Bacteriocin-antimicrobial synergy: A medical and food perspective

Frontiers in Microbiology

Volumn 8, Issue JUN, 2017, Pages

  Mathur, Harsh ^a,b   Field, Des ^b,c   Rea, Mary C ^a,b   Cotter, Paul D ^a,b   Hill, Colin ^b,c   Ross, R Paul ^b,c  

^a TEAGASC FOOD RESEARCH CENTRE   (Ireland)

^b UNIVERSITY COLLEGE CORK   (Ireland)

^c UNIVERSITY COLLEGE CORK   (Ireland)

Author keywords

Antibiotic resistance; Antimicrobials; Bacteriocins; Combinations; Pathogens; Stressors; Synergy

Indexed keywords

ACTAGARDIN; BACTERIOCIN; BENZOYLARGININE ETHYL ESTER; ESSENTIAL OIL; GRAPE SEED EXTRACT; LANTIBIOTIC; METRONIDAZOLE; SINECATECHINS; VANCOMYCIN;

ANTIBIOTIC RESISTANCE; ANTIMICROBIAL ACTIVITY; ANTIMICROBIAL COMBINATION; ANTIMICROBIAL SYNERGY; BACILLUS AMYLOLIQUEFACIENS; BACTERIOPHAGE; BIOFILM; CLINICAL OUTCOME; CLOSTRIDIUM DIFFICILE INFECTION; COLONY FORMING UNIT; COMBINATION DRUG THERAPY; DRUG COST; ENDOCARDITIS; ENTEROCOCCUS FAECALIS; ENTEROHEMORRHAGIC ESCHERICHIA COLI; FOOD CONTAMINATION; FOOD CONTROL; GARDNERELLA VAGINALIS; GRAM NEGATIVE BACTERIUM; HUMAN; LISTERIA MONOCYTOGENES; MATHEMATICAL MODEL; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; METHICILLIN SUSCEPTIBLE STAPHYLOCOCCUS AUREUS; NONHUMAN; OPPORTUNISTIC INFECTION; PSEUDOMONAS AERUGINOSA; REVIEW; STAPHYLOCOCCUS PSEUDINTERMEDIUS; STREPTOCOCCUS SUIS; TRANSMISSION ELECTRON MICROSCOPY; URINARY TRACT INFECTION;

EID: 85021421030     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2017.01205     Document Type: Review

References (173)

1. Abachin, E., Poyart, C., Pellegrini, E., Milohanic, E., Fiedler, F., Berche, P., et al. (2002). Formation of d-alanyl-lipoteichoic acid is required for adhesion and virulence of Listeria monocytogenes. Mol. Microbiol. 43, 1-14. doi: 10.1046/j.1365-2958.2002.02723.x
2. Abdelraouf, K., Braggs, K. H., Yin, T., Truong, L. D., Hu, M., and Tam, V. H. (2012). Characterization of polymyxin B-induced nephrotoxicity: implications for dosing regimen design. Antimicrob. Agents Chemother. 56, 4625-4629. doi: 10.1128/AAC.00280-12
3. Algburi, A., Volski, A., and Chikindas, M. L. (2015). Natural antimicrobials subtilosin and lauramide arginine ethyl ester synergize with conventional antibiotics clindamycin and metronidazole against biofilms of Gardnerella vaginalis but not against biofilms of healthy vaginal lactobacilli. Pathog. Dis. 73:ftv018. doi: 10.1093/femspd/ftv018
4. Al-Seraih, A., Belguesmia, Y., Baah, J., Szunerits, S., Boukherroub, R., and Drider, D. (2017). Enterocin B3A-B3B produced by LAB collected from infant faeces: potential utilization in the food industry for Listeria monocytogenes biofilm management. A. Van Leeuw, J. Microb. 110, 205-219. doi: 10.1007/s10482-016-0791-5
5. Amrouche, T., Sutyak Noll, K., Wang, Y., Huang, Q., and Chikindas, M. L. (2010). Antibacterial activity of subtilosin Alone and combined with curcumin, poly-Lysine and zinc lactate against Listeria monocytogenes strains. Probiot. Antimicrob. Proteins 2, 250-257. doi: 10.1007/s12602-010-9042-7
6. Ananou, S., Gálvez, A., Martínez-Bueno, M., Maqueda, M., and Valdivia, E. (2005). Synergistic effect of enterocin AS-48 in combination with outer membrane permeabilizing treatments against Escherichia coli O157:H7. J. Appl. Microbiol. 99, 1364-1372. doi: 10.1111/j.1365-2672.2005.02733x
7. Ankomah, P., and Levin, B. R. (2012). Two-Drug Antimicrobial Chemotherapy: a mathematical model and experiments with Mycobacterium marinum. PLoS Pathog. 8:e1002487. doi: 10.1371/journal.ppat.1002487
8. Antonio, C. M., Abriouel, H., López, R. L., Omar, N. B., Valdivia, E., and Gálvez, A. (2009). Enhanced bactericidal activity of enterocin AS-48 in combination with essential oils, natural bioactive compounds and chemical preservatives against Listeria monocytogenes in ready-to-eat salad Food Chem. Toxicol. 47, 2216-2223. doi: 10.1016/j.fct.2009.06.012
9. Aranha, C. C., Gupta, S. M., and Reddy, K. V. (2008). Assessment of cervicovaginal cytokine levels following exposure to microbicide Nisin gel in rabbits. Cytokine 43, 63-70. doi: 10.1016/j.cyto.2008.04.005
10. Arnison, P. G., Bibb, M. J., Bierbaum, G., Bowers, A. A., Bugni, T. S., Bulaj, G., et al. (2013). Ribosomally synthesized and post-translationally modified peptide natural products: overview and recommendations for a universal nomenclature. Nat. Prod. Rep. 30, 108-160. doi: 10.1039/c2np20085f
11. Bach, S. J., McAliister, T. A., Veira, D. M., Gannon, V. P. J., and Holley, R. A. (2002). Transmission and control of Escherichia coli O157:H7-A review. Can. J. Anim. Sci. 82, 475-490. doi: 10.4141/A02-021
12. Bacon, A. E., McGrath, S., Fekety, R., and Holloway, W. J. (1991). In vitro synergy studies with Clostridium difficile. Antimicrob. Agents Chemother. 35, 582-583
13. Becker, S. C., Foster-Frey, J., and Donovan, D. M. (2008). The phage K lytic enzyme LysK and lysostaphin act synergistically to kill MRSA. FEMS Microbiol. Lett. 287, 185-191. doi: 10.1111/j.1574-6968.2008.01308.x
14. Besser, R. E., Lett, S. M., Weber, J. T., Doyle, M. P., Barrett, T. J., Wells, J. G., et al. (1993). An outbreak of diarrhea and hemolytic uremic syndrome from Escherichia coli O157:H7 in fresh-pressed apple cider. JAMA 269, 2217-2220. doi: 10.1001/jama.1993.03500170047032
15. Blaser, M. (2011). Antibiotic overuse: stop the killing of beneficial bacteria. Nature 476, 393-394. doi: 10.1038/476393a
16. Branen, J. K., and Davidson, P. M. (2004). Enhancement of nisin, lysozyme, and monolaurin antimicrobial activities by ethylenediaminetetraacetic acid and lactoferrin. Int. J. Food Microbiol. 90, 63-74. doi: 10.1016/S0168-1605(03)00172-7
17. Breukink, E., and de Kruijff, B. (2006). Lipid II as a target for antibiotics. Nat. Rev. Drug Discov. 5, 321-332. doi: 10.1038/nrd2004
18. Briers, Y., Klumpp, J., Schuppler, M., and Loessner, M. (2011). Genome sequence of Listeria monocytogenes Scott, A., a clinical isolate from a food-borne listeriosis outbreak. J. Bacteriol. 193, 4284-4285. doi: 10.1128/JB.05328-11
19. Brötz, H., Bierbaum, G., Markus, A., Molitor, E., and Sahl, H. G. (1995). Mode of action of the lantibiotic mersacidin: inhibition of peptidoglycan biosynthesis via a novel mechanism? Antimicrob. Agents Chemother. 39, 714-719
20. Brumfitt, W., Salton, M. R., and Hamilton-Miller, J. M. (2002). Nisin, alone and combined with peptidoglycan-modulating antibiotics: activity against methicillin-resistant Staphylococcus aureus and vancomycin-resistant enterococci. J. Antimicrob. Chemother. 50, 731-734. doi: 10.1093/jac/dkf190
21. Buommino, E., Scognamiglio, M., Donnarumma, G., Fiorentino, A., and D'Abrosca, B. (2014). Recent advances in natural product-based anti-biofilm approaches to control infections. Mini Rev. Med. Chem. 14, 1169-1182. doi: 10.2174/1389557515666150101095853
22. Burt, S. (2004). Essential oils: their antibacterial properties and potential applications in foods-a review. Int. J. Food Microbiol. 94, 223-253. doi: 10.1016/j.ijfoodmicro.2004.03.022
23. Caballero Gómez, N., Abriouel, H., Grande, M. J., Pérez Pulido, R., and Gálvez, A. (2013). Combined treatments of enterocin AS-48 with biocides to improve the inactivation of methicillin-sensitive and methicillin-resistant Staphylococcus aureus planktonic and sessile cells. Int. J. Food Microbiol. 163, 96-100. doi: 10.1016/j.ijfoodmicro.2013.02.018
24. Camargo, A. C., de Paula, O. A., Todorov, S. D., and Nero, L. A. (2016). In vitro evaluation of bacteriocins activity against Listeria monocytogenes biofilm formation. Appl. Biochem. Biotechnol. 178, 1239-1251. doi: 10.1007/s12010-015-1941-3
25. Campion, A., Morrissey, R., Field, D., Cotter, P. D., Hill, C., and Ross, R. P. (2017). Use of enhanced nisin derivatives in combination with food-grade oils or citric acid to control Cronobacter sakazakii and Escherichia coli O157:H7. Food Microbiol. 65, 254-263. doi: 10.1016/j.fm.2017.01.020
26. Catlin, B. W. (1992). Gardnerella vaginalis: characteristics, clinical considerations, and controversies. Clin. Microbiol. Rev. 5, 213-237. doi: 10.1128/CMR.5.3.213
27. Cavera, V. L., Volski, A., and Chikindas, M. L. (2015). The natural antimicrobial Subtilosin A synergizes with lauramide arginine ethyl ester (LAE), e-Poly-L-lysine (Polylysine), clindamycin phosphate and metronidazole, against the vaginal pathogen Gardnerella vaginalis. Probiotics. Antimicrob. Proteins. 7, 164-171. doi: 10.1007/s12602-014-9183-1
28. Ceotto-Vigoder, H., Marques, S. L., Santos, I. N., Alves, M. D., Barrias, E. S., Potter, A., et al. (2016). Nisin and lysostaphin activity against preformed biofilm of Staphylococcus aureus involved in bovine mastitis. J. Appl. Microbiol. 121, 101-114. doi: 10.1111/jam.13136
29. Chambers, H. F., and Deleo, F. R. (2009). Waves of resistance: Staphylococcus aureus in the antibiotic era. Nat. Rev. Microbiol. 7, 629-641. doi: 10.1038/nrmicro2200
30. Chatterjee, C., Paul, M., Xie, L., and van der Donk, W. A. (2005). Biosynthesis and mode of action of lantibiotics. Chem. Rev. 105, 633-684. doi: 10.1021/cr030105v
31. Chatterjee, S., Chatterjee, D. K., Jani, R. H., Blumbach, J., Ganguli, B. N., Klesel, N., et al. (1992). Mersacidin, a new antibiotic from Bacillus: in vitro and in vivo antibacterial activity. J. Antibiot. 45, 839-845. doi: 10.7164/antibiotics.45.839
32. Chen, D., Liu, X., Yang, Y., Yang, H., and Lu, P. (2015). Systematic synergy modeling: understanding drug synergy from a systems biology perspective. BMC Syst. Biol. 9:56. doi: 10.1186/s12918-015-0202-y
33. Conrads, G., de Soet, J. J., Song, L., Henne, K., Sztajer, H., Wagner-Döbler, I., et al. (2014). Comparing the cariogenic species Streptococcus sobrinus and S. mutans on whole genome level. J. Oral Microbiol. 6:26189. doi: 10.3402/jom.v6.26189
34. Cooper, M. A., and Shlaes, D. (2011). Fix the antibiotics pipeline. Nature 472:32. doi: 10.1038/472032a
35. Cotter, P. D., Emerson, N., Gahan, C. G., and Hill, C. (1999). Identification and disruption of lisRK, a genetic locus encoding a two-component signal transduction system involved in stress tolerance and virulence in Listeria monocytogenes. J. Bacteriol. 181, 6840-6843
36. Cotter, P. D., Hill, C., and Ross, R. P. (2005). Bacteriocins: developing innate immunity for food. Nat. Rev. Microbiol. 3, 777-788. doi: 10.1038/nrmicro1273
37. Cotter, P. D., Ross, R. P., and Hill, C. (2013). Bacteriocins-a viable alternative to antibiotics? Nat. Rev. Microbiol. 11, 95-105. doi: 10.1038/nrmicro2937
38. Cox, C. R., Coburn, P. S., and Gilmore, M. S. (2005). Enterococcal cytolysin: a novel two component peptide system that serves as a bacterial defense against eukaryotic and prokaryotic cells. Curr. Protein Pept. Sci. 6, 77-84. doi: 10.2174/1389203053027557
39. Dabour, N., Zihler, A., Kheadr, E., Lacroix, C., and Fliss, I. (2009). In vivo study on the effectiveness of pediocin PA-1 and Pediococcus acidilactici UL5 at inhibiting Listeria monocytogenes. Int. J. Food Microbiol. 133, 225-233. doi: 10.1016/j.ijfoodmicro.2009.05.005
40. Dajcs, J. J., Thibodeaux, B. A., Girgis, D. O., Shaffer, M. D., Delvisco, S. M., and O'Callaghan, R. J. (2002). Immunity to lysostaphin and its therapeutic value for ocular MRSA infections in the rabbit. Investig. Ophthalmol. Vis. Sci. 43, 3712-3716
41. Davies, D. (2003). Understanding biofilm resistance to antibacterial agents. Nat. Rev. Drug Discov. 2, 114-122. doi: 10.1038/nrd1008
42. de Kwaadsteniet, M., Doeschate, K. T., and Dicks, L. M. (2009). Nisin F in the treatment of respiratory tract infections caused by Staphylococcus aureus. Lett. Appl. Microbiol. 48, 65-70. doi: 10.1111/j.1472-765X.2008.02488.x
43. Delves-Broughton, J. (1990). Nisin and its application as a food preservative. Int. J. Dairy Technol. 43, 73-76. doi: 10.1111/j.1471-0307.1990.tb02449.x
44. Doern, C. D. (2014). When does 2 plus 2 equal 5? A review of antimicrobial synergy testing. J. Clin. Microbiol. 52, 4124-4128. doi: 10.1128/JCM.01121-14
45. Dosler, S., and Gerceker, A. A. (2011). In vitro activities of nisin alone or in combination with vancomycin and ciprofloxacin against methicillin-resistant and methicillin-susceptible Staphylococcus aureus strains. Chemotherapy 57, 511-516. doi: 10.1159/000335598
46. Dosler, S., and Gerceker, A. A. (2012). In vitro activities of antimicrobial cationic peptides; melittin and nisin, alone or in combination with antibiotics against Gram-positive bacteria. J. Chemother. 24, 137-143. doi: 10.1179/1973947812Y.0000000007
47. Dosler, S., and Mataraci, E. (2013). In vitro pharmacokinetics of antimicrobial cationic peptides alone and in combination with antibiotics against methicillin resistant Staphylococcus aureus biofilms. Peptides 49, 53-58. doi: 10.1016/j.peptides.2013.08.008
48. Draper, L. A., Cotter, P. D., Hill, C., and Ross, R. P. (2013). The two peptide lantibiotic lacticin 3147 acts synergistically with polymyxin to inhibit Gram negative bacteria. BMC Microbiol. 13:212. doi: 10.1186/1471-2180-13-212
49. Draper, L. A., Cotter, P. D., Hill, C., and Ross, R. P. (2015). Lantibiotic resistance. Microbiol. Mol. Biol. Rev. 79, 171-191. doi: 10.1128/MMBR.00051-14
50. Drudy, D., Mullane, N. R., Quinn, T., Wall, P. G., and Fanning, S. (2006). Enterobacter sakazakii: an emerging pathogen in powdered infant formula. Clin. Infect. Dis. 42, 996-1002. doi: 10.1086/501019
51. Eijsink, V. G., Skeie, M., Middelhoven, P. H., Brurberg, M. B., and Nes, I. F. (1998). Comparative studies of class IIa bacteriocins of lactic acid bacteria. Appl. Environ. Microbiol. 64, 3275-3281
52. Ettayebi, K., El Yamani, J., and Rossi-Hassani, B. (2000). Synergistic effects of nisin and thymol on antimicrobial activities in Listeria monocytogenes and Bacillus subtilis. FEMS Microbiol. Lett. 183, 191-195. doi: 10.1111/j.1574-6968.2000.tb08956x
53. Field, D., Begley, M., O'Connor, P. M., Daly, K. M., Hugenholtz, F., Cotter, P. D., et al. (2012). Bioengineered nisin A derivatives with enhanced activity against both Gram positive and Gram negative pathogens. PLoS ONE 7:e46884. doi: 10.1371/journal.pone.0046884
54. Field, D., Connor, P. M., Cotter, P. D., Hill, C., and Ross, R. P. (2008). The generation of nisin variants with enhanced activity against specific Gram-positive pathogens. Mol. Microbiol. 69, 218-230. doi: 10.1111/j.1365-2958.2008.06279.x
55. Field, D., Daly, K., O'Connor, P. M., Cotter, P. D., Hill, C., and Ross, R. P. (2015). Efficacies of nisin A and nisin V semipurified preparations alone and in combination with plant essential oils for controlling Listeria monocytogenes. Appl. Environ. Microbiol. 81, 2762-2769. doi: 10.1128/AEM.00070-15
56. Field, D., O'Connor, R., Cotter, P. D., Ross, R. P., and Hill, C. (2016a). In vitro activities of nisin and nisin derivatives alone and in combination with antibiotics against Staphylococcus biofilms. Front. Microbiol. 7:508. doi: 10.3389/fmicb.2016.00508
57. Field, D., Seisling, N., Cotter, P. D., Ross, R. P., and Hill, C. (2016b). Synergistic Nisin-Polymyxin combinations for the control of Pseudomonas biofilm formation. Front. Microbiol. 7:1713. doi: 10.3389/fmicb.2016.01713
58. Fleming, D. W., Cochi, S. L., MacDonald, K. L., Brondum, J., Hayes, P. S., Plikaytis, B. D., et al. (1985). Pasteurized milk as a vehicle of infection in an outbreak of listeriosis. N. Engl. J. Med. 312, 404-407. doi: 10.1056/NEJM198502143120704
59. Flemming, H. C., and Wingender, J. (2010). The biofilm matrix. Nat. Rev. Micro. 8, 623-633. doi: 10.1038/nrmicro2415
60. Flores-Mireles, A. L., Walker, J. N., Caparon, M., and Hultgren, S. J. (2015). Urinary tract infections: epidemiology, mechanisms of infection and treatment options. Nat. Rev. Microbiol. 13, 269-284. doi: 10.1038/nrmicro3432
61. Foweraker, J. E., Laughton, C. R., Brown, D. F., and Bilton, D. (2009). Comparison of methods to test antibiotic combinations against heterogeneous populations of multiresistant Pseudomonas aeruginosa from patients with acute infective exacerbations in cystic fibrosis. Antimicrob. Agents Chemother. 53, 4809-4815. doi: 10.1128/AAC.00269-09
62. García, P., Martínez, B., Rodríguez, L., and Rodríguez, A. (2010). Synergy between the phage endolysin LysH5 and nisin to kill Staphylococcus aureus in pasteurized milk. Int. J. Food Microbiol. 141, 151-155. doi: 10.1016/j.ijfoodmicro.2010.04.029
63. Gellatly, S. L., and Hancock, R. E. (2013). Pseudomonas aeruginosa: new insights into pathogenesis and host defenses. Pathog. Dis. 67, 159-173. doi: 10.1111/2049-632X.12033
64. Ghalfi, H., Benkerroum, N., Doguiet, D. D., Bensaid, M., and Thonart, P. (2007). Effectiveness of cell-adsorbed bacteriocin produced by Lactobacillus curvatus CWBI-B28 and selected essential oils to control Listeria monocytogenes in pork meat during cold storage. Lett. Appl. Microbiol. 44, 268-273. doi: 10.1111/j.1472-765X.2006.02077.x
65. Ghobrial, O., Derendorf, H., and Hillman, J. D. (2010a). Pharmacokinetic and pharmacodynamic evaluation of the lantibiotic MU1140. J. Pharm. Sci. 99, 2521-2528. doi: 10.1002/jps.22015
66. Ghobrial, O., Derendorf, H., and Hillman, J. D. (2010b). Human serum binding and its effect on the pharmacodynamics of the lantibiotic MU1140. Eur. J. Pharm. Sci. 41, 658-664. doi: 10.1016/j.ejps.2010.09.005
67. Ghobrial, O. G., Derendorf, H., and Hillman, J. D. (2009). Development and validation of a LC-MS quantification method for the lantibiotic MU1140 in rat plasma. J. Pharm. Biomed. Anal. 49, 970-975. doi: 10.1016/j.jpba.2008.12.022
68. Giacometti, A., Cirioni, O., Barchiesi, F., Fortuna, M., and Scalise, G. (1999). In vitro activity of cationic peptides alone and in combination with clinically used antimicrobial agents against Pseudomonas aeruginosa. J. Antimicrob. Chemother. 44, 641-645
69. Gill, A. O., and Holley, R. A. (2006a). Disruption of Escherichia coli, Listeria monocytogenes and Lactobacillus sakei cellular membranes by plant oil aromatics. Int. J. Food Microbiol. 108, 1-9. doi: 10.1016/j.ijfoodmicro.2005.10.009
70. Gill, A. O., and Holley, R. A. (2006b). Inhibition of membrane bound ATPases of Escherichia coli and Listeria monocytogenes by plant oil aromatics. Int. J. Food Microbiol. 111, 170-174. doi: 10.1016/j.ijfoodmicro.2006.04.046
71. Goyette-Desjardins, G., Auger, J. P., Xu, J., Segura, M., and Gottschalk, M. (2014). Streptococcus suis, an important pig pathogen and emerging zoonotic agent-an update on the worldwide distribution based on serotyping and sequence typing. Emerg. Microbes Infect. 3:e45. doi: 10.1038/emi.2014.45
72. Grande, M. J., López, R. L., Abriouel, H., Valdivia, E., Ben Omar, N., Maqueda, M., et al. (2007). Treatment of vegetable sauces with enterocin AS-48 alone or in combination with phenolic compounds to inhibit proliferation of Staphylococcus aureus. J. Food Prot. 70, 405-411
73. Gravesen, A., Ramnath, M., Rechinger, K. B., Andersen, N., Jänsch, L., Héchard, Y., et al. (2002). High-level resistance to class IIa bacteriocins is associated with one general mechanism in Listeria monocytogenes. Microbiology 48, 2361-2369. doi: 10.1099/00221287-148-8-2361
74. Grönthal, T., Moodley, A., Nykäsenoja, S., Junnila, J., Guardabassi, L., Thomson, K., et al. (2014). Large outbreak caused by methicillin resistant Staphylococcus pseudintermedius ST71 in a Finnish veterinary teaching hospital-from outbreak control to outbreak prevention. PLoS ONE 9:e110084. doi: 10.1371/journal.pone.0110084
75. Gurtler, J. B., Kornacki, J. L., and Beuchat, L. R. (2005). Enterobacter sakazakii: a coliform of increased concern to infant health. Int. J. Food Microbiol. 104, 1-34. doi: 10.1016/j.ijfoodmicro.2005.02.013
76. Hackbarth, C. J., Kocagoz, T., Kocagoz, S., and Chambers, H. F. (1995). Point mutations in Staphylococcus aureus PBP 2 gene affect penicillin-binding kinetics and are associated with resistance. Antimicrob. Agents Chemother. 39, 103-106
77. Hanchi, H., Hammami, R., Gingras, H., Kourda, R., Bergeron, M. G., Ben Hamida, J., et al. (2017). Inhibition of MRSA and of Clostridium difficile by durancin 61A: synergy with bacteriocins and antibiotics. Future Microbiol. 12, 205-212. doi: 10.2217/fmb-2016-0113
78. Héchard, Y., and Sahl, H. G. (2002). Mode of action of modified and unmodified bacteriocins from Gram-positive bacteria. Biochimie 84, 545-557. doi: 10.1016/S0300-9084(02)01417-7
79. Helander, I. M., Alakomi, H. L., Latva-Kala, K., Mattila-Sandholm, T., Pol, I., Smid, E. J., et al. (1998). Characterization of the action of selected essential oil components on Gram-negative bacteria. J. Agric. Food Chem. 46, 3590-3595. doi: 10.1021/jf980154m
80. Holmes, A. H., Moore, L. S., Sundsfjord, A., Steinbakk, M., Regmi, S., Karkey, A., et al. (2016). Understanding the mechanisms and drivers of antimicrobial resistance. Lancet 387, 176-187. doi: 10.1016/S0140-6736(15)00473-0
81. Hughes, J. M., Wilson, M. E., Wertheim, H. F. L., Trung Nghia, H. D., Taylor, W., and Schultsz, C. (2009). Streptococcus suis: an emerging human pathogen. Clin. Infect. Dis. 48, 617-625. doi: 10.1086/596763
82. Huong, V. T., Ha, N., Huy, N. T., Horby, P., Nghia, H. D., Thiem, V. D., et al. (2014). Epidemiology, clinical manifestations, and outcomes of Streptococcus suis infection in humans. Emerg. Infect. Dis. 20, 1105-1114. doi: 10.3201/eid2007.131594
83. Hussain, M. A., and Dawson, C. O. (2013). Economic impact of food safety outbreaks on food businesses. Foods 2, 585-589. doi: 10.3390/foods2040585
84. Iversen, C., and Forsythe, S. J. (2007). Comparison of media for the isolation of Enterobacter sakazakii. Appl. Environ. Microbiol. 73, 48-52. doi: 10.1128/AEM.01562-06
85. Jabes, D., Brunati, C., Candiani, G., Riva, S., Romano, G., and Donadio, S. (2011). Efficacy of the new lantibiotic NAI-107 in experimental infections induced by MDR Gram positive pathogens. Antimicrob. Agents Chemother. 55, 1671-1676. doi: 10.1128/AAC.01288-10
86. Johnston, L. M., and Jaykus, L.-A. (2004). Antimicrobial resistance of Enterococcus species isolated from produce. Appl. Environ. Microbiol. 70, 3133-3137. doi: 10.1128/AEM.70.5.3133-3137.2004
87. Kallipolitis, B. H., and Ingmer, H. (2001). Listeria monocytogenes response regulators important for stress tolerance and pathogenesis. FEMS Microbiol. Lett. 204, 111-115. doi: 10.1111/j.1574-6968.2001.tb10872.x
88. Khattar, Z. A., Rejasse, A., Destoumieux-Garzón, D., Escoubas, J., Sanchis, V., Lereclus, D., et al. (2009). The dlt operon of Bacillus cereus is required for resistance to cationic antimicrobial peptides and for virulence in insects. J. Bacteriol. 191, 7063-7073. doi: 10.1128/JB.00892-09
89. Khosa, S., Alkhatib, Z., and Smits, S. H. (2013). NSR from Streptococcus agalactiae confers resistance against nisin and is encoded by a conserved nsr operon. Biol. Chem. 394, 1543-1549. doi: 10.1515/hsz-2013-0167
90. Kim, J., and Sudbery, P. (2011). Candida albicans, a major human fungal pathogen. J. Microbiol. 49, 171-177. doi: 10.1007/s12275-011-1064-7
91. Kjos, M., Nes, I. F., and Diep, D. B. (2011). Mechanisms of resistance to bacteriocins targeting the mannose phosphotransferase system. Appl. Environ. Microbiol. 77, 3335-3342. doi: 10.1128/AEM.02602-10
92. Kovacs, M., Halfmann, A., Fedtke, I., Heintz, M., Peschel, A., Vollmer, W., et al. (2006). A functional dlt operon, encoding proteins required for incorporation of d-alanine in teichoic acids in gram-positive bacteria, confers resistance to cationic antimicrobial peptides in Streptococcus pneumoniae. J. Bacteriol. 188, 5797-5805. doi: 10.1128/JB.00336-06
93. Kruszewska, D., Sahl, H. G., Bierbaum, G., Pag, U., Hynes, S. O., and Ljungh, A. (2004). Mersacidin eradicates methicillin-resistant Staphylococcus aureus (MRSA) in a mouse rhinitis model. J. Antimicrob. Chemother. 54, 648-653. doi: 10.1093/jac/dkh387
94. Landersdorfer, C. B., Ly, N. S., Xu, H., Tsuji, B. T., and Bulitta, J. B. (2013).Quantifying subpopulation synergy for antibiotic combinations via mechanism-based modeling and a sequential dosing design. Antimicrob. Agents Chemother. 57, 2343-2351. doi: 10.1128/AAC.00092-13
95. LeBel, G., Piché, F., Frenette, M., Gottschalk, M., and Grenier, D. (2013). Antimicrobial activity of nisin against the swine pathogen Streptococcus suis and its synergistic interaction with antibiotics. Peptides 50, 19-23. doi: 10.1016/j.peptides.2013.09.014
96. Leffler, D. A., and Lamont, J. T. (2015). Clostridium difficile infection. N. Engl. J. Med. 73, 287-288. doi: 10.1056/NEJMc1506004
97. Ling, L. L., Schneider, T., Peoples, A. J., Spoering, A. L., Engels, I., Conlon, B. P., et al. (2015). A new antibiotic kills pathogens without detectable resistance. Nature 517, 455-459. doi: 10.1038/nature14098
98. Lobos, O., Padilla, A., and Padilla, C. (2009). In vitro antimicrobial effect of bacteriocin PsVP-10 in combination with chlorhexidine and triclosan against Streptococcus mutans and Streptococcus sobrinus strains. Arch. Oral Biol. 54, 230-234. doi: 10.1016/j.archoralbio.2008.11.007
99. Loesche, W. J. (1986). Role of Streptococcus mutans in human dental decay. Microbiol. Rev. 50, 353-380
100. Low, J. C., and Donachie, W. (1997). A review of Listeria monocytogenes and listeriosis. Vet. J. 153, 9-29. doi: 10.1016/S1090-0233(97)80005-6
101. Mah, T. F., and O'Toole, G. A. (2001). Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol. 9, 34-39. doi: 10.1016/S0966-842X(00)01913-2
102. Maher, S., and McClean, S. (2006). Investigation of the cytotoxicity of eukaryotic and prokaryotic antimicrobial peptides in intestinal epithelial cells in vitro. Biochem. Pharmacol. 71, 1289-1298. doi: 10.1016/j.bcp.2006.01.012
103. Martínez, B., Obeso, J. M., Rodríguez, A., and García, P. (2008). Nisin-bacteriophage cross resistance in Staphylococcus aureus. Int. J. Food Microbiol. 122, 253-258. doi: 10.1016/j.ijfoodmicro.2008.01.011
104. Mataraci, E., and Dosler, S. (2012). In vitro activities of antibiotics and antimicrobial cationic peptides alone and in combination against methicillin-resistant Staphylococcus aureus biofilms. Antimicrob. Agents Chemother. 56, 6366-6371. doi: 10.1128/AAC.01180-12
105. Mathur, H., O'Connor, P. M., Hill, C., Cotter, P. D., and Ross, R. P. (2013). Analysis of anti-Clostridium difficile activity of thuricin CD, vancomycin, metronidazole, ramoplanin, and actagardine, both singly and in paired combinations. Antimicrob. Agents Chemother. 57, 2882-2886. doi: 10.1128/AAC.00261-13
106. Mathur, H., Rea, M. C., Cotter, P. D., Hill, C., and Ross, R. P. (2015). The sactibiotic subclass of bacteriocins: an update. Curr. Protein Pept. Sci. 16, 549-558. doi: 10.2174/1389203716666150515124831
107. Mazzotta, A. S., and Montville, T. J. (1997). Nisin induces changes in membrane fatty acid composition of Listeria monocytogenes nisin-resistant strains at 10°C and 30°C. J. Appl. Microbiol. 82, 32-38. doi: 10.1111/j.1365-2672.1997.tb03294.x
108. McAuliffe, O., Ryan, M. P., Ross, R. P., Hill, C., Breeuwer, P., and Abee, T. (1998). Lacticin 3147, a broad-spectrum bacteriocin which selectively dissipates the membrane potential. Appl. Environ. Microbiol. 64, 439-445
109. McBride, S. M., and Sonenshein, A. L. (2011a). The dlt operon confers resistance to cationic antimicrobial peptides in Clostridium difficile. Microbiology 157, 1457-1465. doi: 10.1099/mic.0.045997-0
110. McBride, S. M., and Sonenshein, A. L. (2011b). Identification of a genetic locus responsible for antimicrobial peptide resistance in Clostridium difficile. Infect. Immun. 79, 167-176. doi: 10.1128/IAI.00731-10
111. Mendes, C. A., Cordeiro, J. A., and Burdmann, E. A. (2009). Prevalence and risk factors for acute kidney injury associated with parenteral polymyxin B use. Ann. Pharmacother. 43, 1948-1955. doi: 10.1345/aph.1M277
112. Metwalli, K. H., Khan, S. A., Krom, B. P., and Jabra-Rizk, M. A. (2013). Streptococcus mutans, Candida albicans, and the human mouth: a sticky situation. PLoS Pathog. 9:e1003616. doi: 10.1371/journal.ppat.1003616
113. Michael, C. A., Dominey-Howes, D., and Labbate, M. (2014). The antimicrobial resistance crisis: causes, consequences, and management. Front. Public Health. 2:145. doi: 10.3389/fpubh.2014.00145
114. Ming, L., Zhang, Q., Yang, L., and Huang, J. A. (2015). Comparison of antibacterial effects between antimicrobial peptide and bacteriocins isolated from Lactobacillus plantarum on three common pathogenic bacteria. Int. J. Clin. Exp. Med. 8, 5806-5811
115. Modi, K. D., Chikindas, M. L., and Montville, T. J. (2000). Sensitivity of nisin-resistant Listeria monocytogenes to heat and the synergistic action of heat and nisin. Lett. Appl. Microbiol. 30, 249-253. doi: 10.1046/j.1472-765x.2000.00708.x
116. Montanari, M. P., Massidda, O., Mingoia, M., and Varaldo, P. E. (1996). Borderline susceptibility to methicillin in Staphylococcus aureus: a new mechanism of resistance? Microb. Drug Resist. 2, 257-260. doi: 10.1089/mdr.1996.2.257
117. Moon, G. S., Kim, W. J., and Kim, M. (2002). Synergistic effects of bacteriocin-producing Pediococcus acidilactici K10 and organic acids on inhibiting Escherichia coli O157:H7 and applications in ground beef. J. Microbiol. Biotechnol. 12, 936-942
118. Mota-Meira, M., LaPointe, G., Lacroix, C., and Lavoie, M. C. (2000). MICs of mutacin B-Ny266, nisin A, vancomycin, and oxacillin against bacterial pathogens. Antimicrob. Agents Chemother. 44, 24-29. doi: 10.1128/AAC.44.1.24-29.2000
119. Murdock, C. A., Cleveland, J., Matthews, K. R., and Chikindas, M. L. (2007). The synergistic effect of nisin and lactoferrin on the inhibition of Listeria monocytogenes and Escherichia coli O157:H7. Lett. Appl. Microbiol. 44, 255-261. doi: 10.1111/j.1472-765X.2006.02076.x
120. Murray, B. E. (1990). The life and times of the Enterococcus. Clin. Microbiol. Rev. 3, 46-65. doi: 10.1128/CMR.3.1.46
121. Naghmouchi, K., Baah, J., Hober, D., Jouy, E., Rubrecht, C., Sané, F., et al. (2013). 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, 2719-2725. doi: 10.1128/AAC.02328-12
122. Naghmouchi, K., Belguesmia, Y., Baah, J., Teather, R., and Drider, D. (2011). Antibacterial activity of class I and IIa bacteriocins combined with polymyxin E against resistant variants of Listeria monocytogenes and Escherichia coli. Res. Microbiol. 162, 99-107. doi: 10.1016/j.resmic.2010.09.014
123. Nascimento, J. G., Guerreiro-Pereira, M. D., Costa, S. F., São-José, C., and Santos, M. A. (2008). Nisin-triggered activity of Lys44, the secreted endolysin from Oenococcus oeni phage fOg44. J. Bacteriol. 190, 457-461. doi: 10.1128/JB.01195-07
124. Navaratna, M. A., Sahl, H. G., and Tagg, J. R. (1998). Two-component anti-Staphylococcus aureus lantibiotic activity produced by Staphylococcus aureus C55. Appl. Environ. Microbiol. 64, 4803-4808
125. Ndoti-Nembe, A., Vu, K. D., Doucet, N., and Lacroix, M. (2013). Effect of combination of essential oils and bacteriocins on the efficacy of gamma radiation against Salmonella Typhimurium and Listeria monocytogenes. Int. J. Radiat. Biol. 89, 794-800. doi: 10.3109/09553002.2013.797621
126. Nelson, K., Fouts, D., Mongodin, E., Ravel, J., DeBoy, R., Kolonay, J., et al. (2004). Whole genome comparisons of serotype 4b and 1/2a strains of the food-borne pathogen Listeria monocytogenes reveal new insights into the core genome components of this species. Nucleic Acids Res. 32, 2386-2395. doi: 10.1093/nar/gkh562
127. Noll, K. S., Prichard, M. N., Khaykin, A., Sinko, P. J., and Chikindas, M. L. (2012). The natural antimicrobial peptide subtilosin acts synergistically with glycerol monolaurate, lauric arginate, and e-poly-L-lysine against bacterial vaginosis-associated pathogens but not human lactobacilli. Antimicrob. Agents Chemother. 56, 1756-1761. doi: 10.1128/AAC.05861-11
128. Obeso, J. M., Martínez, B., Rodríguez, A., and García, P. (2008). Lytic activity of the recombinant staphylococcal bacteriophage phiH5 endolysin active against Staphylococcus aureus in milk. Int. J. Food Microbiol. 128, 212-218. doi: 10.1016/j.ijfoodmicro.2008.08.010
129. O'Driscoll, J., Glynn, F., Fitzgerald, G. F., and van Sinderen, D. (2006). Sequence analysis of the lactococcal plasmid pNP40: a mobile replicon for coping with environmental hazards. J. Bacteriol. 188, 6629-6639. doi: 10.1128/JB.00672-06
130. O'Flaherty, S., Coffey, A., Meaney, W., Fitzgerald, G. F., and Ross, R. P. (2005). The recombinant phage lysin LysK has a broad spectrum of lytic activity against clinically relevant staphylococci, including methicillin-resistant Staphylococcus aureus. J. Bacteriol. 187, 7161-7164. doi: 10.1128/JB.187.20.7161-7164.2005
131. Oppegård, C., Rogne, P., Emanuelsen, L., Kristiansen, P. E., Fimland, G., and 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
132. Orhan, G., Bayram, A., Zer, Y., and Balci, I. (2005). Synergy tests by E test and checkerboard methods of antimicrobial combinations against Brucella melitensis. J. Clin. Microbiol. 43, 140-143. doi: 10.1128/JCM.43.1.140-143.2005
133. Pena-Miller, R., Laehnemann, D., Jansen, G., Fuentes-Hernandez, A., Rosenstiel, P., Schulenburg, H., et al. (2013). When the most potent combination of antibiotics selects for the greatest bacterial load: the smile-frown transition. PLoS Biol. 11:e1001540. doi: 10.1371/journal.pbio.1001540
134. Peschel, A., Otto, M., Jack, R. W., Kalbacher, H., Jung, G., and Gotz, F. (1999). Inactivation of the dlt operon in Staphylococcus aureus confers sensitivity to defensins, protegrins, and other antimicrobial peptides. J. Biol. Chem. 274, 8405-8410. doi: 10.1074/jbc.274.13.8405
135. Piper, C., Draper, L. A., Cotter, P. D., Ross, R. P., and Hill, C. (2009). A comparison of the activities of lacticin 3147 and nisin against drug-resistant Staphylococcus aureus and Enterococcus species. J. Antimicrob. Chemother. 64, 546-551. doi: 10.1093/jac/dkp221
136. Poyart, C., Lamy, M. C., Boumaila, C., Fiedler, F., and Trieu-Cuot, P. (2001). Regulation of d-alanyl-lipoteichoic acid biosynthesis in Streptococcus agalactiae involves a novel two-component regulatory system. J. Bacteriol. 183, 6324-6334. doi: 10.1128/JB.183.21.6324-6334.2001
137. Pucci, M. J., Vedamuthu, E. R., Kunka, B. S., and Vandenbergh, P. A. (1988). Inhibition of Listeria monocytogenes by using bacteriocin PA-1 produced by Pediococcus acidilactici PAC 1.0. Appl. Environ. Microbiol. 54, 2349-2353
138. Rea, M. C., Clayton, E., O'Connor, P. M., Shanahan, F., Kiely, B., Ross, R. P., et al. (2007). Antimicrobial activity of lacticin 3147 against clinical Clostridium difficile strains. J. Med. Microbiol. 56, 940-946. doi: 10.1099/jmm.0.47085-0
139. Rea, M. C., Sit, C. S., Clayton, E., O'Connor, P. M., Whittal, R. M., Zheng, J., et al. (2010). Thuricin, C. D., a posttranslationally modified bacteriocin with a narrow spectrum of activity against Clostridium difficile. Proc. Natl. Acad. Sci. U.S.A. 107, 9352-9357. doi: 10.1073/pnas.0913554107
140. Reen, F. J., Flynn, S., Woods, D. F., Dunphy, N., Chróinín, M. N., Mullane, D., et al. (2016). Bile signalling promotes chronic respiratory infections and antibiotic tolerance. Sci. Rep. 6:29768. doi: 10.1038/srep29768
141. Rishi, P., Preet Singh, A., Garg, N., and Rishi, M. (2014). Evaluation of nisin-β-lactam antibiotics against clinical strains of Salmonella enterica serovar Typhi. J. Antibiot. (Tokyo) 67, 807-811. doi: 10.1038/ja.2014.75
142. Rodríguez-Rubio, L., García, P., Rodríguez, A., Billington, C., Hudson, J. A., and Martínez, B. (2015). Listeriaphages and coagulin C23 act synergistically to kill Listeria monocytogenes in milk under refrigeration conditions. Int. J. Food. Microbiol. 205, 68-72. doi: 10.1016/j.ijfoodmicro.2015.04.007
143. Rollema, H. S., Kuipers, O. P., Both, P., de Vos, W. M., and Siezen, R. J. (1995). Improvement of solubility and stability of the antimicrobial peptide nisin by protein engineering. Appl. Environ. Microbiol. 61, 2873-2878
144. Schaefer, L., Auchtung, T. A., Hermans, K. E., Whitehead, D., Borhan, B., and Britton, R. A. (2010). The antimicrobial compound reuterin (3-hydroxypropionaldehyde) induces oxidative stress via interaction with thiol groups. Microbiology 156, 1589-1599. doi: 10.1099/mic.0.035642-0
145. Schoeni, J. L., and Wong, A. C. (2005). Bacillus cereus food poisoning and its toxins. J. Food Prot. 68, 636-648. doi: 10.4315/0362-028X-68.3.636
146. Schuppler, M., and Loessner, M. J. (2010). The opportunistic pathogen Listeria monocytogenes: pathogenicity and interaction with the mucosal immune system. Int. J. Inflam. 2010:704321. doi: 10.4061/2010/704321
147. Sharma, A., and Srivastava, S. (2014). Anti-Candida activity of two-peptide bacteriocins, plantaricins (Pln E/F and J/K) and their mode of action. Fungal Biol. 118, 264-275. doi: 10.1016/j.funbio.2013.12.006
148. Singh, A. P., Prabha, V., and Rishi, P. (2013). Value addition in the efficacy of conventional antibiotics by Nisin against Salmonella. PLoS ONE 8:e76844. doi: 10.1371/journal.pone.0076844
149. Singh, A. P., Preet, S., and Rishi, P. (2014). Nisin/β-lactam adjunct therapy against Salmonella enterica serovar Typhimurium: a mechanistic approach. J. Antimicrob. Chemother. 69, 1877-1887. doi: 10.1093/jac/dku049
150. Sivarooban, T., Hettiarachchy, N. S., and Johnson, M. G. (2008). Transmission electron microscopy study of Listeria monocytogenes treated with nisin in combination with either grape seed or green tea extract. J. Food Prot. 71, 2105-2109
151. Smith, M. K., Draper, L. A., Hazelhoff, P. J., Cotter, P. D., Ross, R. P., and Hill, C. (2016). A Bioengineered Nisin derivative, M21A, in combination with good grade additives eradicates biofilms of Listeria monocytogenes. Front. Microbiol. 7:1939. doi: 10.3389/fmicb.2016.01939
152. Soltani, R., Khalili, H., and Shafiee, F. (2012). Double-disk synergy test for detection of synergistic effect between antibiotics against nosocomial strains of Staphylococcus aureus. J. Res. Pharm Pract. 1, 21-24. doi: 10.4103/2279-042X.99673
153. Sopirala, M. M., Mangino, J. E., Gebreyes, W. A., Biller, B., Bannerman, T., Balada-Llasat, J. M., et al. (2010). Synergy testing by Etest, microdilution checkerboard, and time-kill methods for pan-drug-resistant Acinetobacter baumannii. Antimicrob. Agents Chemother. 54, 4678-4683. doi: 10.1128/AAC.00497-10
154. Stapleton, P. D., and Taylor, P. W. (2002). Methicillin resistance in Staphylococcus aureus: mechanisms and modulation. Sci. Prog. 85, 57-72. doi: 10.3184/003685002783238870
155. Stevens, K. A., Sheldon, B. W., Klapes, N. A., and Klaenhammer, T. R. (1991). Nisin treatment for inactivation of Salmonella species and other Gram-negative bacteria. Appl. Environ. Microbiol. 57, 3613-3615
156. Suarez, J. M., Edwards, A. N., and McBride, S. M. (2013). The Clostridium difficile cpr locus is regulated by a noncontiguous two-component system in response to type A and B lantibiotics. J. Bacteriol. 195, 2621-2631. doi: 10.1128/JB.00166-13
157. Tang, J., Wennerberg, K., and Aittokallio, T. (2015). What is synergy? The Saariselkä agreement revisited. Front. Pharmacol. 6:181. doi: 10.3389/fphar.2015.00181
158. Tong, Z., Ling, J., Lin, Z., Li, X., and Mu, Y. (2013). The effect of MTADN on 10 Enterococcus faecalis isolates and biofilm: an in vitro study. J. Endod. 39, 674-678. doi: 10.1016/j.joen.2012.12.010
159. Tong, Z., Zhang, L., Ling, J., Jian, Y., Huang, L., and Deng, D. (2014b). An in vitro study on the effect of free amino acids alone or in combination with nisin on biofilms as well as on planktonic bacteria of Streptococcus mutans. PLoS ONE 9:e99513. doi: 10.1371/journal.pone.0099513
160. Tong, Z., Zhang, Y., Ling, J., Ma, J., Huang, L., and Zhang, L. (2014a). In vitro study on the effects of Nisin on the antibacterial activities of 18 antibiotics against Enterococcus faecalis. PLoS ONE 9:e89209. doi: 10.1371/journal.pone.0089209
161. Tong, Z., Zhou, L., Jiang, W., Kuang, R., Li, J., Tao, R., et al. (2011). An in vitro synergetic evaluation of the use of nisin and sodium fluoride or chlorhexidine against Streptococcus mutans. Peptides. 32, 2021-2026. doi: 10.1016/j.peptides.2011.09.002
162. Torella, J. P., Chait, R., and Kishony, R. (2010). Optimal drug synergy in antimicrobial treatments. PLoS Comput. Biol. 6:e1000796. doi: 10.1371/journal.pcbi.1000796
163. Tsuji, B. T., and Rybak, M. J. (2006). Etest synergy testing of clinical isolates of Staphylococcus aureus demonstrating heterogeneous resistance to vancomycin. Diagn. Microbiol. Infect. Dis. 54, 73-77. doi: 10.1016/j.diagmicrobio.2005.08.014
164. Vaillancourt, K., LeBel, G., Frenette, M., Gottschalk, M., and Grenier, D. (2015). Suicin 3908, a new lantibiotic produced by a strain of Streptococcus suis serotype 2 isolated from a healthy carrier pig. PLoS ONE 10:e0117245. doi: 10.1371/journal.pone.0117245
165. van Duijkeren, E., Catry, B., Greko, C., Moreno, M. A., Pomba, M. C., Pyörälä, S., et al. (2011). Review on methicillin-resistant Staphylococcus pseudintermedius. J. Antimicrob. Chemother. 66, 2705-2714. doi: 10.1093/jac/dkr367
166. van Heel, A. J., Montalban-Lopez, M., and Kuipers, O. P. (2011). Evaluating the feasibility of lantibiotics as an alternative therapy against bacterial infections in humans. Expert Opin. Drug Metab. Toxicol. 7, 675-680. doi: 10.1517/17425255.2011.573478
167. Van Hoovels, L., Vankeerberghen, A., Boel, A., Van Vaerenbergh, K., and De Beenhouwer, H. (2006). First case of Staphylococcus pseudintermedius infection in a human. J. Clin. Microbiol. 44, 4609-4612. doi: 10.1128/JCM.01308-06
168. Vidovic, S., and Korber, D. R. (2016). Escherichia coli O157: Insights into the adaptive stress physiology and the influence of stressors on epidemiology and ecology of this human pathogen. Crit. Rev. Microbiol. 42, 83-93. doi: 10.3109/1040841X.2014.889654
169. Wan Norhana, M. N., Poole, S. E., Deeth, H. C., and Dykes, G. A. (2012). Effects of nisin, EDTA and salts of organic acids on Listeria monocytogenes, Salmonella and native microflora on fresh vacuum packaged shrimps stored at 4°C. Food Microbiol. 31, 43-50. doi: 10.1016/j.fm.2012.01.007
170. Willing, B. P., Russell, S. L., and Finlay, B. B. (2011). Shifting the balance: antibiotic effects on host-microbiota mutualism. Nat. Rev. Microbiol. 9, 233-243. doi: 10.1038/nrmicro2536
171. Xie, L., Miller, L. M., Chatterjee, C., Averin, O., Kelleher, N. L., and van der Donk, W. A. (2004). Lacticin 481: in vitro reconstitution of lantibiotic synthetase activity. Science 303, 679-681. doi: 10.1126/science.1092600
172. Yan, Q. Q., Condell, O., Power, K., Butler, F., Tall, B. D., and Fanning, S. (2012). Cronobacter species (formerly known as Enterobacter sakazakii) in powdered infant formula: a review of our current understanding of the biology of this bacterium. J. Appl. Microbiol. 113, 1-15. doi: 10.1111/j.1365-2672.2012.05281.x
173. Yuan, J., Zhang, Z. Z., Chen, X. Z., Yang, W., and Huan, L. D. (2004). Site-directed mutagenesis of the hinge region of nisinZ and properties of nisinZ mutants. Appl. Microbiol. Biotechnol. 64, 806-815. doi: 10.1007/s00253-004-1599-1