Sensitivity to acetic acid, ability to colonize abiotic surfaces and virulence potential of Listeria monocytogenes EGD-e after incubation on parsley leaves

Journal of Applied Microbiology

Volumn 108, Issue 2, 2010, Pages 560-570

  Rieu, A ^a   Guzzo, J ^a   Piveteau, P ^b,c  

^a UNIVERSITÉ DE BOURGOGNE   (France)

^b UNIVERSITÉ DE BOURGOGNE   (France)

^c CEMAGREF   (France)

Author keywords

Biofilm; Fresh produce; Pathogenicity; Stress response genes

Indexed keywords

ACID RESISTANCE; BIOFILMS; CELL ADHESION; DISEASES; LISTERIA; MAMMALS; PH; PHYSIOLOGICAL MODELS; PHYSIOLOGY; POLYMERASE CHAIN REACTION; TRANSCRIPTION;

ABIOTIC SURFACES; BACTERIAL CELLS; CONDITION; FRESH PRODUCE; L.MONOCYTOGENES; LISTERIA MONOCYTOGENES; PATHOGENICITY; STATIONARY PHASE; STRESS RESPONSE GENES; VIRULENCE POTENTIAL;

ACETIC ACID;

ACETIC ACID; HEAT SHOCK PROTEIN; MESSENGER RNA; STAINLESS STEEL; VIRULENCE FACTOR;

ACETIC ACID; BACTERIUM; DICOTYLEDON; INCUBATION; LEAF; PATHOGENICITY; PHYLLOSPHERE; PHYSIOLOGICAL RESPONSE; SEEDLING; SURVIVAL; VIRULENCE;

ANIMAL TISSUE; ARTICLE; BACTERIAL CELL; BACTERIAL COLONIZATION; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; BACTERIUM COLONY; BIOFILM; CELL ADHESION; CELL STRAIN CACO 2; COLONY FORMING UNIT; CONTROLLED STUDY; GENE EXPRESSION; GENE TARGETING; LISTERIA MONOCYTOGENES; NONHUMAN; PARSLEY; PATHOGENICITY; PLANT LEAF; POLYMERASE CHAIN REACTION; QUANTITATIVE ANALYSIS; SEEDLING; SURFACE PROPERTY;

BACTERIA (MICROORGANISMS); LISTERIA MONOCYTOGENES; LISTERIA MONOCYTOGENES EGD-E; MAMMALIA; PETROSELINUM CRISPUM;

EID: 74049118371     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/j.1365-2672.2009.04463.x     Document Type: Article

References (61)

1. Becker, L.A., Cetin, M.S., Hutkins, R.W. Benson, A.K. (1998) identification of the gene encoding the alternative sigma factor sigmaB from Listeria monocytogenes and its role in osmotolerance. J Bacteriol 180, 4547 4554.
2. Beuchat, L.R. (2002) Ecological factors influencing survival and growth of human pathogens on raw fruits and vegetables. Microbes Infect 4, 413 423.
3. Beuchat, L.R. Brackett, R.E. (1991) Behavior of Listeria monocytogenes inoculated into raw tomatoes and processed tomato products. Appl Environ Microbiol 57, 1367 1371.
4. Blackman, I.C. Franck, J.F. (1996) Growth of Listeria monocytogenes as a biofilm on various food-processing surfaces. J Food Prot 59, 827 831.
5. Bunning, V.K., Crawford, R.G., Tierney, J.T. Peeler, J.T. (1990) Thermotolerance of Listeria monocytogenes and Salmonnella typhimurium after sublethal heat shock. Appl Environ Microbiol 56, 3216 3219.
6. Cotter, P.D., Emerson, N., Gahan, C.G.M. 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.
7. Cotter, P.D., Gahan, C.G.M. Hill, C. (2001) A glutamate decarboxylase system protects Listeria monocytogenes in gastric fluid. Mol Microbiol 40, 465 475.
8. Del Campo, J., Carlin, F. Nguyen-The, C. (2001) Effects of epiphytic enterobacteriaceae and pseudomonads on the growth of Listeria monocytogenes in model media. J Food Prot 64, 721 724.
9. Desroche, N., Beltramo, C. Guzzo, J. (2005) Determination of an internal control to apply reverse transcription quantitative PCR to study stress response in the lactic acid bacterium Oenococcus oeni. J Microbiol Meth 60, 325 333.
10. Donlan, R.M. Costerton, J.W. (2002) Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev 15, 167 193.
11. Doyle, M.P. Erickson, M.C. (2008) Summer meeting 2007 - the problems with fresh produce: an overview. J Appl Microbiol 105, 317 330.
12. Dreux, N., Albagnac, C., Federighi, M., Carlin, F., Morris, C.E. Nguyen-the, C. (2007a) Viable but non-culturable Listeria monocytogenes on parsley leaves and absence of recovery to a culturable state. J Appl Microbiol 103, 1272 1281.
13. Dreux, N., Albagnac, C., Carlin, F., Morris, C.E. Nguyen-the, C. (2007b) Fate of Listeria spp. on parsley leaves grown in laboratory and field cultures. J Appl Microbiol 103, 1821 1827.
14. Dreux, N., Albagnac, C., Sleator, R.D., Hill, C., Carlin, F., Morris, C.E. Nguyen-the, C. (2008) Glycine betaine improves Listeria monocytogenes tolerance to desiccation on parsley leaves independent of the osmolyte transporters BetL, Gbu and OpuC. J Appl Microbiol 104, 1221 1227.
15. Duche, O., Tremoulet, F., Namane, A. Labadie, J. (2002) A proteomic analysis of the salt stress response of Listeria monocytogenes. FEMS Microbiol Lett 215, 183 188.
16. Dussurget, O., Cabanes, D., Dehoux, P., Lecuit, M., Buchrieser, C., Glaser, P. Cossart, P. (2002) Listeria monocytogenes bile salt hydrolase is a PrfA-regulated virulence factor involved in the intestinal and hepatic phases of listeriosis. Mol Microbiol 45, 1095 1106.
17. Elgayyar, M., Draughon, F.A., Golden, D.A. Mount, J.R. (2001) Antimicrobial activity of essential oils from plants against selected pathogenic and saprophytic microorganisms. J Food Prot 64, 1019 1024.
18. Francis, G.A. O'Beirne, D. (2001) Effects of vegetable type, package atmosphere and storage temperature on growth and survival of Escherichia coli O157:H7 and Listeria monocytogenes. J Ind Microbiol Biotechnol, 26, 1 6.
19. Gahan, C.G.M. Hill, C. (2005) Gastrointestinal phase of Listeria monocytogenes infection. J Appl Microbiol 98, 1345 1353.
20. Gahan, C.G.M., O'Mahony, J. Hill, C. (2001) Characterization of the groESL operon in Listeria monocytogenes: utilization of two reporter systems (gfp and hly) for evaluating in vivo expression. Infect Immun 69, 3924 3932.
21. Gaillard, J.L., Berche, P., Frehel, C., Gouln, E. Cossart, P. (1991) Entry of Listeria monocytogenes into cells is mediated by internalin, a repeat protein reminiscent of surface antigens from gram-positive cocci. Cell 65, 1127 1141.
22. Garner, M.R., James, K.E., Callahan, M.C., Wiedmann, M. Boor, K.J. (2006) Exposure to salt and organic acids increases the ability of Listeria monocytogenes to invade caco-2 cells but decreases its ability to survive gastric stress. Appl Environ Microbiol 72, 5384 5395.
23. Girardin, H., Morris, C.E., Albagnac, C., Dreux, N., Glaux, C. Nguyen-The, C. (2005) Behaviour of the pathogen surrogates Listeria innocua and Clostridium sporogenes during production of parsley in fields fertilized with contaminated amendments. FEMS Microbiol Ecol 54, 287 295.
24. Goerges, S., Aigner, U., Silakowski, B. Scherer, S. (2006) Inhibition of Listeria monocytogenes by food-borne yeasts. Appl Environ Microbiol 72, 313 318.
25. Gram, L. (1993) Inhibitory effect against pathogenic and spoilage bacteria of Pseudomonas strains isolated from spoiled and fresh fish. Appl Environ Microbiol 59, 2197 2203.
26. Heisick, J.E., Wagner, D.E., Nierman, M.L. Peeler, J.T. (1989) Listeria spp. found on fresh market produce. Appl Environ Microbiol 55, 1925 1927.
27. Hill, C., Cotter, P.D., Sleator, R.D. Gahan, C.G.M. (2002) Bacterial stress response in Listeria monocytogenes: jumping the hurdles imposed by minimal processing. International Dairy Journal 12, 273 283.
28. Hudson, A.J. Mott, S.J. (1993) Presence of Listeria monocytogenes, motile aeromonads and Yersinia enterocolitica in environmental samples taken from a supermarket delicatessen. Int J Food Microbiol 18, 333 337.
29. Johannessen, G.S., Loncarevic, S. Kruse, H. (2002) Bacteriological analysis of fresh produce in Norway. Int J Food Microbiol 77, 199 204.
30. Lang, M.M., Harris, L.J. Beuchat, L.R. (2004) Survival and recovery of Escherichia coli O157:H7, Salmonella and Listeria monocytogenes on lettuce and parsley as affected by method of inoculation, time between inoculation and analysis, and treatment with chlorinated water. J Food Prot 67, 1092 1103.
31. Leimeister-Wachter, M., Haffner, C., Domann, E., Goebel, W. Chakraborty, T. (1990) Identification of a gene that positively regulates expression of listeriolysin, the major virulence factor of Listeria monocytogenes. Proc Natl Acad Sci U S A 87, 8336 8340.
32. Liao, C.H. Fett, W.F. (2001) Analysis of native microflora and selection of strains antagonistic to human pathogens on fresh produce. J Food Prot 64, 1110 1115.
33. Liao, C.H. Sapers, G.M. (1999) Influence of soft rot bacteria on growth of Listeria monocytogenes on potato tuber slices. J Food Prot 62, 343 348.
34. Lindsay, D. Von Holy, A. (1997) Evaluation of dislodging methods for laboratory-grown bacterial biofilms. Food Microbiol 14, 383 390.
35. Loncarevic, S., Johannessen, G.S. Rorvik, L.M. (2005) Bacteriological quality of organically grown leaf lettuce in Norway. Lett Appl Microbiol 41, 186 189.
36. Manderfeld, M.M., Schafer, H.W., Davidson, P.M. Zottola, E.A. (1997) Isolation and identification of antimicrobial furocoumarins from parsley. J Food Prot 60, 72 77.
37. Mengaud, J., Dramsi, S., Gouin, E., Vasquez-Boland, J.A., Milton, G. Cossart, P. (1991) Pleiotropic control of Listeria monocytogenes virulence factors by a gene that is autoregulated. Mol Microbiol 23, 1075 1085.
38. Morris, C., Monier, J. Jacques, M. (1997) Methods for observing microbial biofilms directly on leaf surfaces and recovering them for isolation of culturable microorganisms. Appl Environ Microbiol 63, 1570 1576.
39. Murray, E.G.D., Webb, R.A. Swann, M.B.R. (1926) A disease of rabbit characterised by a large mononuclear leucocytosis, caused by a hitherto undescribed Bacillus: Bacterium monocytogenes. J Pathol Bacteriol 29, 407 439.
40. Naimi, T.S., Wicklund, J.H., Olsen, S.J., Krause, G., Wells, J.G., Bartkus, J.M., Boxrud, D.J., Sullivan, M. et al. (2003) Concurrent outbreaks of Shigella sonnei and enterotoxigenic Escherichia coli infections associated with parsley: implications for surveillance and control of foodborne illness. J Food Prot 66, 535 541.
41. Nascimento, M.S., Silva, N., Cantanozi, M.P.L.M. Silva, K.C. (2003) Effects of different disinfection treatments on the natural microbiota o lettuce. J Food Prot 66, 1697 1700.
42. Nightingale, K.K., Schukken, Y.H., Nightingale, C.R., Fortes, E.D., Ho, A.J., Her, Z., Grohn, Y.T., McDonough, P.L. et al. (2004) Ecology and transmission of Listeria monocytogenes infecting ruminants and in the farm environment. Appl Environ Microbiol 70, 4458 4467.
43. Norwood, D.E. Gilmour, A. (1999) Adherence of Listeria monocytogenes strains to stainless steel coupons. J Appl Microbiol 86, 576 582.
44. Oktem, A.B., Bayram, G., Ceylan, A.E. Yentur, G. (2006) Prevalence of Listeria monocytogenes in some Turkish foodstuffs. J Food Qual 29, 76 86.
45. Olier, M., Pierre, F., Rousseaux, S., Lemaitre, J.-P., Rousset, A., Piveteau, P. Guzzo, J. (2003) Expression of truncated internalin A is involved in impaired internalization of some Listeria monocytogenes isolates carried asymptomatically by humans. Infect Immun 71, 1217 1224.
46. Palumbo, J.D., Kaneko, A., Nguyen, K.D. Gorski, L. (2005) Identification of genes induced in Listeria monocytogenes during growth and attachment to cut cabbage, using differential display. Appl Environ Microbiol 71, 5236 5243.
47. Prazac, A.M., Murano, E.A., Mercado, I. Acuff, G.R. (2002) Prevalence of Listeria monocytogenes during production and postharvest processing of cabbage. J Food Prot 65, 1728 1734.
48. Rieu, A., Weidmann, S., Garmyn, D., Piveteau, P. Guzzo, J. (2007) agr system of Listeria monocytogenes EGD-e: role in adherence and differential expression pattern. Appl Environ Microbiol 73, 6125 6133.
49. Robertson, L.J., Johannessen, G.S., Gjerde, B.K. Loncarevic, S. (2002) Microbiological analysis of seed sprouts in Norway. Int J Food Microbiol 75, 119 126.
50. Rouquette, C., Ripio, M.-T., Pellegrini, E., Bolla, J.-M., Tascon, R.I., Vazquez-Boland, J.-A. Berche, P. (1996) Identification of a ClpC ATPase required for stress tolerance and in vivo survival of Listeria monocytogenes. Mol Microbiol 21, 977 987.
51. Sanz, S., Gimenez, M. Olarte, C. (2003) Survival and growth of Listeria monocytogenes and enterohemorrhagic Escherichia coli O157:H7 in minimally processed artichokes. J Food Prot 66, 2203 2209.
52. Schoeller, N.P., Ingham, S.C. Ingham, B.H. (2002) Assessment of the potential for Listeria monocytogenes survival and growth during alfafa sprout production and use of ionizing radiation as a potential intervention treatment. J Food Prot 65, 1259 1266.
53. Sleator, R.D., Gahan, C.G.M., O'Driscoll, B. Hill, C. (2000) Analysis of the role of betL in contributing to the growth and survival of Listeria monocytogenes LO28. Int J Food Microbiol 60, 261 268.
54. Sleator, R.D., Wouters, J., Gahan, C.G.M., Abee, T. Hill, C. (2001) Analysis of the role of OpuC, an osmolyte transport system, in salt tolerance and virulence potential of Listeria monocytogenes. Appl Environ Microbiol 67, 2692 2698.
55. Tschape, H., Prager, R., Streckel, W., Fruth, A., Tietze, E. Bohme, G. (1997) Verotoxinogenic Citrobacter freundii associated with severe gastroenteridis and cases of haemolytic uraemic syndrome in a nursery school: green butter as the infection source. Epidemiol Infect 114, 441 450.
56. Weis, J. Seeliger, H.P.R. (1975) Incidence of Listeria monocytogenes in nature. Appl Microbiol 30, 29 32.
57. Welshimer, H.J. Donker-Voet, J. (1971) Listeria monocytogenes in nature. Appl Microbiol 21, 516 519.
58. Wemekamp-Kamphuis, H.H., Wouters, J.A., Sleator, R.D., Gahan, C.G.M., Hill, C. Abee, T. (2002) Multiple deletions of the osmolyte transporters BetL, Gbu, and OpuC of Listeria monocytogenes affect virulence and growth at high osmolarity. Appl Environ Microbiol 68, 4710 4716.
59. Wong, A. (1998) Biofilms in food processing environments. J Dairy Sci 81, 2765 2770.
60. Zhang, S. Farber, J.M. (1996) The effects of various disinfectants against Listeria monocytogenes on fresh-cut vegetables. Food Microbiol 13, 311 321.
61. Zhao, T., Doyle, M.P. Zhao, P. (2004) Control of Listeria monocytogenes in a biofilm by competitive-exclusion microorganisms. Appl Environ Microbiol 70, 3996 4003.