1887

Abstract

High hydrostatic pressure processing (HPP) is currently being used as a treatment for certain foods to control the presence of food-borne pathogens, such as . Genomic microarray analysis was performed to determine the effects of HPP on in order to understand how it responds to mechanical stress injury. Reverse transcriptase PCR analysis of and indicated that the reduction of mRNA expression in HPP-treated cells was dependent on intensity and time of the treatment. Treatments of 400 and 600 MPa for 5 min on cells in the exponential growth phase, though leading to partial or complete cellular inactivation, still resulted in measurable relative differential gene expression. Gene set enrichment analysis indicated that HPP induced increased expression of genes associated with DNA repair mechanisms, transcription and translation protein complexes, the septal ring, the general protein translocase system, flagella assemblage and chemotaxis, and lipid and peptidoglycan biosynthetic pathways. On the other hand, HPP appears to suppress a wide range of energy production and conversion, carbohydrate metabolism and virulence-associated genes accompanied by strong suppression of the SigB and PrfA regulons. HPP also affected genes controlled by the pleotrophic regulator CodY. HPP-induced cellular damage appears to lead to increased expression of genes linked to sections of the cell previously shown in bacteria to be damaged or altered during HPP exposure and suppression of gene expression associated with cellular growth processes and virulence.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.2007/010314-0
2008-02-01
2020-07-13
Loading full text...

Full text loading...

/deliver/fulltext/micro/154/2/462.html?itemId=/content/journal/micro/10.1099/mic.0.2007/010314-0&mimeType=html&fmt=ahah

References

  1. Abe F., Kato C., Horikoshi K.. 1999; Pressure-regulated metabolism in microorganisms. Trends Microbiol7:447–453
    [Google Scholar]
  2. Aertsen A., Michiels C. W.. 2005; Mrr instigates the SOS response after high pressure stress in Escherichia coli . Mol Microbiol58:1381–1391
    [Google Scholar]
  3. Aertsen A., Van Houdt R., Vanoirbeek K., Michiels C. W.. 2004a; An SOS response induced by high pressure in Escherichia coli . J Bacteriol186:6133–6141
    [Google Scholar]
  4. Aertsen A., Vanoirbeek K., De Spiegeleer P., Sermon J., Hauben K., Farewell A., Nyström T., Michiels C. W.. 2004b; Heat shock protein-mediated resistance to high hydrostatic pressure in Escherichia coli . Appl Environ Microbiol70:2660–2666
    [Google Scholar]
  5. Alpas H., Kalchayanand N., Bozoglu F., Sikes A., Dunne C. P., Ray B.. 1999; Variation in resistance to hydrostatic pressure among strains of food-borne pathogens. Appl Environ Microbiol65:4248–4251
    [Google Scholar]
  6. Ananta E., Heinz V., Knorr D.. 2004; Assessment of high pressure induced damage on Lactobacillus rhamnosus GG by flow cytometry. Food Microbiol21:567–577
    [Google Scholar]
  7. Apfel C. M., Takács B., Fountoulakis M., Stieger M., Keck W.. 1999; Use of genomics to identify bacterial undecaprenyl pyrophosphate synthetase: cloning, expression, and characterization of the essential uppS gene. J Bacteriol181:483–492
    [Google Scholar]
  8. Arous S., Buchrieser C., Folio P., Glaser P., Namane A., Hébraud M., Héchard Y.. 2004; Global analysis of gene expression in an rpoN mutant of Listeria monocytogenes . Microbiology150:1581–1590
    [Google Scholar]
  9. Autret N., Raynaud C., Dubail I., Berche P., Charbit A.. 2003; Identification of the agr locus of Listeria monocytogenes : role in bacterial virulence. Infect Immun71:4463–4471
    [Google Scholar]
  10. Barciszewski J., Jurczak J., Porowski S., Specht T., Erdmann V. A.. 1999; The role of water structure in conformational changes of nucleic acids in ambient and high-pressure conditions. Eur J Biochem260:293–307
    [Google Scholar]
  11. Bartlett D. H.. 2002; Pressure effects on in vivo microbial processes. Biochim Biophys Acta1595:367–381
    [Google Scholar]
  12. Bayles D. O., Uhlich G. A.. 2006; Inactivation of the Crp/Fnr family of regulatory genes in Listeria monocytogenes strain F2365 does not alter its heat resistance at 6 °C. J Food Prot69:2758–2760
    [Google Scholar]
  13. Behari J., Youngman P.. 1998; A homolog of CcpA mediates catabolite control in Listeria monocytogenes but not carbon source regulation of virulence genes. J Bacteriol180:6316–6324
    [Google Scholar]
  14. Bell C., Kyriakides A.. 2005; Listeria: a Practical Approach to the Organism and Its Control in Foods (Practical Food Microbiology Series) Oxford: Blackwell Publishing;
  15. Bennett H. J., Pearce D. M., Glenn S., Taylor C. M., Kuhn M., Sonenshein A. L., Andrew P. W., Roberts I. S.. 2007; Characterization of relA and codY mutants of Listeria monocytogenes : identification of the CodY regulon and its role in virulence. Mol Microbiol63:1453–1467
    [Google Scholar]
  16. Boorsma A., Foat B. C., Vis J., Klis F., Bussemaker H. J.. 2005; T-profiler: scoring the activity of predefined groups of gene using gene expression data. Nucleic Acids Res33:W592–W595
    [Google Scholar]
  17. Bothun G. D., Knutson B. L., Berberich J. A., Strobel H. J., Nokes S. E.. 2004; Metabolic selectivity and growth of Clostridium thermocellum in continuous culture under elevated hydrostatic pressure. Appl Microbiol Biotechnol65:149–157
    [Google Scholar]
  18. Bozoglu F., Alpas H., Kaletunç G.. 2004; Injury recovery of foodborne pathogens in high hydrostatic pressure treated milk during storage. FEMS Immunol Med Microbiol40:243–247
    [Google Scholar]
  19. Bull M. K., Hayman M. M., Stewart C. M., Szabo E. A., Knabel S. J.. 2005; Effect of prior growth temperature, type of enrichment medium, and temperature and time of storage on recovery of Listeria monocytogenes following high pressure processing of milk. Int J Food Microbiol101:53–61
    [Google Scholar]
  20. Dame R. T., Goosen N.. 2002; HU: promoting or counteracting DNA compaction?. FEBS Lett529:151–156
    [Google Scholar]
  21. Desvaux M., Hébraud M.. 2006; The protein secretion systems in Listeria : inside out bacterial virulence. FEMS Microbiol Rev30:774–805
    [Google Scholar]
  22. Doan T., Aymerich S.. 2003; Regulation of the central glycolytic genes in Bacillus subtilis : binding of the repressor CggR to its single DNA target sequence is modulated by fructose-1,6-bisphosphate. Mol Microbiol47:1709–1721
    [Google Scholar]
  23. Drews O., Weiss W., Reil G., Parlar H., Wait R., Görg A.. 2002; High pressure effects step-wise altered protein expression in Lactobacillus sanfranciscensis . Proteomics2:765–774
    [Google Scholar]
  24. Erijman L., Clegg R. M.. 1998; Reversible stalling of transcription elongation complexes by high pressure. Biophys J75:453–462
    [Google Scholar]
  25. Gao H., Aronson A. I.. 2004; The delta subunit of RNA polymerase functions in sporulation. Curr Microbiol48:401–404
    [Google Scholar]
  26. Glaser P., Frangeul L., Buchreiser C., Rusniok C., Amend A., Baquero F., Berche P., Bloecker H., Brandt P.. other authors 2001; Comparative genomics of Listeria species. Science294:849–852
    [Google Scholar]
  27. Gross M., Jaenicke R.. 1994; Proteins under pressure: the influence of high hydrostatic pressure on structure, function and assembly of proteins and protein complexes. Eur J Biochem221:617–630
    [Google Scholar]
  28. Hauben K. J. A., Bernaerts K., Michiels C. W.. 1998; Protective effect of calcium on inactivation of Escherichia coli by high hydrostatic pressure. J Appl Microbiol85:678–684
    [Google Scholar]
  29. Helloin E., Jansch L., Phan-Thanh L.. 2003; Carbon starvation survival of Listeria monocytogenes in planktonic state and in biofilm: a proteomic study. Proteomics3:2052–2064
    [Google Scholar]
  30. Hiles I. D., Gallagher M. P., Jamieson D. J., Higgins C. F.. 1987; Molecular characterization of the oligopeptide permease of Salmonella typhimurium . J Mol Biol195:125–142
    [Google Scholar]
  31. Hörmann S., Scheyhing C., Behr J., Pavlovic M., Ehrmann M., Vogel R. F.. 2006; Comparative proteome approach to characterize the high-pressure stress response of Lactobacillus sanfranciscensis DSM 20451. Proteomics6:1878–1885
    [Google Scholar]
  32. Huß V. A. R., Festl H., Schleifer K. H.. 1983; Studies on the spectrophotometric determination of DNA hybridization from renaturation rates. Syst Appl Microbiol4:184–192
    [Google Scholar]
  33. Ishii A., Oshima T., Sato T., Nakasone K., Mori H., Kato C.. 2005; Analysis of hydrostatic pressure effects on transcription in Escherichia coli by DNA microarray procedure. Extremophiles9:65–73
    [Google Scholar]
  34. Iwahashi H., Shimizu H., Odani M., Komatsu Y.. 2003; Piezophysiology of genome wide gene expression levels in the yeast Saccharomyces cerevisiae . Extremophiles7:291–298
    [Google Scholar]
  35. Jantzen M. M., Navas J., de Paz M., Rodriguez B., da Silva W. P., Nunez M., Martinez-Suarez J. V.. 2006; Evaluation of ALOA plating medium for its suitability to recover high pressure-injured Listeria monocytogenes from ground chicken meat. Lett Appl Microbiol43:313–317
    [Google Scholar]
  36. Jiang W., Hou Y., Inouye M.. 1997; CspA, the major cold-shock protein of Escherichia coli , is an RNA chaperone. J Biol Chem272:196–202
    [Google Scholar]
  37. Juang Y. L., Helmann J. D.. 1995; Pathway of promoter melting by Bacillus subtilis RNA polymerase at a stable RNA promoter: effects of temperature, delta protein, and sigma factor mutations. Biochemistry34:8465–8473
    [Google Scholar]
  38. Kaletunç G., Lee J., Alpas H., Bozoglu F.. 2004; Evaluation of structural changes induced by high hydrostatic pressure in Leuconostoc mesenteroides . Appl Environ Microbiol70:1116–1122
    [Google Scholar]
  39. Karatzas K. A. G., Valdramidis V. P., Wells-Bennik M. H. J.. 2005; Contingency locus in ctsR of Listeria monocytogenes Scott A: a strategy for occurrence of abundant piezotolerant isolates within clonal populations. Appl Environ Microbiol71:8390–8396
    [Google Scholar]
  40. Kawarai T., Wachi M., Ogino H., Furukawa S., Suzuki K., Ogihara H., Yamasaki M.. 2004; SulA-independent filamentation of Escherichia coli during growth after release from high hydrostatic pressure treatment. Appl Microbiol Biotechnol64:255–262
    [Google Scholar]
  41. Kazmierczak M. J., Mithoe S. C., Boor K. J., Wiedamann M.. 2003; Listeria monocytogenes σ B regulates stress and virulence functions. J Bacteriol185:5722–5734
    [Google Scholar]
  42. Khelef N., Lecuit M., Buchrieser C., Cabanes D., Dussurget O., Cossart P.. 2006; Listeria monocytogenes and the genus Listeria . In The Prokaryotes vol. 4 pp404–476 Edited by Dworkin M., Falkow S., Rosenberg E., Schleifer K. H., Stackebrandt E.. New York: Springer-Verlag;
  43. Kilimann K. V., Hartmann C., Delgado A., Vogel R. F., Ganzle M. G.. 2005; A fuzzy logic-based model for the multistage high-pressure inactivation of Lactococcus lactis ssp. cremoris MG 1363. Int J Food Microbiol98:89–105
    [Google Scholar]
  44. Koseki S., Yamamoto K.. 2006; pH and solute concentration of suspension media affect the outcome of high hydrostatic pressure treatment of Listeria monocytogenes . Int J Food Microbiol111:175–179
    [Google Scholar]
  45. Lane D. J.. 1991; 16S/23S Sequencing. In Nucleic Acid Techniques in Bacterial Systematics pp115–175 Edited by Stackebrandt E., Goodfellow M.. Chichester: John Wiley & Sons;
  46. Livak K. J., Schmittgen T. D.. 2001; Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔ C T Method. Methods25:402–408
    [Google Scholar]
  47. Lopez de Saro F. J., Yoshikawa N., Helmann J. D.. 1999; Expression, abundance, and RNA polymerase binding properties of the delta factor of Bacillus subtilis . J Biol Chem274:15953–15958
    [Google Scholar]
  48. Mackey B. M., Forestiere K., Isaacs N.. 1995; Factors affecting the resistance of Listeria monocytogenes to high hydrostatic-pressure. Food Biotechnol9:1–11
    [Google Scholar]
  49. Malone A. S., Chung Y. K., Yousef A. E.. 2006; Genes of Escherichia coli O157 : H7 that are involved in high-pressure resistance. Appl Environ Microbiol72:2661–2671
    [Google Scholar]
  50. Mañas P., Mackey B. M.. 2004; Morphological and physiological changes induced by high hydrostatic pressure in exponential- and stationary-phase cells of Escherichia coli : relationship with cell death. Appl Environ Microbiol70:1545–1554
    [Google Scholar]
  51. Marquis R. E., Bender G. R.. 1987; Barophysiology of prokaryotes and proton translocating ATPases. In Current Perspectives in High Pressure Biology pp65–73 Edited by Jannasch H. W., Marquis R. E., Zimmerman A. M.. London: Academic Press;
  52. Martin D. D., Bartlett D. H., Roberts M. F.. 2002; Solute accumulation in the deep-sea bacterium Photobacterium profundum . Extremophiles6:507–514
    [Google Scholar]
  53. Milohanic E., Glaser P., Coppée J.-Y., Frangeul L., Vega Y., Vázquez-Boland J. A., Kunst F., Cossart P., Buchrieser C.. 2003; Transcriptome analysis of Listeria monocytogenes identifies three groups of genes differently regulated by PrfA. Mol Microbiol47:1613–1625
    [Google Scholar]
  54. Morales P., Calzada J., Rodriguez B., de Paz M., Gaya P., Nunez M.. 2006; Effect of cheese water activity and carbohydrate content on the barotolerance of Listeria monocytogenes Scott A. J Food Prot69:1328–1333
    [Google Scholar]
  55. Nachin L., Nannmark U., Nystrom T.. 2005; Differential roles of the universal stress proteins of Escherichia coli in oxidative stress resistance, adhesion, and motility. J Bacteriol187:6265–6272
    [Google Scholar]
  56. Neidhardt F. C., Curtiss R. III, Ingraham J. L., Lin E. C. C., Low K. B. Jr, Magasanik B., Reznikoff W. S., Riley M., Schaechter M., Umbarger H. E.. 1996; Escherichia coli and Salmonella: Cellular and Molecular Biology , 2nd edn. Washington, DC: American Society for Microbiology;
  57. Niven G. W., Miles C. A., Mackey B. M.. 1999; The effects of hydrostatic pressure on ribosome conformation in Escherichia coli : an in vivo study using differential scanning calorimetry. Microbiology145:419–425
    [Google Scholar]
  58. Pounds S., Cheng C.. 2004; Improving false discovery rate estimation. Bioinformatics20:1737–1745
    [Google Scholar]
  59. Rieu A., Weidmann S., Garmyn D., Piveteau P., Guzzo J.. 2007; Differential expression pattern of the agr operon of Listeria monocytogenes EGD-e. Proceedings of the 16th International Symposium on Problems of ListeriosisSavannah, Georgia, USAMarch 20–23, 2007
    [Google Scholar]
  60. Ritz M., Tholozan J. L., Federighi M., Pilet M. F.. 2001; Morphological and physiological characterization of Listeria monocytogenes subjected to high hydrostatic pressure. Appl Environ Microbiol67:2240–2247
    [Google Scholar]
  61. Ritz M., Pilet M. F., Jugiau F., Rama F., Federighi M.. 2006; Inactivation of Salmonella Typhimurium and Listeria monocytogenes using high-pressure treatments: destruction or sublethal stress?. Lett Appl Microbiol42:357–362
    [Google Scholar]
  62. Rozen S., Skaletsky H.. 2000; Primer3 on the WWW for general users and for biologist programmers. In Bioinformatics Methods and Protocols: Methods in Molecular Biology pp365–386 Edited by Krawetz S., Misener S. Totowa: Humana Press;
  63. Schujman G. E., Paoletti L., Grossman A. D., de Mendoza D.. 2003; FapR, a bacterial transcription factor involved in global regulation of membrane lipid biosynthesis. Dev Cell4:663–672
    [Google Scholar]
  64. Seepersaud R., Needham R. H. V., Kim C. S., Jones A. L.. 2006; Abundance of the δ subunit of RNA polymerase is linked to the virulence of Streptococcus agalactiae . J Bacteriol188:2096–2105
    [Google Scholar]
  65. Semrad K., Green R., Schroeder R.. 2004; RNA chaperone activity of large ribosomal subunit proteins from Escherichia coli . RNA10:1855–1860
    [Google Scholar]
  66. Shen A., Kamp H. D., Gründling A., Higgins D. E.. 2006; A bifunctional O-GlcNAc transferase governs flagellar motility through anti-repression. Genes Dev20:3283–3295
    [Google Scholar]
  67. Smiddy M., O'Gorman L., Sleator R. D., Kerry J. P., Patterson M. F., Kelly A. L., Hill C.. 2005; Greater high-pressure resistance of bacteria in oysters than in buffer. Innov Food Sci Emerg Technol6:83–90
    [Google Scholar]
  68. Smyth G. K.. 2004; Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol3: Article 3 ()
    [Google Scholar]
  69. Sonenshein A. L.. 2005; CodY, a global regulator of stationary growth phase and virulence in Gram-positive bacteria. Curr Opin Microbiol8:203–207
    [Google Scholar]
  70. Storey J. D., Xiao W., Leek J. T., Tompkins R. G., Davis R. W.. 2005; Significance analysis of time course microarray experiments. Proc Natl Acad Sci U S A102:12837–12842
    [Google Scholar]
  71. Tasara T., Stephan R.. 2006; Cold stress tolerance of Listeria monocytogenes : a review of molecular adaptive mechanisms and food safety implications. J Food Prot69:1473–1484
    [Google Scholar]
  72. Toepfl S., Mathys A., Heinz V., Knorr D.. 2006; Potential of high hydrostatic pressure and pulsed electric fields for energy efficient and environmentally friendly food processing. Food Rev Int22:405–423
    [Google Scholar]
  73. Trémoulet F., Duché O., Namane A., Martinie B., Labadie J. C.. European Listeria Genome Consortium 2002; Comparison of protein patterns of Listeria monocytogenes grown in biofilm or in planktonic mode by proteomic analysis. FEMS Microbiol Lett210:25–31
    [Google Scholar]
  74. Ulmer H. M., Ganzle M. G., Vogel R. F.. 2000; Effects of high pressure on survival and metabolic activity of Lactobacillus plantarum TMW1. 460 . Appl Environ Microbiol66:3966–3973
    [Google Scholar]
  75. Weiss D. S.. 2004; Bacterial cell division and the septal ring. Mol Microbiol54:588–597
    [Google Scholar]
  76. Welch T. J., Farewell A., Neidhardt F. C., Bartlett D. H.. 1993; Stress response of Escherichia coli to elevated hydrostatic pressure. J Bacteriol175:7170–7177
    [Google Scholar]
  77. Wemekamp-Kamphuis H. H., Wouters J. A., de Leeuw P. P. L. A., Hain T., Chakraborty T., Abee T.. 2004; Identification of sigma factor sigmaB-controlled genes and their impact on acid stress, high hydrostatic pressure, and freeze survival in Listeria monocytogenes EGD-e. Appl Environ Microbiol70:3457–3466
    [Google Scholar]
  78. Wieser M., Busse H. J.. 2000; Rapid identification of Staphylococcus epidermidis . Int J Syst Evol Microbiol50:1087–1093
    [Google Scholar]
  79. Wouters P. C., Glaasker E., Smelt J. P. P. M.. 1998; Effects of high pressure on inactivation kinetics and events related to proton efflux in Lactobacillus plantarum . Appl Environ Microbiol64:509–514
    [Google Scholar]
  80. Xia X., McClelland M., Wang Y.. 2005; WebArray: an online platform for microarray data analysis. BMC Bioinformatics6:306–311
    [Google Scholar]
  81. Yarwood J. M., Bartels D. J., Volper E. M., Greenberg E. P.. 2004; Quorum sensing in Staphylococcus aureus biofilms. J Bacteriol186:1838–1850
    [Google Scholar]
  82. Yayanos A. A., Pollard E. C.. 1969; A study of the effects of hydrostatic pressure on macromolecular synthesis in Escherichia coli . Biophys J9:1464–1482
    [Google Scholar]
  83. Zheng D., Constantinidou C., Hobman J. L., Minchin S. D.. 2004; Identification of the CRP regulon using in vitro and in vivo transcriptional profiling. Nucleic Acids Res32:5874–5893
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.2007/010314-0
Loading
/content/journal/micro/10.1099/mic.0.2007/010314-0
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

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