Listeria monocytogenes grown at 7°C shows reduced acid survival and an altered transcriptional response to acid shock compared to L. Monocytogenes grown at 37°C

Applied and Environmental Microbiology

Volumn 78, Issue 11, 2012, Pages 3824-3836

  Ivy, R A ^a   Wiedmann, M ^a   Boor, K J ^a  

^a Cornell University ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACID SURVIVAL; ACIDIC ENVIRONMENT; BRAIN HEART INFUSIONS; DIFFERENTIAL EXPRESSIONS; FOOD-BORNE PATHOGENS; GASTRIC FLUIDS; GENE TRANSCRIPTIONS; GROWTH PHASE; LISTERIA MONOCYTOGENES; LISTERIOSIS; LOW TEMPERATURES; MICROARRAY TRANSCRIPTOMIC ANALYSIS; MONOCYTOGENES; PROPHAGES; READY-TO-EAT FOODS; STATIONARY PHASE; TRANSCRIPTIONAL REGULATOR; TRANSCRIPTIONAL RESPONSE;

CELLS; CYTOLOGY; FOOD STORAGE; GENES; LISTERIA; PATHOGENS; THERMAL LOGGING; TRANSCRIPTION;

CHEMICAL RESISTANCE;

BACTERIAL PROTEIN;

BACTERIUM; CELL ORGANELLE; GENE; LOW TEMPERATURE; NUMERICAL MODEL; PHYSIOLOGICAL RESPONSE; TEMPERATURE EFFECT;

ADAPTATION; ARTICLE; BACTERIAL COUNT; COLD; CULTURE MEDIUM; DNA MICROARRAY; FOOD STORAGE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HEAT SHOCK RESPONSE; HUMAN; LISTERIA MONOCYTOGENES; METABOLISM; MICROBIAL VIABILITY; PH; PHYSIOLOGY; STOMACH ACID;

ADAPTATION, PHYSIOLOGICAL; BACTERIAL PROTEINS; COLD TEMPERATURE; COLONY COUNT, MICROBIAL; CULTURE MEDIA; FOOD STORAGE; GASTRIC ACID; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; HEAT-SHOCK RESPONSE; HUMANS; HYDROGEN-ION CONCENTRATION; LISTERIA MONOCYTOGENES; MICROBIAL VIABILITY; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS;

LISTERIA MONOCYTOGENES;

EID: 84864087772     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00051-12     Document Type: Article

References (70)

1. Abram F, et al. 2008. Identification of components of the sigma B regulon in Listeria monocytogenes that contribute to acid and salt tolerance. Appl. Environ. Microbiol. 74:6848-6858.
2. Álvarez-Ordóñez A, Fernandez A, Bernardo A, López M. 2010. Arginine and lysine decarboxylases and the acid tolerance response of Salmonella Typhimurium. Int. J. Food Microbiol. 136:278 -282.
3. Audits International/FDA. 1999. 1999 U.S. food temperature evaluation. U.S. Food and Drug Administration, Washington, DC. http://foodrisk.org/default/assets/File/Audits-FDA_temp_study.pdf.
4. Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B (Stat. Method.) 1:289 -300.
5. Berry DB, et al. 2011. Multiple means to the same end: the genetic basis of acquired stress resistance in yeast. PLoS Genet. 7:e1002353.
6. Bhagwat AA, et al. 2003. Computational methods and evaluation of RNA stabilization reagents for genome-wide expression studies. J. Microbiol. Methods 55:399-409.
7. Bore E, Langsrud S, Langsrud O, Rode TM, Holck A. 2007. Acid-shock responses in Staphylococcus aureus investigated by global gene expression analysis. Microbiology 153:2289 -2303.
8. Chan YC, Raengpradub S, Boor KJ, Wiedmann M. 2007. Microarraybased characterization of the Listeria monocytogenes cold regulon in logand stationary-phase cells. Appl. Environ. Microbiol. 73:6484-6498.
9. B-dependent survival under environmental, energy, and intracellular stress conditions in Listeria monocytogenes. Appl. Environ. Microbiol. 70:5349- 5356.
10. Chaturongakul S, Boor KJ. 2006. Sigma B activation under environmental and energy stress conditions in Listeria monocytogenes. Appl. Environ. Microbiol. 72:5197-5203.
11. Chaturongakul S, et al. 2011. Transcriptomic and phenotypic analyses identify coregulated, overlapping regulons among PrfA, CtsR, HrcA, and the alternative sigma factors sigma B, sigma C, sigma H, and sigma L in Listeria monocytogenes. Appl. Environ. Microbiol. 77:187-200.
12. Conte MP, et al. 2002. Effect of acid adaptation on the fate of Listeria monocytogenes in THP-1 human macrophages activated by gamma interferon. Infect. Immun. 70:4369-4378.
13. Cotter PD, Gahan CGM, Hill C. 2001. A glutamate decarboxylase system protects Listeria monocytogenes in gastric fluid. Mol. Microbiol. 40:465- 475.
14. Cotter PD, Ryan S, Gahan CGM, Hill C. 2005. Presence of GadD1 glutamate decarboxylase in selected Listeria monocytogenes strains is associated with an ability to grow at low pH. Appl. Environ. Microbiol. 71: 2832-2839.
15. Davis MJ, Coote PJ, O'Byrne CP. 1996. Acid tolerance in Listeria monocytogenes: the adaptive acid tolerance response (ATR) and growth-phasedependent acid resistance. Microbiology 142:2975-2982.
16. Dykes GA, Moorhead SM. 2000. Survival of osmotic and acid stress by Listeria monocytogenes strains of clinical or meat origin. Int. J. Food Microbiol. 56:161-166.
17. Ehira S, Teramoto H, Inui M, Yukawa H. 2009. Regulation of Corynebacterium glutamicum heat shock response by the extracytoplasmicfunction sigma factor SigH and transcriptional regulators HspR and HrcA. J. Bacteriol. 191:2964 -2972.
18. Ferreira A, O'Byrne CP, Boor KJ. 2001. Role of SigB in heat, ethanol, acid, and oxidative stress resistance and during carbon starvation in Listeria monocytogenes. Appl. Environ. Microbiol. 67:4454-4457.
19. B in survival of lethal acidic conditions and in the acquired acid tolerance response. Appl. Environ. Microbiol. 69:2692-2698.
20. Ferreira V, et al. 2011. Diverse geno- and phenotypes of persistent Listeria monocytogenes isolates from fermented meat sausage production facilities in Portugal. Appl. Environ. Microbiol. 77:2701-2715.
21. Gaillot O, Pellegrini E, Bregenholt S, Nair S, Berche P. 2000. The ClpP serine protease is essential for the intracellular parasitism and virulence of Listeria monocytogenes. Mol. Microbiol. 35:1286 -1294.
22. Garner MR, James KE, Callahan MC, Wiedmann M, Boor KJ. 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. Gohmann S, Leimeister-Wachter M, Schiltz E, Goebel W, Chakraborty T. 1990. Characterization of a Listeria monocytogenes-specific protein capable of inducing delayed hypersensitivity in Listeria-immune mice. Mol. Microbiol. 4:1091-1099.
24. Hanawa T, et al. 1999. The Listeria monocytogenes DnaK chaperone is required for stress tolerance and efficient phagocytosis with macrophages. Cell Stress Chaperones 4:118 -128.
25. Harrison C. 2003. GrpE, a nucleotide exchange factor for DnaK. Cell Stress Chaperones 8:218 -224.
26. Hodgson DA. 2000. Generalized transduction of serotype 1/2 and serotype 4b strains of Listeria monocytogenes. Mol. Microbiol. 35:312-323.
27. Hu Y, Coates AR. 1999. Transcription of two sigma 70 homologue genes, sigA and sigB, in stationary-phase Mycobacterium tuberculosis. J. Bacteriol. 181:469-476.
28. Hu Y, et al. 2007. Transcriptomic and phenotypic analyses suggest a network between the transcriptional regulators HrcA and SigB in Listeria monocytogenes. Appl. Environ. Microbiol. 73:7981-7991.
29. Hu Y, et al. 2007. Phenotypic and transcriptomic analyses demonstrate interactions between the transcriptional regulators CtsR and sigma B in Listeria monocytogenes. Appl. Environ. Microbiol. 73:7967-7980.
30. Karatzas K-AG, Brennan O, Heavin S, Morrissey J, O'Byrne CP. 2010. Intracellular accumulation of high levels of -aminobutyrate by Listeria monocytogenes 10403S in response to low pH: uncoupling of -aminobutyrate synthesis from efflux in a chemically defined medium. Appl. Environ. Microbiol. 76:3529 -3537.
31. Kazmierczak MJ, Mithoe SC, Boor KJ, Wiedmann M. 2003. Listeria monocytogenes sigma B regulates stress response and virulence functions. J. Bacteriol. 185:5722-5734.
32. Kazmierczak MJ, Wiedmann M, Boor KJ. 2006. Contributions of Listeria monocytogenes sigma B and PrfA to expression of virulence and stress response genes during extra- and intracellular growth. Microbiology 152: 1827-1838.
33. Klarsfeld AD, Goossens PL, Cossart P. 1994. Five Listeria monocytogenes genes preferentially expressed in infected mammalian cells: plcA, purH, purD, pyrE and an arginine ABC transporter gene, arpJ. Mol. Microbiol. 13:585-597.
34. Kress W, Maglica Z, Weber-Ban E. 2009. Clp chaperone-proteases: structure and function. Res. Microbiol. 160:618-628.
35. Lemos JA, Chen YY, Burne RA. 2001. Genetic and physiologic analysis of the groE operon and role of the HrcA repressor in stress gene regulation and acid tolerance in Streptococcus mutans. J. Bacteriol. 183:6074-6084.
36. Lou Y, Yousef AE. 1997. Adaptation to sublethal environmental stresses protects Listeria monocytogenes against lethal preservation factors. Appl. Environ. Microbiol. 63:1252-1255.
37. Martin-Galiano AJ, et al. 2005. Transcriptional analysis of the acid tolerance response in Streptococcus pneumoniae. Microbiology 151:3935- 3946.
38. H. J. Bacteriol. 191: 3965-3980.
39. Nair S, Derré I, Msadek T, Gaillot O, Berche P. 2000. CtsR controls class III heat shock gene expression in the human pathogen Listeria monocytogenes. Mol. Microbiol. 35:800-811.
40. Nelson KE, et al. 2004. Whole genome comparisons of serotype 4b and 1/2a 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.
41. O'Driscoll B, Gahan CG, Hill C. 1996. Adaptive acid tolerance response in Listeria monocytogenes: isolation of an acid-tolerant mutant which demonstrates increased virulence. Appl. Environ. Microbiol. 62:1693-1698.
42. Okada Y, et al. 2006. The sigma factor RpoN (sigma54) is involved in osmotolerance in Listeria monocytogenes. FEMS Microbiol. Lett. 263:54-60.
43. Olesen I, Vogensen FK, Jespersen L. 2009. Gene transcription and virulence potential of Listeria monocytogenes strains after exposure to acidic and NaCl stress. Foodborne Pathog. Dis. 6:669-680.
44. Ollinger J, Bowen B, Wiedmann M, Boor KJ, Bergholz TM. 2009. Listeria monocytogenes sigma B modulates PrfA-mediated virulence factor expression. Infect. Immun. 77:2113-2124.
45. Patchett RA, Watson N, Fernandez PS, Kroll RG. 1996. The effect of temperature and growth rate on the susceptibility of Listeria monocytogenes to environmental stress conditions. Lett. Appl. Microbiol. 22:121- 124.
46. Phan-Thanh L, Mahouin F. 1999. A proteomic approach to study the acid response in Listeria monocytogenes. Electrophoresis 20:2214 -2224.
47. Raengpradub S, Wiedmann M, Boor KJ. 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.
48. Richard HT, Foster JW, Laskin AI, Bennett JW, Gadd GM. 2003. Acid resistance in Escherichia coli. Adv. Appl. Microbiol. 52:167-186.
49. 54) gene from Listeria monocytogenes is involved in resistance to mesentericin Y105, an antibacterial peptide from Leuconostoc mesenteroides. J. Bacteriol. 179:7591-7594.
50. Rohde KH, Abramovitch RB, Russell DG. 2007. Mycobacterium tuberculosis invasion of macrophages: linking bacterial gene expression to environmental cues. Cell Host Microbe 2:352-364.
51. Rouquette C, de Chastellier C, Nair S, Berche P. 1998. The ClpC ATPase of Listeria monocytogenes is a general stress protein required for virulence and promoting early bacterial escape from the phagosome of macrophages. Mol. Microbiol. 27:1235-1245.
52. Russell TL, et al. 1993. Upper gastrointestinal pH in seventy-nine healthy, elderly, North American men and women. Pharm. Res. 10:187-196.
53. Ryan S, Hill C, Gahan CGM. 2008. Acid stress responses in Listeria monocytogenes. Adv. Appl. Microbiol. 65:67-91.
54. Samelis J, Ikeda JS, Sofos JN. 2003. Evaluation of the pH-dependent, stationary-phase acid tolerance in Listeria monocytogenes and Salmonella Typhimurium DT104 induced by culturing in media with 1% glucose: a comparative study with Escherichia coli O157:H7. J. Appl. Microbiol. 95: 563-575.
55. Schaferkordt S, Chakraborty T. 1997. Identification, cloning, and characterization of the Lma operon, whose gene products are unique to Listeria monocytogenes. J. Bacteriol. 179:2707-2716.
56. Schubert ML. 2009. Gastric exocrine and endocrine secretion. Curr. Opin. Gastroenterol. 25:529 -536.
57. Scortti M, Monzo HJ, Lacharme-Lora L, Lewis DA, Vazquez-Boland JA. 2007. The PrfA virulence regulon. Microb. Infect. 9:1196 -1207.
58. Stasiewicz MJ, Wiedmann M, Bergholz TM. 2010. The combination of lactate and diacetate synergistically reduces cold growth in brain heart infusion broth across Listeria monocytogenes lineages. J. Food Prot. 73: 631-640.
59. Subramanian A, et al. 2005. Gene set enrichment analysis: A knowledgebased approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. U. S. A. 102:15545-15550.
60. Toledo-Arana A, et al. 2009. The Listeria transcriptional landscape from saprophytism to virulence. Nature 459:950 -956.
61. United States Department of Agriculture Food Safety and Inspection Service. 2011. Basics for handling food safely. U.S. Department of Agriculture, Washington, DC. http://www.fsis.usda.gov/PDF/Basics_for_Safe _Food_Handling.pdf.
62. van der Veen S, et al. 2007. The heat-shock response of Listeria monocytogenes comprises genes involved in heat shock, cell division, cell wall synthesis, and the SOS response. Microbiology 153:3593-3607.
63. van der Veen S, et al. 2010. The SOS response of Listeria monocytogenes is involved in stress resistance and mutagenesis. Microbiology 156:374- 384.
64. Waldor MK, Friedman DI. 2005. Phage regulatory circuits and virulence gene expression. Curr. Opin. Microbiol. 8:459-465.
65. Walker SJ, Archer P, Banks JG. 1990. Growth of Listeria monocytogenes at refrigeration temperatures. J. Appl. Microbiol. 68:157-162.
66. Wall T, et al. 2007. The early response to acid shock in Lactobacillus reuteri involves the ClpL chaperone and a putative cell wall-altering esterase. Appl. Environ. Microbiol. 73:3924 -3935.
67. Wemekamp-Kamphuis HH, et al. 2004. Identification of sigma factor sigma B-controlled genes and their impact on acid stress, high hydrostatic pressure, and freeze survival in Listeria monocytogenes EGD-e. Appl. Environ. Microbiol. 70:3457-3466.
68. Wiedmann M, Arvik TJ, Hurley RJ, Boor KJ. 1998. General stress transcription factor sigma B and its role in acid tolerance and virulence of Listeria monocytogenes. J. Bacteriol. 180:3650 -3656.
69. Zink R, Loessner MJ. 1992. Classification of virulent and temperate bacteriophages of Listeria spp. on the basis of morphology and protein analysis. Appl. Environ. Microbiol. 58:296 -302.
70. Zink R, Loessner MJ, Scherer S. 1995. Characterization of cryptic prophages (monocins) in Listeria and sequence analysis of a holin/endolysin gene. Microbiology 141:2577-2584.