiol 72 (2006), 1148–1156.
132. [132] Pieterse, R., Todorov, S.D., Dicks, L.M.T., Mode of action and in vitro susceptibility of mastitis pathogens to macedocin ST91KM and preparation of a teat seal containing the bacteriocin. Braz J Microbiol 41 (2010), 133–145.
133. [133] Barboza-Corona, J.E., de la Fuente-Salcido, N., Alva-Murillo, N., Ochoa-Zarzosa, A., Lopez-Meza, J.E., Activity of bacteriocins synthesized by Bacillus thuringiensis against Staphylococcus aureus isolates associated to bovine mastitis. Vet Microbiol 138 (2009), 179–183.
134. [134] Salvucci, E., Saavedra, L., Hebert, E.M., Haro, C., Sesma, F., Enterocin CRL35 inhibits Listeria monocytogenes in a murine model. Foodborne Pathog Dis 9 (2012), 68–74.
135. [135] Zuckerman, H., Ben Avraham, R., Control of growth of L. monocytogenes in fresh salmon using MicrogardTM and nisin. Lebensmittel-Wissenschaft Und-Technologie Food Sci Tech 35 (2002), 543–548.
136. [136] Martin-Visscher, L.A., van Belkum, M.J., Garneau-Tsodikova, S., Whittal, R.M., Zheng, J., McMullen, L.M., et al. Isolation and characterization of carnocyclin A, a novel circular bacteriocin produced by Carnobacterium maltaromaticum UAL307. Appl Environ Microbiol 74 (2008), 4756–4763.
137. [137] Corr, S.C., Li, Y., Riedel, C.U., O'Toole, P.W., Hill, C., Gahan, C.G.M., Bacteriocin production as a mechanism for the antiinfective activity of Lactobacillus salivarius UCC118. Proc Natl Acad Sci USA 104 (2007), 7617–7621.
138. [138] Cursino, L., Smajs, D.S., Marda, J., Nardi, R.M.D., Nicoli, J.R., Chartone-Souza, E., et al. Exoproducts of the Escherichia coli strain H22 inhibiting some enteric pathogens both in vitro and in vivo. J Appl Microbiol 100 (2006), 821–829.
139. [139] Huang, E., Zhang, L., Chung, Y.K., Zheng, Z., Yousef, A.E., Characterization and application of enterocin RM6, a bacteriocin from Enterococcus faecalis. Biomed Res Int, 2013, 2013, 206917.
140. [140] Ahmad, V., Iqbal, A.N., Haseeb, M., Khan, M.S., Antimicrobial potential of bacteriocin producing Lysinibacillus jx416856 against foodborne bacterial and fungal pathogens, isolated from fruits and vegetable waste. Anaerobe 27 (2014), 87–95.
141. [141] Chopra, L., Singh, G., Choudhary, V., Sahoo, D.K., Sonorensin: an antimicrobial peptide, belonging to heterocycloanthracin subfamily of bacteriocins, from a new marine isolate Bacillus sonorensis MT93. Appl Environ Microbiol 80 (2014), 2981–2990.
142. [142] Schillinger, U., Geisen, R., Holzapfel, W.H., Potential of antagonistic microorganisms and bacteriocins for the biological preservation of foods. Trends Food Sci Technol 7 (1996), 158–164.
143. [143] Dabour, N., Zihler, A., Kheadr, E., Lacroix, C., Fliss, I., In vivo study on the effectiveness of pediocin PA-1 and Pediococcus acidilactici UL5 at inhibiting Listeria monocytogenes. Int J Food Microbiol 133 (2009), 225–233.
144. [144] Jay, J.M., Modern food microbiology. 5th ed, 1996, Chapman and Hall, New York (NY).
145. [145] Ryser, E.T., Marth, E.H., Listeria, listeriosis and food safety. 2nd ed, 1999, Marcel Dekker, Inc., New York (NY).
146. [146] Caballero Gómez, N., Abriouel, H., Ennahar, S., Gálvez, A., Comparative proteomic analysis of Listeria monocytogenes exposed to enterocin AS-48 in planktonic and sessile states. Int J Food Microbiol 167 (2013), 202–207.
147. [147] Espitia, P.J., Soares, N.F., Teófilo, R.F., Coimbra, J.S., Vitor, D.M., Batista, R.A., et al. Physical-mechanical and antimicrobial properties of nanocomposite films with pediocin and ZnO nanoparticles. Carbohydr Polym 94 (2013), 199–208.
148. [148] Barbosa, A.A., Silva de Araújo, H.G., Matos, P.N., Carnelossi, M.A., Almeida de Castro, A., Effects of nisin-incorporated films on the microbiological and physicochemical quality of minimally processed mangoes. Int J Food Microbiol 164 (2013), 135–140.
149. [149] Galvez, A., Lopez, R.L., Abriouel, H., Valdivia, E., Omar, N.B., Application of bacteriocins in the control of foodborne pathogenic and spoilage bacteria. Crit Rev Biotechnol 28 (2008), 125–152.
150. [150] García, P., Rodríguez, L., Rodríguez, A., Martínez, B., Food biopreservation: promising strategies using bacteriocins, bacteriophages and endolysins. Trends Food Sci Technol 21 (2010), 373–382.
151. [151] Pilet, M.F., Leroi, F., Applications of protective cultures, bacteriocins and bacteriophages in fresh seafood and seafood products. Lacroix, C., (eds.) Protective cultures, antimicrobial metabolites and bacteriophages for food and beverage biopreservation, 2011, Woodhead Publishing Ltd., Cambridge, UK, 1–21.
152. [152] McCall, J.O., Sizemore, R.K., Description of a bacteriocinogenic plasmid in Beneckea harveyi. Appl Environ Microbiol 38 (1979), 974–979.
153. [153] Calo-Mata, P., Arlindo, S., Boehme, K., Miguel, T., Pascoal, A., Barros-Velazquez, J., Current applications and future trends of lactic acid bacteria and their bacteriocins for the bio-preservation of aquatic food products. Food Bioprocess Technol 1 (2007), 43–63.
154. [154] Galvez, A., Abriouel, H., Lopez, R.L., Ben Omar, N., Bacteriocin-based strategies for food biopreservation. Int J Food Microbiol 120 (2007), 51–70.
155. [155] Brillet, A., Pilet, M.F., Prevost, H., Cardinal, M., Leroi, F., Effect of inoculation of Carnobacterium divergens V41, a bio-preservative strain against Listeria monocytogenes risk, on the microbiological, chemical and sensory quality of cold smoked salmon. Int J Food Microbiol 104 (2005), 309–324.
156. [156] Schobitz, R., Zaror, T., Leon, O., Costa, M., A bacteriocin from Carnobacterium piscicola for the control of Listeria monocytogenes in vacuum-packaged meat. Food Microbiol 16 (1999), 249–255.
157. [157] Gebreyohannes, G., Moges, F., Sahile, S., Raja, N., Isolation and characterization of potential antibiotic producing actinomycetes from water and sediments of lake Tana, Ethiopia. Asian Pac J Trop Biomed 3 (2013), 426–435.
158. [158] Valli, S., Sugasini, S., Aysha, O.S., Nirmala, P., Kumar, V.P., Reena, A., Antimicrobial potential of actinomycetes species isolated from marine environment. Asian Pacific J Trop Biomed 9 (2012), 416–473.
159. [159] Nykanen, A., Weckman, K., Lapvetelainen, A., Synergistic inhibition of Listeria monocytogenes on cold-smoked rainbow trout by nisin and sodium lactate. Int J Food Microbiol 61 (2000), 63–72.
160. [160] Neetoo, H., Ye, M., Chen, H., Joerger, R.D., Hicks, D.T., Hoover, D.G., Use of nisin-coated plastic films to control Listeria monocytogenes on vacuum-packaged cold-smoked salmon. Int J Food Microbiol 122 (2008), 8–15.
161. [161] Aasen, I.M., Markussen, S., Moretro, T., Katla, T., Axelsson, L., Naterstad, K., Interactions of the bacteriocins sakacin P and nisin with food constituents. Int J Food Microbiol 87 (2003), 35–43.
162. [162] Al-Holy, M., Ruiter, J., Lin, M., Kang, D.H., Rasco, B., Inactivation of Listeria innocua in nisin-treated salmon (Oncorhynchus keta) and sturgeon (Acipenser transmontanus) caviar heated by radio frequency. J Food Prot 67 (2004), 1848–1854.
163. [163] Elotmani, F., Assobhei, O., In vitro inhibition of microbial flora of fish by nisin and lactoperoxidase system. Lett Appl Microbiol 38 (2004), 60–65.
164. [164] Luders, T., Birkemo, G.A., Fimland, G., Nissen-Meyer, J., Nes, I.F., Strong synergy between a eukaryotic antimicrobial peptide and bacteriocins from lactic acid bacteria. Appl Environ Microbiol 69 (2003), 1797–1799.
165. [165] Nilsson, L., Huss, H.H., Gram, L., Inhibition of Listeria monocytogenes on cold smoked salmon by nisin and carbon dioxide atmosphere. Int J Food Microbiol 38 (1997), 217–227.
166. 2. Lett Appl Microbiol 28 (1999), 373–377.
167. [167] Tahiri, I., Desbiens, M., Kheadr, E., Lacroix, C., Fliss, I., Comparison of different application strategies of divergicin M35 for inactivation of Listeria monocytogenes in cold-smoked wild salmon. Food Microbiol 26 (2009), 783–793.
168. [168] Tsironi, T.N., Taoukis, P.S., Modeling microbial spoilage and quality of gilthead seabream fillets: combined effect of osmotic pretreatment, modified atmosphere packaging, and nisin on shelf life. J Food Sci 75 (2010), 243–251.
169. [169] Bushra, U., Ahmed Mohammad, N.V., Ahmad, V.U., Edwards, D., Screening of marine bacteria of Pakistan coast for drug discovery potential. Proc Pak Acad Sci 46 (2009), 137–144.
170. [170] Sameiro, M., Gonalves, T., Fluorescent labeling of biomolecules with organic probes. Chem Rev 109 (2009), 190–212.
171. [171] Imran, M., Revol-Junelles, A.M., de Bruin, M., Paris, C., Breukink, E., Desobry, S., Fluorescent labeling of nisin Z and assessment of anti-listerial action. J Microbiol Methods 95 (2013), 107–113.
172. [172] Kuipers, O.P., Beerthuyzen, M.M., Siezen, R.J., de Vos, W.M., Characterization of the nisin gene cluster nisABTCIPR of Lactococcus lactis. Eur J Biochem 216 (1993), 281–291.
173. [173] Engelke, G., Gutowski-Eckel, Z., Kiesau, P., Siegers, K., Hammelmann, M., Entian, K.D., Regulation of nisin biosynthesis and immunity in Lactococcus lactis 6F3. Appl Environ Microbiol 60 (1994), 814–825.
174. [174] Smith, K., Martin, L., Rinaldi, A., Rajendran, R., Ramage, G., Walker, D., Activity of pyocin S2 against Pseudomonas aeruginosa biofilms. Antimicrob Agents Chemother 56 (2012), 1599–1601.
175. [175] Qiu, X.Q., Wang, H., Lu, X.F., Zhang, J., Li, S.F., Cheng, G., et al. An engineered multidomain bactericidal peptide as a model for targeted antibiotics against specific bacteria. Nat Biotechnol 21 (2003), 1480–1485.
176. [176] Yan, L.Z., Gibbs, A.C., Stiles, M.E., Wishart, D.S., Vederas, J.C., Analogues of bacteriocins: antimicrobial specificity and interactions of leucocin A with its enantiomer, carnobacteriocin B2, and truncated derivatives. J Med Chem 43 (2000), 4579–4581.
177. [177] Oppegard, C., Rogne, P., Kristiansen, P.E., Nissen-Meyer, J., Structure analysis of the two-peptide bacteriocin lactococcin G by introducing D-amino acid residues. Microbiology 156 (2010), 1883–1889.
178. [178] Grasemann, H., Stehling, F., Brunar, H., Widmann, R., Laliberte, T.W., Molina, L., et al. Inhalation of Moli1901 in patients with cystic fibrosis. Chest 131 (2007), 1461–1466.