1887

Abstract

serovar Typhimurium (. Typhimurium) remains an important cause of food-borne infection in the developed world. In order to establish infection within a host, must survive and recover from a range of environmental stresses. . Typhimurium strain SL1344 is among the most extensively studied pathogenic strains, while . Typhimurium phage type DT104 is an important type that has been associated with pandemic spread and a high number of food-borne disease outbreaks over the last two decades. In this study, we have compared the abilities of these two . Typhimurium types to recover from stress exposures commonly encountered in food production, including 685 mM NaCl, pH 3.8, low temperature (6 °C) and combinations thereof. Following removal from prolonged (8 days) stress, DT104 cultures that had been exposed to low temperature, with or without additional stress, resumed exponential growth more rapidly than SL1344 cultures exposed to the same conditions. SL1344 showed higher levels of filamentation than DT104 in response to NaCl exposure at low temperature. Further, SL1344 incurred higher levels of membrane damage in response to elevated NaCl and pH 3.8 at both temperatures compared with DT104. However, both strains recovered normal cell division and membrane integrity within 6 h when all stresses were removed. Expression of the pathogenicity island 1 gene , the first gene in the operon, was monitored using a chromosomal reporter in which expression was driven by the promoter. Recovery of expression was comparable for SL1344 and DT104 exposed to stress at 22 °C. However, DT104 cultures exposed to pH 3.8 or combined NaCl and low-pH stress at low temperature resumed expression more rapidly than SL1344. Both strains recovered maximal levels of expression after 6 h recovery from all stresses and, interestingly, maximal levels of expression were significantly higher in SL1344, consistent with expression in late-exponential, non-stressed SL1344 and DT104 cultures. Together, these data show that . Typhimurium is capable of rapid recovery from environmental and food-related stresses, and give insight into the enhanced ability of DT104 compared with SL1344 to adapt to such stresses, which may contribute to the success of this globally disseminated pathogenic phage type.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.045666-0
2011-04-01
2019-10-22
Loading full text...

Full text loading...

/deliver/fulltext/micro/157/4/1103.html?itemId=/content/journal/micro/10.1099/mic.0.045666-0&mimeType=html&fmt=ahah

References

  1. Adaska, J. M., Silva, A. J. & Sischo, W. M. ( 2008; ). Comparison of Salmonella enterica subspecies enterica serovar Typhimurium isolates from dairy cattle and humans using in vitro assays of virulence. Vet Microbiol 128, 90–95.[CrossRef]
    [Google Scholar]
  2. Allen, C. A., Fedorka-Cray, P. J., Vazquez-Torres, A., Suyemoto, M., Altier, C., Ryder, L. R., Fang, F. C. & Libby, S. J. ( 2001; ). In vitro and in vivo assessment of Salmonella enterica serovar Typhimurium DT104 virulence. Infect Immun 69, 4673–4677.[CrossRef]
    [Google Scholar]
  3. Anon ( 2010; ). The Community Summary Report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in the European Union in 2008. EFSA Journal 8, 1496.
    [Google Scholar]
  4. Bajaj, V., Lucas, R. L., Hwang, C. & Lee, C. A. ( 1996; ). Co-ordinate regulation of Salmonella typhimurium invasion genes by environmental and regulatory factors is mediated by control of hilA expression. Mol Microbiol 22, 703–714.[CrossRef]
    [Google Scholar]
  5. Barrow, P. A., Tucker, J. F. & Simpson, J. M. ( 1987; ). Inhibition of colonization of the chicken alimentary tract with Salmonella typhimurium Gram-negative facultatively anaerobic bacteria. Epidemiol Infect 98, 311–322.[CrossRef]
    [Google Scholar]
  6. Beuchat, L. R. ( 1996; ). Pathogenic microorganisms associated with fresh produce. J Food Prot 59, 204–216.
    [Google Scholar]
  7. Carlson, S. A., Browning, M., Ferris, K. E. & Jones, B. D. ( 2000; ). Identification of diminished tissue culture invasiveness among multiple antibiotic resistant Salmonella typhimurium DT104. Microb Pathog 28, 37–44.[CrossRef]
    [Google Scholar]
  8. Clark, L., Martinez-Argudo, I., Humphrey, T. J. & Jepson, M. A. ( 2009; ). GFP plasmid-induced defects in Salmonella invasion depend on plasmid architecture, not protein expression. Microbiology 155, 461–467.[CrossRef]
    [Google Scholar]
  9. Croak, S. & Corredig, M. ( 2006; ). The role of pectin in orange juice stabilization: effect of pectin methylesterase and pectinase activity on the size of cloud particles. Food Hydrocoll 20, 961–965.[CrossRef]
    [Google Scholar]
  10. Datsenko, K. A. & Wanner, B. L. ( 2000; ). One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 97, 6640–6645.[CrossRef]
    [Google Scholar]
  11. Davies, A., O'Neill, P., Towers, L. & Cooke, M. ( 1996; ). An outbreak of Salmonella typhimurium DT104 food poisoning associated with eating beef. Commun Dis Rep CDR Rev 6, R159–R162.
    [Google Scholar]
  12. Davis, M. A., Hancock, D. D. & Besser, T. E. ( 2002; ). Multiresistant clones of Salmonella enterica: the importance of dissemination. J Lab Clin Med 140, 135–141.[CrossRef]
    [Google Scholar]
  13. Dechet, A. M., Scallan, E., Gensheimer, K., Hoekstra, R., Gunderman-King, J., Lockett, J., Wrigley, D., Chege, W. & Sobel, J., Multistate Working Group ( 2006; ). Outbreak of multidrug-resistant Salmonella enterica serotype Typhimurium definitive type 104 infection linked to commercial ground beef, northeastern United States, 2003–2004. Clin Infect Dis 42, 747–752.[CrossRef]
    [Google Scholar]
  14. Ellermeier, J. R. & Slauch, J. M. ( 2007; ). Adaptation to the host environment: regulation of the SPI1 type III secretion system in Salmonella enterica serovar Typhimurium. Curr Opin Microbiol 10, 24–29.[CrossRef]
    [Google Scholar]
  15. Ernst, R. K., Dombroski, D. M. & Merrick, J. M. ( 1990; ). Anaerobiosis, type 1 fimbriae, and growth phase are factors that affect invasion of HEp-2 cells by Salmonella typhimurium. Infect Immun 58, 2014–2016.
    [Google Scholar]
  16. Fratamico, P. M. ( 2003; ). Tolerance to stress and ability of acid-adapted and non-acid-adapted Salmonella enterica serovar Typhimurium DT104 to invade and survive in mammalian cells in vitro. J Food Prot 66, 1115–1125.
    [Google Scholar]
  17. Galán, J. E. ( 2001; ). Salmonella interactions with host cells: type III secretion at work. Annu Rev Cell Dev Biol 17, 53–86.[CrossRef]
    [Google Scholar]
  18. Galán, J. E. & Curtiss, R., III ( 1990; ). Expression of Salmonella typhimurium genes required for invasion is regulated by changes in DNA supercoiling. Infect Immun 58, 1879–1885.
    [Google Scholar]
  19. Glynn, M. K., Bopp, C., Dewitt, W., Dabney, P., Mokhtar, M. & Angulo, F. J. ( 1998; ). Emergence of multidrug-resistant Salmonella enterica serotype Typhimurium DT104 infections in the United States. N Engl J Med 338, 1333–1339.[CrossRef]
    [Google Scholar]
  20. Hasan, N., Koob, M. & Szybalsk, W. ( 1994; ). Escherichia coli genome targeting, I. Cre-lox-mediated in vitro generation of ori plasmids and their in vivo chromosomal integration and retrieval. Gene 150, 51–56.[CrossRef]
    [Google Scholar]
  21. Hautefort, I., Proença, M. J. & Hinton, J. C. D. ( 2003; ). Single-copy green fluorescent protein gene fusions allow accurate measurement of Salmonella gene expression in vitro and during infection of mammalian cells. Appl Environ Microbiol 69, 7480–7491.[CrossRef]
    [Google Scholar]
  22. Hazeleger, W. C., Dalvoorde, M. & Beumer, R. R. ( 2006; ). Fluorescence microscopy of NaCl-stressed, elongated Salmonella and Listeria cells reveals the presence of septa in filaments. Int J Food Microbiol 112, 288–290.[CrossRef]
    [Google Scholar]
  23. Henry, T., García-Del Portillo, F. & Gorvel, J. P. ( 2005; ). Identification of Salmonella functions critical for bacterial cell division within eukaryotic cells. Mol Microbiol 56, 252–267.[CrossRef]
    [Google Scholar]
  24. Hoiseth, S. K. & Stocker, B. A. D. ( 1981; ). Aromatic-dependent Salmonella typhimurium are non-virulent and effective as live vaccines. Nature 291, 238–239.[CrossRef]
    [Google Scholar]
  25. Hughes, C., Gillespie, I. A., O'Brien, S. J. & Breakdowns Food Safety, G. ( 2007; ). Foodborne transmission of infectious intestinal disease in England and Wales, 1992–2003. Food Contr 18, 766–772.[CrossRef]
    [Google Scholar]
  26. Humphrey, T. ( 2004; ). Salmonella, stress responses and food safety. Nat Rev Microbiol 2, 504–509.[CrossRef]
    [Google Scholar]
  27. Jørgensen, F., Leach, S., Wilde, S. J., Davies, A., Stewart, G. S. & Humphrey, T. ( 2000; ). Invasiveness in chickens, stress resistance and RpoS status of wild-type Salmonella enterica subsp. enterica serovar Typhimurium definitive type 104 and serovar Enteritidis phage type 4 strains. Microbiology 146, 3227–3235.
    [Google Scholar]
  28. Justice, S. S., Hunstad, D. A., Cegelski, L. & Hultgren, S. J. ( 2008; ). Morphological plasticity as a bacterial survival strategy. Nat Rev Microbiol 6, 162–168.[CrossRef]
    [Google Scholar]
  29. Karatzas, K. A. G., Hocking, P. M., Jørgensen, F., Mattick, K., Leach, S. & Humphrey, T. J. ( 2008; ). Effects of repeated cycles of acid challenge and growth on the phenotype and virulence of Salmonella enterica. J Appl Microbiol 105, 1640–1648.[CrossRef]
    [Google Scholar]
  30. Klein, J. R., Fahlen, T. F. & Jones, B. D. ( 2000; ). Transcriptional organization and function of invasion genes within Salmonella enterica serovar Typhimurium pathogenicity island 1, including the prgH, prgI, prgJ, prgK, orgA, orgB, and orgC genes. Infect Immun 68, 3368–3376.[CrossRef]
    [Google Scholar]
  31. Kubori, T., Matsushima, Y., Nakamura, D., Uralil, J., Lara-Tejero, M., Sukhan, A., Galán, J. E. & Aizawa, S. I. ( 1998; ). Supramolecular structure of the Salmonella Typhimurium type III protein secretion system. Science 280, 602–605.[CrossRef]
    [Google Scholar]
  32. Leach, S. A., Williams, A., Davies, A. C., Wilson, J., Marsh, P. D. & Humphrey, T. J. ( 1999; ). Aerosol route enhances the contamination of intact eggs and muscle of experimentally infected laying hens by Salmonella typhimurium DT104. FEMS Microbiol Lett 171, 203–207.[CrossRef]
    [Google Scholar]
  33. Lee, C. A. & Falkow, S. ( 1990; ). The ability of Salmonella to enter mammalian cells is affected by bacterial growth state. Proc Natl Acad Sci U S A 87, 4304–4308.[CrossRef]
    [Google Scholar]
  34. Mattick, K. L., Jørgensen, F., Legan, J. D., Cole, M. B., Porter, J., Lappin-Scott, H. M. & Humphrey, T. J. ( 2000; ). Survival and filamentation of Salmonella enterica serovar Enteritidis PT4 and Salmonella enterica serovar Typhimurium DT104 at low water activity. Appl Environ Microbiol 66, 1274–1279.[CrossRef]
    [Google Scholar]
  35. Mattick, K. L., Phillips, L. E., Jørgensen, F., Lappin-Scott, H. M. & Humphrey, T. J. ( 2003a; ). Filament formation by Salmonella spp. inoculated into liquid food matrices at refrigeration temperatures, and growth patterns when warmed. J Food Prot 66, 215–219.
    [Google Scholar]
  36. Mattick, K. L., Rowbury, R. J. & Humphrey, T. J. ( 2003b; ). Morphological changes to Escherichia coli O157 : H7, commensal E. coli and Salmonella spp in response to marginal growth conditions, with special reference to mildly stressing temperatures. Sci Prog 86, 103–113.[CrossRef]
    [Google Scholar]
  37. Mor-Mur, M. & Yuste, J. ( 2010; ). Emerging bacterial pathogens in meat and poultry: an overview. Food and Bioprocess Technology 3, 24–35.[CrossRef]
    [Google Scholar]
  38. Perrett, C. A. & Jepson, M. A. ( 2007; ). Applications of cell imaging in Salmonella research. Methods Mol Biol 394, 235–273.
    [Google Scholar]
  39. Perrett, C. A., Karavolos, M. H., Humphrey, S., Mastroeni, P., Martinez-Argudo, I., Spencer, H., Bulmer, D., Winzer, K., McGhie, E. & other authors ( 2009; ). LuxS-based quorum sensing does not affect the ability of Salmonella enterica serovar Typhimurium to express the SPI-1 type 3 secretion system, induce membrane ruffles, or invade epithelial cells. J Bacteriol 191, 7253–7259.[CrossRef]
    [Google Scholar]
  40. Phillips, L. E., Humphrey, T. J. & Lappin-Scott, H. M. ( 1998; ). Chilling invokes different morphologies in two Salmonella enteritidis PT4 strains. J Appl Microbiol 84, 820–826.[CrossRef]
    [Google Scholar]
  41. Rowley, G., Spector, M., Kormanec, J. & Roberts, M. ( 2006; ). Pushing the envelope: extracytoplasmic stress responses in bacterial pathogens. Nat Rev Microbiol 4, 383–394.[CrossRef]
    [Google Scholar]
  42. Rychlik, I. & Barrow, P. A. ( 2005; ). Salmonella stress management and its relevance to behaviour during intestinal colonisation and infection. FEMS Microbiol Rev 29, 1021–1040.[CrossRef]
    [Google Scholar]
  43. Saunders, M. P., Wu, G., Abuoun, M., Pan, Z., Anjum, M. & Woodward, M. J. ( 2010; ). Optical genetic mapping defines regions of chromosomal variation in serovars of S. enterica subsp. enterica of concern for human and animal health. Epidemiol Infect (published online 22 September 2010).
    [Google Scholar]
  44. Sivapalasingam, S., Friedman, C. R., Cohen, L. & Tauxe, R. V. ( 2004; ). Fresh produce: a growing cause of outbreaks of foodborne illness in the United States, 1973 through 1997. J Food Prot 67, 2342–2353.
    [Google Scholar]
  45. Temme, K., Salis, H., Tullman-Ercek, D., Levskaya, A., Hong, S. H. & Voigt, C. A. ( 2008; ). Induction and relaxation dynamics of the regulatory network controlling the type III secretion system encoded within Salmonella pathogenicity island 1. J Mol Biol 377, 47–61.[CrossRef]
    [Google Scholar]
  46. Threlfall, E. J. ( 2000; ). Epidemic Salmonella typhimurium DT 104 – a truly international multiresistant clone. J Antimicrob Chemother 46, 7–10.[CrossRef]
    [Google Scholar]
  47. Threlfall, E. J. ( 2002; ). Antimicrobial drug resistance in Salmonella: problems and perspectives in food- and water-borne infections. FEMS Microbiol Rev 26, 141–148.[CrossRef]
    [Google Scholar]
  48. Villar, R. G., Macek, M. D., Simons, S., Hayes, P. S., Goldoft, M. J., Lewis, J. H., Rowan, L. L., Hursh, D., Patnode, M. & Mead, P. S. ( 1999; ). Investigation of multidrug-resistant Salmonella serotype Typhimurium DT104 infections linked to raw-milk cheese in Washington State. JAMA 281, 1811–1816.[CrossRef]
    [Google Scholar]
  49. Vojdani, J. D., Beuchat, L. R. & Tauxe, R. V. ( 2008; ). Juice-associated outbreaks of human illness in the United States, 1995 through 2005. J Food Prot 71, 356–364.
    [Google Scholar]
  50. Wall, P. G., Morgan, D., Lamden, K., Ryan, M., Griffin, M., Threlfall, E. J., Ward, L. R. & Rowe, B. ( 1994; ). A case control study of infection with an epidemic strain of multiresistant Salmonella typhimurium DT104 in England and Wales. Commun Dis Rep CDR Rev 4, R130–R135.
    [Google Scholar]
  51. Wu, V. C. H. ( 2008; ). A review of microbial injury and recovery methods in food. Food Microbiol 25, 735–744.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.045666-0
Loading
/content/journal/micro/10.1099/mic.0.045666-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error