ChIP-seq and transcriptome analysis of the OmpR regulon of Salmonella enterica serovars Typhi and Typhimurium reveals accessory genes implicated in host colonization

Molecular Microbiology

Volumn 87, Issue 3, 2013, Pages 526-538

  Perkins, Timothy T ^a   Davies, Mark R ^a   Klemm, Elizabeth J ^a   Rowley, Gary ^b   Wileman, Thomas ^a   James, Keith ^a   Keane, Thomas ^a   Maskell, Duncan ^c   Hinton, Jay C D ^d   Dougan, Gordon ^a   Kingsley, Robert A ^a  

^a WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^b UNIVERSITY OF EAST ANGLIA   (United Kingdom)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

MURAMIC ACID; N ACETYLMURAMIC ACID; OUTER MEMBRANE PROTEIN REGULATOR; SIALIC ACID; STREPTOMYCIN; TRANSCRIPTOME; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GENE; BACTERIAL GROWTH; BINDING KINETICS; BINDING SITE; CARBON SOURCE; CECUM; CHROMATIN IMMUNOPRECIPITATION; COLITIS; DISEASE MODEL; ESCHERICHIA COLI; FEMALE; GENE CONTROL; GENE EXPRESSION; GENE IDENTIFICATION; GENE LOCATION; GENE MUTATION; GENETIC ASSOCIATION; GENETIC TRANSCRIPTION; ILEUM; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OPERON; ORTHOLOGY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DETERMINATION; REGULON; RNA SEQUENCE; SALMONELLA TYPHI; SALMONELLA TYPHIMURIUM; SEQUENCE HOMOLOGY;

ANIMALS; BINDING SITES; CECUM; CHROMATIN IMMUNOPRECIPITATION; COLITIS; DISEASE MODELS, ANIMAL; DNA, BACTERIAL; GENE EXPRESSION PROFILING; ILEUM; MICE; REGULON; SALMONELLA INFECTIONS, ANIMAL; SALMONELLA TYPHI; SALMONELLA TYPHIMURIUM; SEQUENCE ANALYSIS, DNA; TRANS-ACTIVATORS; VIRULENCE;

EID: 84873025773     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12111     Document Type: Article

References (48)

1. Balbontin, R., Rowley, G., Pucciarelli, M.G., Lopez-Garrido, J., Wormstone, Y., Lucchini, S., etal. (2006) DNA adenine methylation regulates virulence gene expression in Salmonella enterica serovar Typhimurium. J Bacteriol 188: 8160-8168.
2. Bäumler, A.J. (1997) The record of horizontal gene transfer in Salmonella. Trends Microbiol 5: 318-322.
3. Bäumler, A.J., Gilde, A.J., Tsolis, R.M., van der Velden, A.W.M., Ahmer, B.M.M., and Heffron, F. (1997) Contribution of horizontal gene transfer and deletion events to the development of distinctive patterns of fimbrial operons during evolution of Salmonella serotypes. J Bacteriol 179: 317-322.
4. Bertin, Y., Chaucheyras-Durand, F., Robbe-Masselot, C., Durand, A., Foye, A., Harel, J., etal. (2012) Carbohydrate utilization by enterohaemorrhagic Escherichia coli O157:H7 in bovine intestinal content. Environ Microbiol. doi: 10.1111/1462-2920.12019
5. Blattner, F., Plunkett, G., Bloch, C., Perna, N., Burland, V., Riley, M., etal. (1997) The complete genome sequence of Escherichia coli K-12. Science 277: 1453-1462.
6. Cameron, A.D., and Dorman, C.J. (2012) A fundamental regulatory mechanism operating through OmpR and DNA topology controls expression of Salmonella pathogenicity islands SPI-1 and SPI-2. PLoS Genet 8: e1002615.
7. Campbell, J.W., Morgan-Kiss, R.M., and Cronan, J.E. (2003) A new Escherichia coli metabolic competency: growth on fatty acids by a novel anaerobic beta-oxidation pathway. Mol Microbiol 47: 793-805.
8. Chang, D.E., Smalley, D.J., Tucker, D.L., Leatham, M., Norris, W.E., Stevenson, S.J., etal. (2004) Carbon nutrition of Escherichia coli in the mouse intestine. Proc Natl Acad Sci USA 101: 7427-7432.
9. Clarke, T.A., Mills, P.C., Poock, S.R., Butt, J.N., Cheesman, M.R., Cole, J.A., etal. (2008) Escherichia coli cytochrome c nitrite reductase NrfA. Methods Enzymol 437: 63-77.
10. Cunningham, L., and Guest, J.R. (1998) Transcription and transcript processing in the sdhCDAB-sucABCD operon of Escherichia coli. Microbiology 144 (Pt 8): 2113-2123.
11. Feng, X., Oropeza, R., and Kenney, L.J. (2003) Dual regulation by phospho-OmpR of ssrA/B gene expression in Salmonella pathogenicity island 2. Mol Microbiol 48: 1131-1143.
12. Forst, S.A., and Roberts, D.L. (1994) Signal transduction by the EnvZ-OmpR phosphotransfer system in bacteria. Res Microbiol 145: 363-373.
13. Giraud, A., Arous, S., Paepe, M.D., Gaboriau-Routhiau, V., Bambou, J.C., Rakotobe, S., etal. (2008) Dissecting the genetic components of adaptation of Escherichia coli to the mouse gut. PLoS Genet 4: e2.
14. Golubeva, Y.A., Sadik, A.Y., Ellermeier, J.R., and Slauch, J.M. (2012) Integrating global regulatory input into the Salmonella pathogenicity island 1 type III secretion system. Genetics 190: 79-90.
15. Groisman, E.A., and Ochman, H. (1997) How Salmonella became a pathogen. Trends Microbiol 5: 343-349.
16. Hapfelmeier, S., and Hardt, W.D. (2005) A mouse model for S. Typhimurium-induced enterocolitis. Trends Microbiol 13: 497-503.
17. Hapfelmeier, S., Ehrbar, K., Stecher, B., Barthel, M., Kremer, M., and Hardt, W.D. (2004) Role of the Salmonella pathogenicity island 1 effector proteins SipA, SopB, SopE, and SopE2 in Salmonella enterica subspecies 1 serovar Typhimurium colitis in streptomycin-pretreated mice. Infect Immun 72: 795-809.
18. Harari, O., Park, S.Y., Huang, H., Groisman, E.A., and Zwir, I. (2010) Defining the plasticity of transcription factor binding sites by deconstructing DNA consensus sequences: the PhoP-binding sites among gamma/enterobacteria. PLoS Comput Biol 6: e1000862.
19. Harlocker, S.L., Bergstrom, L., and Inouye, M. (1995) Tandem binding of six OmpR proteins to the ompF upstream regulatory sequence of Escherichia coli. J Biol Chem 270: 26849-26856.
20. Head, C.G., Tardy, A., and Kenney, L.J. (1998) Relative binding affinities of OmpR and OmpR-phosphate at the ompF and ompC regulatory sites. J Mol Biol 281: 857-870.
21. Huang, K.J., Schieberl, J.L., and Igo, M.M. (1994) A distant upstream site involved in the negative regulation of the Escherichia coli ompF gene. J Bacteriol 176: 1309-1315.
22. Kelly, A., Goldberg, M.D., Carroll, R.K., Danino, V., Hinton, J.C., and Dorman, C.J. (2004) A global role for Fis in the transcriptional control of metabolism and type III secretion in Salmonella enterica serovar Typhimurium. Microbiology 150: 2037-2053.
23. Kenney, L.J., Bauer, M.D., and Silhavy, T.J. (1995) Phosphorylation-dependent conformational changes in OmpR, an osmoregulatory DNA-binding protein of Escherichia coli. Proc Natl Acad Sci USA 92: 8866-8870.
24. Kingsley, R.A., Humphries, A.D., Weening, E.H., Zoete, M.R.D., Winter, S., Papaconstantinopoulou, A., etal. (2003) Molecular and phenotypic analysis of the CS54 island of Salmonella enterica serotype Typhimurium: identification of intestinal colonization and persistence determinants. Infect Immun 71: 629-640.
25. Lowe, D.C., Savidge, T.C., Pickard, D., Eckmann, L., Kagnoff, M.F., Dougan, G., and Chatfield, S.N. (1999) Characterization of candidate live oral Salmonella typhi vaccine strains harboring defined mutations in aroA, aroC, and htrA. Infect Immun 67: 700-707.
26. Oropeza, R., and Calva, E. (2009) The cysteine 354 and 277 residues of Salmonella enterica serovar Typhi EnvZ are determinants of autophosphorylation and OmpR phosphorylation. FEMS Microbiol Lett 292: 282-290.
27. Oshima, T., Aiba, H., Masuda, Y., Kanaya, S., Sugiura, M., Wanner, B.L., etal. (2002) Transcriptome analysis of all two-component regulatory system mutants of Escherichia coli K-12. Mol Microbiol 46: 281-291.
28. Parkhill, J., Dougan, G., James, K.D., Thomson, N.R., Pickard, D., Wain, J., etal. (2001) Complete genome sequence of a multiple drug resistant Salmonella enterica serovar Typhi CT18. Nature 413: 848-852.
29. Perkins, T.T., Kingsley, R.A., Fookes, M.C., Gardner, P.P., James, K.D., Yu, L., etal. (2009) A strand-specific RNA-Seq analysis of the transcriptome of the typhoid bacillus Salmonella typhi. PLoS Genet 5: e1000569.
30. Pfeiffer, V., Sittka, A., Tomer, R., Tedin, K., Brinkmann, V., and Vogel, J. (2007) A small non-coding RNA of the invasion gene island (SPI-1) represses outer membrane protein synthesis from the Salmonella core genome. Mol Microbiol 66: 1174-1191.
31. Pickard, D., Li, J., Roberts, M., Maskell, D., Hone, D., Levine, M., etal. (1994) Characterization of defined ompR mutants of Salmonella typhi: ompR is involved in the regulation of Vi polysaccharide expression. Infect Immun 62: 3984-3993.
32. Plumbridge, J., and Vimr, E. (1999) Convergent pathways for utilization of the amino sugars N-acetylglucosamine, N-acetylmannosamine, and N-acetylneuraminic acid by Escherichia coli. J Bacteriol 181: 47-54.
33. Popoff, M.Y., Bockemühl, J., and Gheesling, L.L. (2004) Supplement 2002 (No. 46) to the Kauffmann-White scheme. Res Microbiol 155: 568-570.
34. Rhee, J.E., Sheng, W., Morgan, L.K., Nolet, R., Liao, X., and Kenney, L.J. (2008) Amino acids important for DNA recognition by the response regulator OmpR. J Biol Chem 283: 8664-8677.
35. Rowe, J.J., Ubbink-Kok, T., Molenaar, D., Konings, W.N., and Driessen, A.J. (1994) NarK is a nitrite-extrusion system involved in anaerobic nitrate respiration by Escherichia coli. Mol Microbiol 12: 579-586.
36. Rutherford, K., Parkhill, J., Crook, J., Horsnell, T., Rice, P., Rajandream, M.A., and Barrell, B. (2000) Artemis: sequence visualization and annotation. Bioinformatics 16: 944-945.
37. Santos, R.L., Zhang, S., Tsolis, R.M., Kingsley, R.A., Adams, L.G., and Baumler, A.J. (2001) Animal models of Salmonella infections: enteritis versus typhoid fever. Microbes Infect 3: 1335-1344.
38. Severi, E., Randle, G., Kivlin, P., Whitfield, K., Young, R., Moxon, R., etal. (2005) Sialic acid transport in Haemophilus influenzae is essential for lipopolysaccharide sialylation and serum resistance and is dependent on a novel tripartite ATP-independent periplasmic transporter. Mol Microbiol 58: 1173-1185.
39. Severi, E., Hood, D.W., and Thomas, G.H. (2007) Sialic acid utilization by bacterial pathogens. Microbiology 153: 2817-2822.
40. Severi, E., Muller, A., Potts, J.R., Leech, A., Williamson, D., Wilson, K.S., and Thomas, G.H. (2008) Sialic acid mutarotation is catalyzed by the Escherichia coli beta-propeller protein YjhT. J Biol Chem 283: 4841-4849.
41. Severi, E., Hosie, A.H., Hawkhead, J.A., and Thomas, G.H. (2010) Characterization of a novel sialic acid transporter of the sodium solute symporter (SSS) family and in vivo comparison with known bacterial sialic acid transporters. FEMS Microbiol Lett 304: 47-54.
42. Sinha, S., and Tompa, M. (2003) YMF: a program for discovery of novel transcription factor binding sites by statistical overrepresentation. Nucleic Acids Res 31: 3586-3588.
43. Stecher, B., Robbiani, R., Walker, A.W., Westendorf, A.M., Barthel, M., Kremer, M., etal. (2007) Salmonella enterica serovar Typhimurium exploits inflammation to compete with the intestinal microbiota. PLoS Biol 5: 2177-2189.
44. Stecher, B., Barthel, M., Schlumberger, M.C., Haberli, L., Rabsch, W., Kremer, M., and Hardt, W.D. (2008) Motility allows S. Typhimurium to benefit from the mucosal defence. Cell Microbiol 10: 1166-1180.
45. Thiennimitr, P., Winter, S.E., Winter, M.G., Xavier, M.N., Tolstikov, V., Huseby, D.L., etal. (2011) Intestinal inflammation allows Salmonella to use ethanolamine to compete with the microbiota. Proc Natl Acad Sci USA 108: 17480-17485.
46. Tsolis, R.M., Kingsley, R.A., Townsend, S.M., Ficht, T.A., Adams, L.G., and Baumler, A.J. (1999) Of mice, calves, and men. Comparison of the mouse typhoid model with other Salmonella infections. Adv Exp Med Biol 473: 261-274.
47. Turner, A.K., Nair, S., and Wain, J. (2006) The acquisition of full fluoroquinolone resistance in Salmonella Typhi by accumulation of point mutations in the topoisomerase targets. J Antimicrob Chemother 58: 733-740.
48. Winter, S.E., Thiennimitr, P., Winter, M.G., Butler, B.P., Huseby, D.L., Crawford, R.W., etal. (2010) Gut inflammation provides a respiratory electron acceptor for Salmonella. Nature 467: 426-429.