Synergistic effects of sodium chloride, glucose, and temperature on biofilm formation by listeria monocytogenes Serotype 1/2a and 4b Strains

Applied and Environmental Microbiology

Volumn 76, Issue 5, 2010, Pages 1433-1441

  Pan, Youwen ^a,d   Breidt Jr , Frederick ^b   Gorski, Lisa ^c  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

^b NORTH CAROLINA STATE UNIVERSITY   (United States)

^c AGRICULTURAL RESEARCH SERVICE   (United States)

^d BAXTER HEALTHCARE CORPORATION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL CELLS; BIOFILM CELLS; BIOFILM FORMATION; BIOFILM MATRIX; CRYSTAL VIOLET; ENVIRONMENTAL FACTORS; EXTRA-CELLULAR POLYMERIC SUBSTANCES; LISTERIA MONOCYTOGENES; LISTERIOSIS; MICROPLATE ASSAY; PROCESSING ENVIRONMENTS; SEROTYPES; SYNERGISTIC EFFECT; TRYPTIC SOY BROTHS;

BIOFILMS; ETHANOL; GLUCOSE; LISTERIA; SODIUM; SODIUM CHLORIDE;

BIOFILTERS;

ALCOHOL; COLORING AGENT; CRYSTAL VIOLET; GLUCOSE; SODIUM CHLORIDE;

BACTERIUM; BIOFILM; ENVIRONMENTAL FACTOR; GLUCOSE; GROWTH RATE; MICROBIAL ACTIVITY; MICROBIAL ECOLOGY; SODIUM CHLORIDE; TEMPERATURE EFFECT;

ARTICLE; BIOFILM; DRUG EFFECT; EXTRACELLULAR MATRIX; GROWTH, DEVELOPMENT AND AGING; HUMAN; LISTERIA MONOCYTOGENES; METABOLISM; PHYSIOLOGY; STAINING; TEMPERATURE;

BIOFILMS; COLORING AGENTS; ETHANOL; EXTRACELLULAR MATRIX; GENTIAN VIOLET; GLUCOSE; HUMANS; LISTERIA MONOCYTOGENES; SODIUM CHLORIDE; STAINING AND LABELING; TEMPERATURE;

BACTERIA (MICROORGANISMS); LISTERIA MONOCYTOGENES;

EID: 77649200447     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.02185-09     Document Type: Article

References (31)

1. Borucki, M. K., J. D. Peppin, D. White, F. Loge, and D. R. Call. 2003. Variation in biofilm formation among strains of Listeria monocytogenes. Appl. Environ. Microbiol. 69:7336-7342.
2. Briandet, R., T. Meylheuc, C. Maher, and M. N. Bellon-Fontaine. 1999. Listeria monocytogenes Scott A: cell surface charge, hydrophobicity, and electron donor and acceptor characteristics under different environmental growth conditions. Appl. Environ. Microbiol. 65:5328-5333.
3. Bruhn, J. B., B. F. Vogel, and L. Gram. 2005. Bias in the Listeria monocytogenes enrichment procedure: lineage 2 strains outcompete lineage 1 strains in University of Vermont selective enrichments. Appl. Environ. Microbiol. 71:961-967.
4. Buncic, S., S. M. Avery, J. Rocourt, and M. Dimitrijevic. 2001. Can foodrelated environmental factors induce different behaviour in two key serovars, 4b and l/2a, of Listeria monocytogenes? Int. J. Food Microbiol. 65:201-212.
5. Chae, M. S., and H. Schratt. 2000. Comparative evaluation of adhesion and biofilm formation of different Listeria monocytogenes strains. Int. J. Food Microbiol. 62:103-111.
6. Chavant, P., B. Martinie, T. Meylheuc, M. Bellon-Fontaine, and M. Hebraud. 2002. Listeria monocytogenes L028: surface physicochemical properties and ability to form biofilms at different temperatures and growth phases. Appl. Environ. Microbiol. 68:728-737.
7. Di Bonaventura, G., R. Piccolomini, D. Paludi, V. D'Orio, A. Vergara, M. Conter, and A. Ianieri. 2008. Influence of temperature on biofilm formation by Listeria monocytogenes on various food-contact surfaces: relationship with motility and cell surface hydrophobicity. J. Appl. Microbiol. 104:1552-1561.
8. Djordjevic, D., M. Wiedmann, and L. A. McLandsborough. 2002. Microtiter plate assay for assessment oí Listeria monocytogenes biofilm formation. Appl. Environ. Microbiol. 68:2950-2958.
9. Dobinsky, S., K. Kiel, H. Rohde, K. Bartscht, J. K. Knobloch, M. A. Horstkotte, and D. Mack. 2003. Glucose-related dissociation between icaADBC transcription and biofilm expression by Staphylococcus epidermidis: evidence for an additional factor required for polysaccharide intercellular adhesin synthesis. J. Bacteriol. 185:2879-2886.
10. Eifert, J. D., P. A. Curtis, M. C. Bazaco, R. J. Meinersmann, M. E. Berrang, S. Kernodle, C. Stam, L.-A. Jaykus, and S. Kathariou. 2005. Molecular characterization of Listeria monocytogenes of the serotype 4b complex (4b, 4d, 4e) from two turkey processing plants. Foodborne Fathog. Dis. 2:192-200.
11. Folsom, J. P., G. R. Siragusa, and J. F. Frank. 2006. Formation of biofilm at different nutrient levels by various genotypes of Listeria monocytogenes. J. Food Prot. 69:826-834.
12. Frank, K. L., and R. Patel. 2007. Foly-N-acetylglucosamine is not a major component of the extracellular matrix in biofilms formed by icaADBC-positive Staphylococcus lugdunensis isolates. Infect. Immun. 75:4728-4742.
13. Gandhi, M., and M. L. Chikindas. 2007. Listeria: a foodborne pathogen that knows how to survive. Int. J. Food Microbiol. 113:1-15.
14. Gorski, L., D. Flaherty, and R. E. Mandrell. 2006. Competitive fitness of Listeria monocytogenes serotype 1/2a and 4b strains in mixed cultures with and without food, in the U.S. Food and Drug Administration enrichment protocol. Appl. Environ. Microbiol. 72:776-783.
15. Gravesen, A., C. Lekkas, and S. Knochel. 2005. Surface attachment of Listeria monocytogenes is induced by sublethal concentrations of alcohol at low temperatures. Appl. Environ. Microbiol. 71:5601-5603.
16. Jefferson, K. K. 2004. What drives bacteria to produce a biofilm? FEMS Microbiol. Lett. 236:163-173.
17. Jensen, A., M. H. Larsen, H. Ingmer, B. F. Vogel, and L. Gram. 2007. Sodium chloride enhances adherence and aggregation and strain variation influences invasiveness of Listeria monocytogenes strains. J. Food Prot. 70:592-599.
18. Kalmokoff, M. L., J. W. Austin, X. D. Wan, G. Sanders, S. Banerjee, and J. M. Farber. 2001. Adsorption, attachment and biofilm formation among isolates of Listeria monocytogenes using model conditions. J. Appl. Microbiol. 91:725-734.
19. Kathariou, S. 2002. Listeria monocytogenes virulence and pathogenicity, a food safety perspective. J. Food Prot. 65:1811-1829.
20. Kathariou, S., L. Graves, C. Buchrieser, P. Glaser, R. M. Siletzky, and B. Swaminathan. 2006. Involvement of closely related strains of a new clonal group of Listeria monocytogenes in the 1989-99 and 2002 multistate outbreaks of foodborne listeriosis in the United States. Foodborne Fathog. Dis. 3:292-302.
21. Kim, J., R. M. Siletzky, and S. Kathariou. 2008. Host ranges of Listeriaspecific bacteriophages from the turkey processing plant environment in the United States. Appl. Environ. Microbiol. 74:6623-6630.
22. Lim, Y., M. Jana, T. T. Luong, and C. Y. Lee. 2004. Control of glucose- and NaCl-induced biofilm formation by rbf in Staphylococcus aureus. J. Bacteriol. 186:722-729.
23. Moltz, A. G., and S. E. Martin. 2005. Formation of biofilms by Listeria monocytogenes under various growth conditions. J. Food Prot. 68:92-97.
24. Moretre, T., L. Hermansen, A. L. Hoick, M. S. Sidhu, K. Rudi, and S. Langsrud. 2003. Biofilm formation and the presence of the intercellular adhesion locus ica among staphylococci from food and food processing environments. Appl. Environ. Microbiol. 69:5648-5655.
25. Moretre, T., and S. Langsrud. 2004. Listeria monocytogenes: biofilm formation and persistence in food-processing environments. Biofilms 1:107-121.
26. Mullapudi, S., R. M. Siletzky, and S. Kathariou. 2008. Heavy-metal and benzalkonium chloride resistance of Listeria monocytogenes isolates from the environment of turkey-processing plants. Appl. Environ. Microbiol. 74:1464-1468.
27. Nelson, K. E., D. E. Fouts, E. F. Mongodin, J. Ravel, R. T. DeBoy, J. F. Kolonay, D. A. Rasko, S. V. Angiuoli, S. R. Gill, I. T. Paulsen, J. Peterson, O. White, W. C. Nelson, W. Nierman, M. J. Beanan, L. M. Brinkac, S. C. Daugherty, R. J. Dodson, A. S. Durkin, R. Madupu, D. H. Haft, J. Selengut, S. Van Aken, H. Khouri, N. Fedorova, H. Forberger, B. Tran, S. Kathariou, L. D. Wonderling, G. A. Uhlich, D. O. Bayles, J. B. Luchansky, and C. M. Fraser. 2004. Whole genome comparisons of serotype 4b and l/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.
28. Norwood, D. E., and A. Gilmour. 1999. Adherence of Listeria monocytogenes strains to stainless steel coupons. J. Appl. Microbiol. 86:576-582.
29. O'Toole, G., and H. B. Kaplan. 2000. Biofilm formation as microbial development. Annu. Rev. Microbiol. 54:49-79.
30. Pan, Y., F. Breidt, Jr., and S. Kathariou. 2006. Resistance of Listeria monocytogenes biofilms to sanitizing agents in a simulated food processing environment. Appl. Environ. Microbiol. 72:7711-7717.
31. Pan, Y., F. Breidt, Jr., and S. Kathariou. 2009. Competition of Listeria monocytogenes serotype 1/2a and 4b strains in mixed culture biofilms. Appl. Environ. Microbiol. 75:5846-5852.