Characterization of the escherichia coli δS core regulon by chromatin immunoprecipitation-sequencing (ChIP-seq) analysis

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Peano, Clelia ^a   Wolf, Johannes ^b   Demol, Julien ^c,d   Rossi, Elio ^e   Petiti, Luca ^a   De Bellis, Gianluca ^a   Geiselmann, Johannes ^c,d   Egli, Thomas ^b   Lacour, Stephan ^c,d   Landini, Paolo ^e  

^a CNR   (Italy)

^b SWISS FEDERAL INSTITUTE OF AQUATIC SCIENCE AND TECHNOLOGY   (Switzerland)

^c UNIV GRENOBLE ALPES   (France)

^d CNRS   (France)

^e UNIVERSITY OF MILAN   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

SIGMA FACTOR; UNTRANSLATED RNA;

BINDING SITE; CHROMATIN IMMUNOPRECIPITATION; ESCHERICHIA COLI; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; PROMOTER REGION;

BINDING SITES; CHROMATIN IMMUNOPRECIPITATION; ESCHERICHIA COLI; GENE EXPRESSION REGULATION, BACTERIAL; PROMOTER REGIONS, GENETIC; RNA, UNTRANSLATED; SIGMA FACTOR; TRANSCRIPTION, GENETIC;

EID: 84930674706     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep10469     Document Type: Article

References (60)

1. Lloyd, G., Landini, P. & Busby, S. Activation and repression of transcription initiation in bacteria. Essays Biochem 37, 17-31 (2001).
2. Gourse, R. L., Ross, W. & Rutherford, S. T. General pathway for turning on promoters transcribed by RNA polymerases containing alternative sigma factors. J Bacteriol 188, 4589-4591 (2006).
3. Battesti, A., Majdalani, N. & Gottesman, S. The RpoS-mediated general stress response in Escherichia coli. Annu Rev Microbiol 65, 189-213.
4. Hengge-Aronis, R. in Bacterial Stress Responses 161-178 (ASM Press, Washington, DC; 2000).
5. Landini, P., Egli, T., Wolf, J. & Lacour, S. sigmaS, a major player in the response to environmental stresses in Escherichia coli: Role, regulation and mechanisms of promoter recognition. Environ Microbiol Rep 6, 1-13 (2014).
6. Typas, A., Becker, G. & Hengge, R. The molecular basis of selective promoter activation by the sigmaS subunit of RNA polymerase. Mol Microbiol 63, 1296-1306 (2007).
7. Tanaka, K., Takayanagi, Y., Fujita, N., Ishihama, A. & Takahashi, H. Heterogeneity of the principal sigma factor in Escherichia coli: The rpoS gene product, sigma 38, is a second principal sigma factor of RNA polymerase in stationary-phase Escherichia coli. Proc Natl Acad Sci U S A 90, 8303 (1993).
8. Gaal, T. et al. Promoter recognition and discrimination by EsigmaS RNA polymerase. Mol Microbiol 42, 939-954 (2001).
9. Becker, G. & Hengge-Aronis, R. What makes an Escherichia coli promoter sigma(S) dependent? Role of the-13/-14 nucleotide promoter positions and region 2.5 of sigma(S). Mol Microbiol 39, 1153-1165 (2001).
10. Maciag, A. et al. In vitro transcription profiling of the sigmaS subunit of bacterial RNA polymerase: Re-definition of the sigmaS regulon and identification of sigmaS-specific promoter sequence elements. Nucleic Acids Res 39, 5338-5355 (2011).
11. Tanaka, K., Handel, K., Loewen, P. C. & Takahashi, H. Identification and analysis of the rpoS-dependent promoter of katE, encoding catalase HPII in Escherichia coli. Biochim Biophys Acta 1352, 161-166 (1997).
12. Ji, H. et al. An integrated software system for analyzing ChIP-chip and ChIP-seq data. Nat Biotechnol 26, 1293-1300 (2008).
13. Wade, J. T. et al. Extensive functional overlap between sigma factors in Escherichia coli. Nat Struct Mol Biol 13, 806-814 (2006).
14. Lacour, S. & Landini, P. SigmaS-dependent gene expression at the onset of stationary phase in Escherichia coli: Function of sigmaS-dependent genes and identification of their promoter sequences. J Bacteriol 186, 7186-7195 (2004).
15. Patten, C. L., Kirchhof, M. G., Schertzberg, M. R., Morton, R. A. & Schellhorn, H. E. Microarray analysis of RpoS-mediated gene expression in Escherichia coli K-12. Mol Genet Genomics 272, 580-591 (2004).
16. Weber, H., Polen, T., Heuveling, J., Wendisch, V. F. & Hengge, R. Genome-wide analysis of the general stress response network in Escherichia coli: SigmaS-dependent genes, promoters, and sigma factor selectivity. J Bacteriol 187, 1591-1603 (2005).
17. Dong, T., Kirchhof, M. G. & Schellhorn, H. E. RpoS regulation of gene expression during exponential growth of Escherichia coli K12. Mol Genet Genomics 279, 267-277 (2008).
18. Dong, T. & Schellhorn, H. E. Control of RpoS in global gene expression of Escherichia coli in minimal media. Mol Genet Genomics 281, 19-33 (2009).
19. Dong, T. & Schellhorn, H. E. Global effect of RpoS on gene expression in pathogenic Escherichia coli O157:H7 strain EDL933. BMC Genomics 10, 349 (2009).
20. Ibanez-Ruiz, M., Robbe-Saule, V., Hermant, D., Labrude, S. & Norel, F. Identification of RpoS (sigma(S))-regulated genes in Salmonella enterica serovar typhimurium. J Bacteriol 182, 5749-5756 (2000).
21. Braun, V. & Rehn, K. Chemical characterization, spatial distribution and function of a lipoprotein (murein-lipoprotein) of the E. coli cell wall. The specific effect of trypsin on the membrane structure. Eur J Biochem 10, 426-438 (1969).
22. Huerta, A. M. & Collado-Vides, J. Sigma70 promoters in Escherichia coli: Specific transcription in dense regions of overlapping promoter-like signals. J Mol Biol 333, 261-278 (2003).
23. Fabrega, A., Rosner, J. L., Martin, R. G., Sole, M. & Vila, J. SoxS-dependent coregulation of ompN and ydbK in a multidrugresistant Escherichia coli strain. FEMS Microbiol Lett 332, 61-67 (2012).
24. Mendoza-Vargas, A. et al. Genome-wide identification of transcription start sites, promoters and transcription factor binding sites in E. coli. PLoS One 4, e7526 (2009).
25. De Lay, N. & Gottesman, S. A complex network of small non-coding RNAs regulate motility in Escherichia coli. Mol Microbiol 86, 524-538 (2012).
26. Guillier, M. & Gottesman, S. The 5' end of two redundant sRNAs is involved in the regulation of multiple targets, including their own regulator. Nucleic Acids Res 36, 6781-6794 (2008).
27. Vogel, J. et al. RNomics in Escherichia coli detects new sRNA species and indicates parallel transcriptional output in bacteria. Nucleic Acids Res 31, 6435-6443 (2003).
28. Fozo, E. M. et al. Repression of small toxic protein synthesis by the Sib and OhsC small RNAs. Mol Microbiol 70, 1076-1093 (2008).
29. Frohlich, K. S., Papenfort, K., Berger, A. A. & Vogel, J. A conserved RpoS-dependent small RNA controls the synthesis of major porin OmpD. Nucleic Acids Res 40, 3623-3640 (2012).
30. Levi-Meyrueis, C. et al. Expanding the RpoS/sigmaS-network by RNA sequencing and identification of sigmaS-controlled small RNAs in Salmonella. PLoS One 9, e96918 (2014).
31. Repoila, F., Majdalani, N. & Gottesman, S. Small non-coding RNAs, co-ordinators of adaptation processes in Escherichia coli: The RpoS paradigm. Mol Microbiol 48, 855-861 (2003).
32. Lacour, S., Leroy, O., Kolb, A. & Landini, P. Substitutions in region 2.4 of sigma70 allow recognition of the sigmaS-dependent aidB promoter. J Biol Chem 279, 55255-55261 (2004).
33. Cho, B. K., Kim, D., Knight, E. M., Zengler, K. & Palsson, B. O. Genome-scale reconstruction of the sigma factor network in Escherichia coli: Topology and functional states. BMC Biol 12, 4 (2014).
34. McMeechan, A. et al. Role of the alternative sigma factors sigmaE and sigmaS in survival of Salmonella enterica serovar Typhimurium during starvation, refrigeration and osmotic shock. Microbiology 153, 263-269 (2007).
35. Janaszak, A., Nadratowska-Wesolowska, B., Konopa, G. & Taylor, A. The P1 promoter of the Escherichia coli rpoH gene is utilized by sigma 70-RNAP or sigma s-RNAP depending on growth phase. FEMS Microbiol Lett 291, 65-72 (2009).
36. Kocharunchitt, C., King, T., Gobius, K., Bowman, J.P. & Ross, T. Global genome response of Escherichia coli O157ratioH7 Sakai during dynamic changes in growth kinetics induced by an abrupt downshift in water activity. PLoS One 9, e90422 (2014).
37. Weber, M. M., French, C. L., Barnes, M. B., Siegele, D. A. & McLean, R. J. A previously uncharacterized gene, yjfO (bsmA), influences Escherichia coli biofilm formation and stress response. Microbiology 156, 139-147 (2010).
38. Wanner, U. & Egli, T. Dynamics of microbial growth and cell composition in batch culture. FEMS Microbiol Rev 6, 19-43 (1990).
39. Lacour, S., Kolb, A. & Landini, P. Nucleotides from-16 to-12 determine specific promoter recognition by bacterial sigmaS-RNA polymerase. J Biol Chem 278, 37160-37168 (2003).
40. Mika, F. & Hengge, R. Small RNAs in the control of RpoS, CsgD, and biofilm architecture of Escherichia coli. RNA Biol 11, 494-507 (2014).
41. Datsenko, K. A. & Wanner, B. L. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97, 6640-6645 (2000).
42. Yu, D. et al. An efficient recombination system for chromosome engineering in Escherichia coli. Proc Natl Acad Sci USA 97, 5978-5983 (2000).
43. Herring, C. D. et al. Immobilization of Escherichia coli RNA polymerase and location of binding sites by use of chromatin immunoprecipitation and microarrays. J Bacteriol 187, 6166-6174 (2005).
44. Mooney, R. A. et al. Regulator trafficking on bacterial transcription units in vivo. Mol Cell 33, 97-108 (2009).
45. Langmead, B., Trapnell, C., Pop, M. & Salzberg, S. L. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10, R25 (2009).
46. Li, H. et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078-2079 (2009).
47. Quinlan, A. R. & Hall, I. M. BEDTools: A flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841-842 (2010).
48. Kharchenko, P. V., Tolstorukov, M. Y. & Park, P. J. Design and analysis of ChIP-seq experiments for DNA-binding proteins. Nat Biotechnol 26, 1351-1359 (2008).
49. Gualdi, L., Tagliabue, L. & Landini, P. Biofilm formation-gene expression relay system in Escherichia coli: Modulation of sigmaSdependent gene expression by the CsgD regulatory protein via sigmaS protein stabilization. J Bacteriol 189, 8034-8043 (2007).
50. Dudin, O., Lacour, S. & Geiselmann, J. Expression dynamics of RpoS/Crl-dependent genes in Escherichia coli. Res Microbiol 164, 838-847 (2013).
51. Visick, J. E. & Clarke, S. RpoS-and OxyR-independent induction of HPI catalase at stationary phase in Escherichia coli and identification of rpoS mutations in common laboratory strains. J Bacteriol 179, 4158-4163 (1997).
52. Ihssen, J. & Egli, T. Specific growth rate and not cell density controls the general stress response in Escherichia coli. Microbiology 150, 1637-1648 (2004).
53. Hengge-Aronis, R. Survival of hunger and stress: The role of rpoS in early stationary phase gene regulation in E. coli. Cell 72, 165-168 (1993).
54. Wise, A., Brems, R., Ramakrishnan, V. & Villarejo, M. Sequences in the-35 region of Escherichia coli rpoS-dependent genes promote transcription by E sigma S. J Bacteriol 178, 2785-2793 (1996).
55. Schellhorn, H. E., Audia, J. P., Wei, L. I. & Chang, L. Identification of conserved, RpoS-dependent stationary-phase genes of Escherichia coli. J Bacteriol 180, 6283-6291 (1998).
56. Marschall, C. et al. Molecular analysis of the regulation of csiD, a carbon starvation-inducible gene in Escherichia coli that is exclusively dependent on sigma s and requires activation by cAMP-CRP. J Mol Biol 276, 339-353 (1998).
57. Yakhnin, H. et al. Complex regulation of the global regulatory gene csrA: CsrA-mediated translational repression, transcription from five promoters by Esigma(7)(0) and Esigma(S), and indirect transcriptional activation by CsrA. Mol Microbiol 81, 689-704 (2011).
58. Farewell, A., Kvint, K. & Nystrom, T. Negative regulation by RpoS: A case of sigma factor competition. Mol Microbiol 29, 1039-1051 (1998).
59. Dartigalongue, C., Missiakas, D. & Raina, S. Characterization of the Escherichia coli sigma E regulon. J Biol Chem 276, 20866-20875 (2001).
60. Rhodius, V. A., Suh, W. C., Nonaka, G., West, J. & Gross, C. A. Conserved and variable functions of the sigmaE stress response in related genomes. PLoS Biol 4, e2 (2006).