Functional consequences of genome evolution in Listeria monocytogenes: The lmo0423 and lmo0422 genes encode σC and LstR, a lineage II-specific heat shock system

Journal of Bacteriology

Volumn 187, Issue 21, 2005, Pages 7243-7253

  Zhang, Chaomei ^a   Nietfeldt, Joe ^a   Zhang, Min ^a   Benson, Andrew K ^a  

^a UNIVERSITY OF NEBRASKA LINCOLN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN FTSW; PROTEIN RODA; REGULATOR PROTEIN; RNA POLYMERASE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENE; CELL LINEAGE; FTSW GENE; GENETIC RESISTANCE; HEAT TOLERANCE; LISTERIA MONOCYTOGENES; LMO0422 GENE; LMO0423 GENE; MICROBIAL DIVERSITY; MOLECULAR EVOLUTION; NONHUMAN; NULL ALLELE; OPERON; PADR GENE; PHYLOGENY; PRIORITY JOURNAL; PROMOTER REGION; REGULATOR GENE; RODA GENE; SEROTYPE; SIGC GENE; TRANSCRIPTION REGULATION;

ADAPTATION, PHYSIOLOGICAL; BACTERIAL PROTEINS; COLONY COUNT, MICROBIAL; DNA-BINDING PROTEINS; EVOLUTION; EVOLUTION, MOLECULAR; GENE DELETION; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; GENOME, BACTERIAL; HEAT; LISTERIA MONOCYTOGENES; MEMBRANE PROTEINS; MULTIGENE FAMILY; OPERON; PHYLOGENY; PROMOTER REGIONS (GENETICS); REPRESSOR PROTEINS; RNA, BACTERIAL; RNA, MESSENGER; SEQUENCE HOMOLOGY; SIGMA FACTOR; SYNTENY; TRANSCRIPTION, GENETIC;

BACTERIA (MICROORGANISMS); LISTERIA; LISTERIA MONOCYTOGENES;

EID: 27144467458     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.187.21.7243-7253.2005     Document Type: Article

References (66)

1. Arous, S., C. Buchrieser, P. Folio, P. Glaser, A. Namane, M. Hebraud, and Y. Hechard. 2004. Global analysis of gene expression in an rpoN mutant of Listeria monocytogenes. Microbiology 150:1581-1590.
2. B from Listeria monocytogenes and its role in osmotolerance. J. Bacteriol. 180:4547-4554.
3. B in adaptation of Listeria monocytogenes to growth at low temperature. J. Bacteriol. 182:7083-7087.
4. Begg, K. J., and W. D. Donachie. 1985. Cell shape and division in Escherichia coli: experiments with shape and division mutants. J. Bacteriol. 163:615-622.
5. Begg, K. J., B. G. Spratt, and W. D. Donachie. 1986. Interaction between membrane proteins PBP3 and RodA is required for normal cell shape and division in Escherichia coli. J. Bacteriol. 167:1004-1008.
6. B- dependent promoter of the Bacillus subtilis sigB operon is induced by heat shock. J. Bacteriol. 175:1929-1935.
7. Bishop, D. K., and D. J. Hinrichs. 1987. Adoptive transfer of immunity to Listeria monocytogenes. The influence of in vitro stimulation on lymphocyte subset requirements. J. Immunol. 139:2005-2009.
8. Botta, G. A., and J. T. Park. 1981. Evidence for involvement of penicillin-binding protein 3 in murein synthesis during septation but not during cell elongation. J. Bacteriol. 145:333-340.
9. 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.
10. Canepari, P., C. Signoretto, M. Boaretti, and M. Del Mar Lleo. 1997. Cell elongation and septation are two mutually exclusive processes in Escherichia coli. Arch. Microbiol. 168:152-159.
11. B, in Listeria monocytogenes. J. Bacteriol. 186:794-802.
12. Church, G. M., and W. Gilbert. 1984. Genomic sequencing. Proc. Natl. Acad. Sci. USA 81:1991-1995.
13. Cotter, P. D., N. Emerson, C. G. Gahan, and C. Hill. 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.
14. Dancz, C. E., A. Haraga, D. A. Portnoy, and D. E. Higgins. 2002. Inducible control of virulence gene expression in Listeria monocytogenes: temporal requirement of listeriolysin O during intracellular infection. J. Bacteriol. 184:5935-5945.
15. de Pedro, M. A., W. D. Donachie, J. V. Holtje, and H. Schwarz. 2001. Constitutive septal murein synthesis in Escherichia coli with impaired activity of the morphogenetic proteins RodA and penicillin-binding protein 2. J. Bacteriol. 183:4115-4126.
16. de Pedro, M. A., J. C. Quintela, J. V. Holtje, and H. Schwarz. 1997. Murein segregation in Escherichia coli. J. Bacteriol. 179:2823-2834.
17. Doumith, M., C. Cazalet, N. Simoes, L. Frangeul, C. Jacquet, F. Kunst, P. Martin, P. Cossart, P. Glaser, and C. Buchrieser. 2004. New aspects regarding evolution and virulence of Listeria monocytogenes revealed by comparative genomics and DNA arrays. Infect. Immun. 72:1072-1083.
18. Dussurget, O., D. Cabanes, P. Dehoux, M. Lecuit, C. Buchrieser, P. Glaser, and P. Cossart. 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.
19. Evans, M. R., B. Swaminathan, L. M. Graves, E. Altermann, T. R. Klaenhammer, R. C. Fink, S. Kernodle, and S. Kathariou. 2004. Genetic markers unique to Listeria monocytogenes serotype 4b differentiate epidemic clone II (hot dog outbreak strains) from other lineages. Appl. Environ. Microbiol. 70:2383-2390.
20. Felsenstein, J. 1988. Phylogenies from molecular sequences: inference and reliability. Annu. Rev. Genet. 22:521-565.
21. Glaser, P., L. Frangeul, C. Buchrieser, C. Rusniok, A. Amend, F. Baquero, P. Berche, H. Bloecker, P. Brandt, T. Chakraborty, A. Charbit, F. Chetouani, E. Couve, A. de Daruvar, P. Dehoux, E. Domann, G. Dominguez-Bernal, E. Duchaud, L. Durant, O. Dussurget, K. D. Entian, H. Fsihi, F. Garcia-del Portillo, P. Garrido, L. Gautier, W. Goebel, N. Gomez-Lopez, T. Hain, J. Hauf, D. Jackson, L. M. Jones, U. Kaerst, J. Kreft, M. Kuhn, F. Kunst, G. Kurapkat, E. Madueno, A. Maitournam, J. M. Vicente, E. Ng, H. Nedjari, G. Nordsiek, S. Novella, B. de Pablos, J. C. Perez-Diaz, R. Purcell, B. Remmel, M. Rose, T. Schlueter, N. Simoes, A. Tierrez, J. A. Vazquez-Boland, H. Voss, J. Wehland, and P. Cossart. 2001. Comparative genomics of Listeria species. Science 294:849-852.
22. Gray, M. J., R. N. Zadoks, E. D. Fortes, B. Dogan, S. Cai, Y. Chen, V. N. Scott, D. E. Gombas, K. J. Boor, and M. Wiedmann. 2004. Listeria monocytogenes isolates from foods and humans form distinct but overlapping populations. Appl. Environ. Microbiol. 70:5833-5841.
23. Gury, J., L. Barthelmebs, N. P. Tran, C. Divies, and J. F. Cavin. 2004. Cloning, deletion, and characterization of PadR, the transcriptional repressor of the phenolic acid decarboxylasc-encoding padA gene of Lactobacillus plantarum. Appl. Environ. Microbiol. 70:2146-2153.
24. Hanawa, T., M. Kai, S. Kamiya, and T. Yamamoto. 2000. Cloning, sequencing, and transcriptional analysis of the dnaK heat shock operon of Listeria monocytogenes. Cell Stress Chaperones 5:21-29.
25. Helmann, J. D. 2002. The extracytoplasmic function (ECF) sigma factors. Adv. Microb. Physiol. 46:47-110.
26. Henriques, A. O., H. de Lencastre, and P. J. Piggot. 1992. A Bacillus subtilis morphogene cluster that includes spoVE is homologous to the mra region of Escherichia coli. Biochimie 74:735-748.
27. Henriques, A. O., P. Glaser, P. J. Piggot, and C. P. Moran, Jr. 1998. Control of cell shape and elongation by the rodA gene in Bacillus subtilis. Mol. Microbiol. 28:235-247.
28. Herd, M., and C. Kocks. 2001. Gene fragments distinguishing an epidemic-associated strain from a virulent prototype strain of Listeria monocytogenes belong to a distinct functional subset of genes and partially cross-hybridize with other Listeria species. Infect. Immun. 69:3972-3979.
29. Hopp, T. P., and K. R. Woods. 1981. Prediction of protein antigenic determinants from amino acid sequences. Proc. Natl. Acad. Sci. USA 78:3824-3828.
30. X protein is an extracytoplasmic function sigma factor contributing to survival at high temperature. J. Bacteriol. 179:2915-2921.
31. Jacquet, C., E. Gouin, D. Jeannel, P. Cossart, and J. Recourt. 2002. Expression of ActA, Ami, InlB, and listeriolysin O in Listeria monocytogenes of human and food origin. Appl. Environ. Microbiol. 68:616-622.
32. Jeffers, G. T., J. L. Bruce, P. L. McDonough, J. Scarlett, K. J. Boor, and M. Wiedmann. 2001. Comparative genetic characterization of Listeria monocytogenes isolates from human and animal listeriosis cases. Microbiology 147: 1095-1104.
33. Karatzas, K. A., J. A. Wouters, C. G. Gahan, C. Hill, T. Abee, and M. H. Bennik. 2003. The CtsR regulator of Listeria monocytogenes contains a variant glycine repeat region that affects piezotolerance, stress resistance, motility and virulence. Mol. Microbiol. 49:1227-1238.
34. B regulates stress response and virulence functions. J. Bacteriol. 185:5722-5734.
35. Konyecsni, W. M., and V. Deretic. 1990. DNA sequence and expression analysis of algP and algQ, components of the multigene system transcriptionally regulating mucoidy in Pseudomonas aeruginosa: algP contains multiple direct repeats. J. Bacteriol. 172:2511-2520.
36. Kruger, E., D. Zuhlke, E. Witt, H. Ludwig, and M. Hecker. 2001. Clp-mediated proteolysis in gram-positive bacteria is autoregulated by the stability of a repressor. EMBO J. 20:852-863.
37. Kyte, J., and R. F. Doolittle. 1982. A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157:105-132.
38. Lauer, P., M. Y. Chow, M. J. Loessner, D. A. Portnoy, and R. Calendar. 2002. Construction, characterization, and use of two Listeria monocytogenes site-specific phage integration vectors. J. Bacteriol. 184:4177-4186.
39. Liu, S., J. E. Graham, L. Bigelow, P. D. Morse II, and B. J. Wilkinson. 2002. Identification of Listeria monocytogenes genes expressed in response to growth at low temperature. Appl. Environ. Microbiol. 68:1697-1705.
40. Mead, P. S., L. Slutsker, V. Dietz, L. F. McCaig, J. S. Bresee, C. Shapiro, P. M. Griffin, and R. V. Tauxe. 1999. Food-related illness and death in the United States. Emerg. Infect. Dis. 5:607-625.
41. Milohanic, E., P. Glaser, J. Y. Coppee, L. Frangeul, Y. Vega, J. A. Vazquez-Boland, F. Kunst, P. Cossart, and C. Buchrieser. 2003. Transcriptome analysis of Listeria monocytogenes identifies three groups of genes differently regulated by PrfA. Mol. Microbiol. 47:1613-1625.
42. Nadon, C. A., B. M. Bowen, M. Wiedmann, and K. J. Boor. 2002. Sigma B contributes to PrfA-mediated virulence in Listeria monocytogenes. Infect. Immun. 70:3948-3952.
43. Nadon, C. A., D. L. Woodward, C. Young, F. G. Rodgers, and M. Wiedmann. 2001. Correlations between molecular subtyping and serotyping of Listeria monocytogenes. J. Clin. Microbiol. 39:2704-2707.
44. Nair, S., I. Derre, T. Msadek, O. Gaillot, and P. Berche. 2000. CtsR controls class III heat shock gene expression in the human pathogen Listeria monocytogenes. Mol. Microbiol. 35:800-811.
45. 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 1/2a strains of the food-borne pathogen Listeria monocytogenes reveal new insights into the core genome components of this species. Nucleic Acids Res. 32:2385-2395.
46. Park, J. T., and L. G. Burman. 1985. Elongation of the murein sacculus of Escherichia coli. Ann. Inst. Pasteur Microbiol. 136A:51-58.
47. Piffaretti, J. C., H. Kressebuch, M. Aeschbacher, J. Bille, E. Bannerman, J. M. Musser, R. K. Selander, and J. Recourt. 1989. Genetic characterization of clones of the bacterium Listeria monocytogenes causing epidemic disease. Proc. Natl. Acad. Sci. USA 86:3818-3822.
48. Rasmussen, O. F., P. Skouboe, L. Dons, L. Rossen, and J. E. Olsen. 1995. Listeria monocytogenes exists in at least three evolutionary lines: evidence from flagellin, invasive associated protein and listeriolysin O genes. Microbiology 141:2053-2061.
49. Saitou, N., and M. Nei. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4:406-425.
50. Schulz, A., and W. Schumann. 1996. hrcA, the first gene of the Bacillus subtilis dnaK operon encodes a negative regulator of class I heat shock genes. J. Bacteriol. 178:1088-1093.
51. Schumann, W. 2003. The Bacillus subtilis heat shock stimulon. Cell Stress Chaperones 8:207-217.
52. Simon, R., U. Priefer, and A. Puhler. 1982. A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in gram-negative bacteria. Biotechnology 1:784-791.
53. Sleator, R. D., J. Wouters, C. G. Gahan, T. Abee, and C. Hill. 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.
54. Smith, K., and P. Youngman. 1992. Use of a new integrational vector to investigate compartment-specific expression of the Bacillus subtilis spoIIM gene. Biochimie 74:705-711.
55. Spratt, B. G. 1975. Distinct penicillin binding proteins involved in the division, elongation, and shape of Escherichia coli K12. Proc. Natl. Acad. Sci. USA 72:2999-3003.
56. B-dependent expression patterns of compatible solute transporter genes opuCA and lmoI421 and the conjugated bile salt hydrolase gene bsh in Listeria monocytogenes. Microbiology 149:3247-3256.
57. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
58. Todd, E. 1990. Epidemiology of foodborne illness: North America. Lancet 336:788-790.
59. Vines, A., M. W. Reeves, S. Hunter, and B. Swaminathan. 1992. Restriction fragment length polymorphism in four virulence-associated genes of Listeria monocytogenes. Res. Microbiol. 143:281-294.
60. B-dependent general stress regulon confers multiple stress resistance in Bacillus subtilis. J. Bacteriol. 181:3942-3948.
61. Ward, T. J., L. Gorski, M. K. Borucki, R. E. Mandrell, J. Hutchins, and K. Pupedis. 2004. Intraspecific phylogeny and lineage group identification based on the prfA virulence gene cluster of Listeria monocytogenes. J. Bacteriol. 186:4994-5002.
62. Wemekamp-Kamphuis, H. H., J. A. Wouters, R. D. Sleator, C. G. Gahan, C. Hill, and T. Abee. 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.
63. B and its role in acid tolerance and virulence of Listeria monocytogenes. J. Bacteriol. 180:3650-3656.
64. Wientjes, F. B., and N. Nanninga. 1989. Rate and topography of peptidoglycan synthesis during cell division in Escherichia coli: concept of a leading edge. J. Bacteriol. 171:3412-3419.
65. Zhang, C., M. Zhang, J. Ju, J. Nietfeldt, J. Wise, P. M. Terry, M. Olson, S. D. Kachman, M. Wiedmann, M. Samadpour, and A. K. Benson. 2003. Genome diversification in phylogenetic lineages I and II of Listeria monocytogenes: identification of segments unique to lineage II populations. J. Bacteriol. 185:5573-5584.
66. Zheng, W., and S. Kathariou. 1995. Differentiation of epidemic-associated strains of Listeria monocytogenes by restriction fragment length polymorphism in a gene region essential for growth at low temperatures (4°C). Appl. Environ. Microbiol. 61:4310-4314.