A single exposure to a sublethal pediocin concentration initiates a resistance-associated temporal cell envelope and general stress response in Listeria monocytogenes

Environmental Microbiology

Volumn 17, Issue 4, 2015, Pages 1134-1151

  Laursen, Martin F ^a   Bahl, Martin I ^a   Licht, Tine R ^a   Gram, Lone ^a   Knudsen, Gitte M ^a  

^a TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

LACTOBACILLUS; LISTERIA MONOCYTOGENES;

BACTERIOCIN; PEDIOCIN 5; SIGB PROTEIN, LISTERIA MONOCYTOGENES; SIGMA FACTOR;

ADAPTATION; ANTIBIOTIC RESISTANCE; CELL MEMBRANE; CELL WALL; DRUG EFFECTS; FOOD POISONING; GENETICS; HUMAN; LACTOBACILLUS PLANTARUM; LISTERIA MONOCYTOGENES; LISTERIOSIS; METABOLISM; MICROBIOLOGY; PHYSIOLOGICAL STRESS;

ADAPTATION, PHYSIOLOGICAL; BACTERIOCINS; CELL MEMBRANE; CELL WALL; DRUG RESISTANCE, BACTERIAL; FOODBORNE DISEASES; HUMANS; LACTOBACILLUS PLANTARUM; LISTERIA MONOCYTOGENES; LISTERIOSIS; SIGMA FACTOR; STRESS, PHYSIOLOGICAL;

EID: 84926416155     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/1462-2920.12534     Document Type: Article

References (71)

1. Abachin, E., Poyart, C., Pellegrini, E., Milohanic, E., Fiedler, F., Berche, P., and Trieu-Cuot, P. (2002) Formation of D-alanyl-lipoteichoic acid is required for adhesion and virulence of Listeria monocytogenes. Mol Microbiol 43: 1-14.
2. Arous, S., Buchrieser, C., Folio, P., Glaser, P., Namane, A., Hébraud, M., and Héchard, Y. (2004) Global analysis of gene expression in an rpoN mutant of Listeria monocytogenes. Microbiology 150: 1581-1590.
3. Baggerly, K.A., Deng, L., Morris, J.S., and Aldaz, C.M. (2003) Differential expression in SAGE: accounting for normal between-library variation. Bioinformatics 19: 1477-1483.
4. Begley, M., Hill, C., and Ross, R.P. (2006) Tolerance of Listeria monocytogenes to cell envelope-acting antimicrobial agents is dependent on SigB. Appl Environ Microbiol 72: 2231-2234.
5. Begley, M., Sleator, R.D., Gahan, C.G.M., and Hill, C. (2005) Contribution of three bile-associated loci, bsh, pva, and btlB, to gastrointestinal persistence and bile tolerance of Listeria monocytogenes. Infect Immun 73: 894-904.
6. Bergholz, T.M., Bowen, B., Wiedmann, M., and Boor, K.J. (2012) Listeria monocytogenes shows temperature-dependent and -independent responses to salt stress, including responses that induce cross-protection against other stresses. Appl Environ Microbiol 78: 2602-2612.
7. Bernbom, N., Jelle, B., Brogren, C.-H., Vogensen, F.K., Nørrung, B., and Licht, T.R. (2009) Pediocin PA-1 and a pediocin producing Lactobacillus plantarum strain do not change the HMA rat microbiota. Int J Food Microbiol 130: 251-257.
8. Boneca, I.G., Dussurget, O., Cabanes, D., Nahori, M.-A., Sousa, S., Lecuit, M., etal. (2007) A critical role for peptidoglycan N-deacetylation in Listeria evasion from the host innate immune system. Proc Natl Acad Sci USA 104: 997-1002.
9. Bowman, J.P., Lee Chang, K.J., Pinfold, T., and Ross, T. (2010) Transcriptomic and phenotypic responses of Listeria monocytogenes strains possessing different growth efficiencies under acidic conditions. Appl Environ Microbiol 76: 4836-4850.
10. Brøndsted, L., Kallipolitis, B.H., Ingmer, H., and Knöchel, S. (2003) kdpE and a putative RsbQ homologue contribute to growth of Listeria monocytogenes at high osmolarity and low temperature. FEMS Microbiol Lett 219: 233-239.
11. Brouwer, M.C., van de Beek, D., Heckenberg, S.G.B., Spanjaard, L., and de Gans, J. (2006) Community-acquired Listeria monocytogenes meningitis in adults. Clin Infect Dis 43: 1233-1238.
12. Chakraborty, T., Leimeister-Wachter, M., Domann, E., Hartl, M., Goebel, W., Nichterlein, T., and Notermans, S. (1992) Coordinate regulation of virulence genes in Listeria monocytogenes requires the product of the prfA gene. J Bacteriol 174: 568-574.
13. Collins, B., Curtis, N., Cotter, P.D., Hill, C., and Ross, R.P. (2010) The ABC transporter AnrAB contributes to the innate resistance of Listeria monocytogenes to nisin, bacitracin, and various beta-lactam antibiotics. Antimicrob Agents Chemother 54: 4416-4423.
14. Cotter, P.D., Guinane, C.M., and Hill, C. (2002) The LisRK signal transduction system determines the sensitivity of Listeria monocytogenes to nisin and cephalosporins. Antimicrob Agents Chemother 46: 2784-2790.
15. Cotter, P.D., Ross, R.P., and Hill, C. (2013) Bacteriocins - a viable alternative to antibiotics? Nat Rev Microbiol 11: 95-105.
16. 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.
17. 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.
18. 54-dependent PTS permease of the mannose family is responsible for sensitivity of Listeria monocytogenes to mesentericin Y105. Microbiology 147: 3263-3269.
19. Desvaux, M., Dumas, E., Chafsey, I., Chambon, C., and Hébraud, M. (2010) Comprehensive appraisal of the extracellular proteins from a monoderm bacterium: theoretical and empirical exoproteomes of Listeria monocytogenes EGD-e by secretomics. J Proteome Res 9: 5076-5092.
20. Ennahar, S., Assobhel, O., and Hasselmann, C. (1998) Inhibition of Listeria monocytogenes in a smear-surface soft cheese by Lactobacillus plantarum WHE 92, a pediocin AcH producer. J Food Prot 61: 186-191.
21. Ennahar, S., Aoude-Werner, D., Sorokine, O., Van Dorsselaer, A., Bringel, F., Hubert, J.C., and Hasselmann, C. (1996) Production of pediocin AcH by Lactobacillus plantarum WHE 92 isolated from cheese. Appl Environ Microbiol 62: 4381-4387.
22. Feehily, C., and Karatzas, K.A.G. (2013) Role of glutamate metabolism in bacterial responses towards acid and other stresses. J Appl Microbiol 114: 11-24.
23. Fritsch, F., Mauder, N., Williams, T., Weiser, J., Oberle, M., and Beier, D. (2010) The cell envelope stress response mediated by the LiaFSRLm three-component system of Listeria monocytogenes is controlled via the phosphatase activity of the bifunctional histidine kinase LiaSLm. Microbiology 157: 373-386.
24. Gálvez, A., Abriouel, H., López, R.L., and Ben Omar, N. (2007) Bacteriocin-based strategies for food biopreservation. Int J Food Microbiol 120: 51-70.
25. Gardan, R., Cossart, P., and Labadie, J. (2003) Identification of Listeria monocytogenes genes involved in salt and alkaline-pH tolerance. Appl Environ Microbiol 69: 3137-3143.
26. Gottschalk, S., Bygebjerg-Hove, I., Bonde, M., Nielsen, P.K., Nguyen, T.H., Gravesen, A., and Kallipolitis, B.H. (2008) The two-component system CesRK controls the transcriptional induction of cell envelope-related genes in Listeria monocytogenes in response to cell wall-acting antibiotics. J Bacteriol 190: 4772-4776.
27. Gravesen, A., Sørensen, K., Aarestrup, F.M., and Knøchel, S. (2001) Spontaneous nisin-resistant Listeria monocytogenes mutants with increased expression of a putative penicillin-binding protein and their sensitivity to various antibiotics. Microb Drug Resist 7: 127-135.
28. Gravesen, A., Jydegaard Axelsen, A.-M., Mendes da Silva, J., Hansen, T.B., and Knøchel, S. (2002) Frequency of bacteriocin resistance development and associated fitness costs in Listeria monocytogenes. Appl Environ Microbiol 68: 756-764.
29. Gravesen, A., Kallipolitis, B., Holmstrøm, K., Høiby, P.E., Ramnath, M., and Knøchel, S. (2004) pbp2229-mediated nisin resistance mechanism in Listeria monocytogenes confers cross-protection to class IIa bacteriocins and affects virulence gene expression. Appl Environ Microbiol 70: 1669-1679.
30. Hain, T., Hossain, H., Chatterjee, S.S., Machata, S., Volk, U., Wagner, S., etal. (2008) Temporal transcriptomic analysis of the Listeria monocytogenes EGD-e sigmaB regulon. BMC Microbiol 8: 20.
31. Hein-Kristensen, L., Franzyk, H., Holch, A., and Gram, L. (2013) Adaptive evolution of Escherichia coli to an α-peptide/β-peptoid peptidomimetic induces stable resistance. PLoS ONE 8: e73620.
32. Hughes, D., and Andersson, D.I. (2012) Selection of resistance at lethal and non-lethal antibiotic concentrations. Curr Opin Microbiol 15: 555-560.
33. + antiporter and insights into mechanism of action and regulation by pH. Nature 435: 1197-1202.
34. Katla, T., Naterstad, K., Vancanneyt, M., Swings, J., and Axelsson, L. (2003) Differences in susceptibility of Listeria monocytogenes strains to sakacin P, sakacin A, pediocin PA-1, and nisin. Appl Environ Microbiol 69: 4431-4437.
35. Kazmierczak, M.J., Mithoe, S.C., Boor, K.J., and Wiedmann, M. (2003) Listeria monocytogenes sigma B regulates stress response and virulence functions. J Bacteriol 185: 5722-5734.
36. 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.
37. Kjos, M., Salehian, Z., Nes, I.F., and Diep, D.B. (2010) An extracellular loop of the mannose phosphotransferase system component IIC is responsible for specific targeting by class IIa bacteriocins. J Bacteriol 192: 5906-5913.
38. Knudsen, G.M., Holch, A., and Gram, L. (2012) Subinhibitory concentrations of antibiotics affect stress and virulence gene expression in Listeria monocytogenes and cause enhanced stress sensitivity but do not affect Caco-2 cell invasion. J Appl Microbiol 113: 1273-1286.
39. Kohanski, M.A., DePristo, M.A., and Collins, J.J. (2010) Sublethal antibiotic treatment leads to multidrug resistance via radical-induced mutagenesis. Mol Cell 37: 311-320.
40. Larsen, C.N., Nørrung, B., Sommer, H.M., and Jakobsen, M. (2002) In vitro and in vivo invasiveness of different pulsed-field gel electrophoresis types of Listeria monocytogenes. Appl Environ Microbiol 68: 5698-5703.
41. Ledala, N., Sengupta, M., Muthaiyan, A., Wilkinson, B.J., and Jayaswal, R.K. (2010) Transcriptomic response of Listeria monocytogenes to iron limitation and Fur mutation. Appl Environ Microbiol 76: 406-416.
42. Linnan, M.J., Mascola, L., Lou, X.D., Goulet, V., May, S., Salminen, C., etal. (1988) Epidemic listeriosis associated with Mexican-style cheese. N Engl J Med 319: 823-828.
43. Loessner, M., Guenther, S., Steffan, S., and Scherer, S. (2003) A pediocin-producing Lactobacillus plantarum strain inhibits Listeria monocytogenes in a multispecies cheese surface microbial ripening consortium. Appl Environ Microbiol 69: 1854-1857.
44. Mandin, P., Fsihi, H., Dussurget, O., Vergassola, M., Milohanic, E., Toledo-Arana, A., etal. (2005) VirR, a response regulator critical for Listeria monocytogenes virulence. Mol Microbiol 57: 1367-1380.
45. Mattila, M., Somervuo, P., Rattei, T., Korkeala, H., Stephan, R., and Tasara, T. (2012) Phenotypic and transcriptomic analyses of Sigma L-dependent characteristics in Listeria monocytogenes EGD-e. Food Microbiol 32: 152-164.
46. Medema, M.H., Blin, K., Cimermancic, P., de Jager, V., Zakrzewski, P., Fischbach, M.A., etal. (2011) antiSMASH: rapid identification, annotation and analysis of secondary metabolite biosynthesis gene clusters in bacterial and fungal genome sequences. Nucleic Acids Res 39: 339-346.
47. Milillo, S.R., Friedly, E.C., Saldivar, J.C., Muthaiyan, A., O'Bryan, C., Crandall, P.G., etal. (2012) A review of the ecology, genomics, and stress response of Listeria innocua and Listeria monocytogenes. Crit Rev Food Sci Nutr 52: 712-725.
48. Miller, K.W., Ray, P., Steinmetz, T., Hanekamp, T., and Ray, B. (2005) Gene organization and sequences of pediocin AcH/PA-1 production operons in Pediococcus and Lactobacillus plasmids. Lett Appl Microbiol 40: 56-62.
49. Moorhead, S.M., and Dykes, G.A. (2003) The role of the sigB gene in the general stress response of Listeria monocytogenes varies between a strain of serotype 1/2a and a strain of serotype 4c. Curr Microbiol 46: 461-466.
50. Mylonakis, E., Paliou, M., Hohmann, E.L., Calderwood, S.B., and Wing, E.J. (2002) Listeriosis during pregnancy: a case series and review of 222 cases. Medicine (Baltimore) 81: 260-269.
51. Nielsen, P.K., Andersen, A.Z., Mols, M., van der Veen, S., Abee, T., and Kallipolitis, B.H. (2012) Genome-wide transcriptional profiling of the cell envelope stress response and the role of LisRK and CesRK in Listeria monocytogenes. Microbiology 158: 963-974.
52. Oliver, H.F., Orsi, R.H., Ponnala, L., Keich, U., Wang, W., Sun, Q., etal. (2009) Deep RNA sequencing of L. monocytogenes reveals overlapping and extensive stationary phase and sigma B-dependent transcriptomes, including multiple highly transcribed noncoding RNAs. BMC Genomics 10: 641.
53. L contribute to Listeria monocytogenes 10403S response to the antimicrobial peptides SdpC and nisin. Foodborne Pathog Dis 6: 1057-1065.
54. Raengpradub, S., Wiedmann, M., and Boor, K.J. (2008) Comparative analysis of the sigma B-dependent stress responses in Listeria monocytogenes and Listeria innocua strains exposed to selected stress conditions. Appl Environ Microbiol 74: 158-171.
55. 54) gene from Listeria monocytogenes is involved in resistance to mesentericin Y105, an antibacterial peptide from Leuconostoc mesenteroides. J Bacteriol 179: 7591-7594.
56. Rodríguez, J.M., Martínez, M.I., and Kok, J. (2002) Pediocin PA-1, a wide-spectrum bacteriocin from lactic acid bacteria. Crit Rev Food Sci Nutr 42: 91-121.
57. Salamina, G., Dalle Donne, E., Niccolini, A., Poda, G., Cesaroni, D., Bucci, M., etal. (1996) A foodborne outbreak of gastroenteritis involving Listeria monocytogenes. Epidemiol Infect 117: 429-436.
58. T method. Nat Protoc 3: 1101-1108.
59. Seifart Gomes, C., Izar, B., Pazan, F., Mohamed, W., Mraheil, M.A., Mukherjee, K., etal. (2011) Universal stress proteins are important for oxidative and acid stress resistance and growth of Listeria monocytogenes EGD-e in vitro and in vivo. PLoS ONE 6: e24965.
60. Sleator, R.D., and Hill, C. (2005) A novel role for the LisRK two-component regulatory system in listerial osmotolerance. Clin Microbiol Infect 11: 599-601.
61. Tessema, G.T., Møretrø, T., Kohler, A., Axelsson, L., and Naterstad, K. (2009) Complex phenotypic and genotypic responses of Listeria monocytogenes strains exposed to the class IIa bacteriocin sakacin P. Appl Environ Microbiol 75: 6973-6980.
62. Tessema, G.T., Møretrø, T., Snipen, L., Axelsson, L., and Naterstad, K. (2011) Global transcriptional analysis of spontaneous sakacin P-resistant mutant strains of Listeria monocytogenes during growth on different sugars. PLoS ONE 6: e16192.
63. Torres, C., Galián, C., Freiberg, C., Fantino, J.-R., and Jault, J.-M. (2009) The YheI/YheH heterodimer from Bacillus subtilis is a multidrug ABC transporter. Biochim Biophys Acta 1788: 615-622.
64. B in response to osmotic stress in Listeria monocytogenes. Appl Environ Microbiol 77: 7841-7845.
65. Vadyvaloo, V., Arous, S., Gravesen, A., Héchard, Y., Chauhan-Haubrock, R., Hastings, J.W., and Rautenbach, M. (2004) Cell-surface alterations in class IIa bacteriocin-resistant Listeria monocytogenes strains. Microbiology 150: 3025-3033.
66. Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., Van Roy, N., De Paepe, A., and Speleman, F. (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3: research0034.1-0034.11.
67. Vicente, M.F., Mengaud, J., Chenevert, J., Pérez-Diaz, J.C., Geoffroy, C., Baquero, F., etal. (1989) Reacquisition of virulence of haemolysin-negative Listeria monocytogenes mutants by complementation with a plasmid carrying the hlyA gene. Acta Microbiol Hung 36: 199-203.
68. Watson, R. (2009) Listeriosis remains a cause for concern in Europe. Br Med J 338: b319.
69. Williams, T., Bauer, S., Beier, D., and Kuhn, M. (2005) Construction and characterization of Listeria monocytogenes mutants with in-frame deletions in the response regulator genes identified in the genome sequence. Infect Immun 73: 3152-3159.
70. Wulff, G., Gram, L., Ahrens, P., and Vogel, B.F. (2006) One group of genetically similar Listeria monocytogenes strains frequently dominates and persists in several fish slaughter- and smokehouses. Appl Environ Microbiol 72: 4313-4322.
71. Wurtzel, O., Sesto, N., Mellin, J.R., Karunker, I., Edelheit, S., Bécavin, C., etal. (2012) Comparative transcriptomics of pathogenic and non-pathogenic Listeria species. Mol Syst Biol 8: 583.