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Volume 159, Issue Pt_7

Phosphate starvation relayed by PhoB activates the expression of the σ ECF factor and its target genes Free

Abstract

The cell-surface signalling (CSS) system represents an important regulatory mechanism by which Gram-negative bacteria respond to the environment. Gene regulation by CSS systems is particularly present and important in the opportunistic human pathogen . In this bacterium, these mechanisms regulate mainly the uptake of iron, but also virulence functions. The latter is the case for the PUMA3 CSS system formed by the putative VreA receptor, the σ extracytoplasmic function sigma factor and the VreR anti-sigma factor. A role for this system in virulence has been demonstrated previously. However, the conditions under which this system is expressed and activated have not been elucidated so far. In this work, we have identified and characterized the global regulatory cascade activating the expression of the PUMA3 system. We show that the PhoB transcriptional regulator, part of the PhoB-PhoR two-component signalling system, can sense a limitation of inorganic phosphate to turn on the expression of the , and genes, which constitute an operon. Upon expression of these genes in this condition, σ factor mediates transcription of most, but not all, of the previously identified σ-regulated genes. Indeed, we found new σ-targeted genes and we show that σ-regulon genes are all located immediately downstream to the gene cluster.

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2013-07-01
2024-04-20
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References

  1. Bains M., Fernández L., Hancock R. E.( 2012). Phosphate starvation promotes swarming motility and cytotoxicity of Pseudomonas aeruginosa.. Appl Environ Microbiol 78:6762–6768 [View Article][PubMed]
     [Google Scholar]
  2. Ball G., Durand E., Lazdunski A., Filloux A.( 2002). A novel type II secretion system in Pseudomonas aeruginosa.. Mol Microbiol 43:475–485 [View Article][PubMed]
     [Google Scholar]
  3. Bastiaansen K. C., Bitter W., Llamas M. A.( 2012). ECF sigma factors: from stress management to iron uptake.. Bacterial Regulatory Networks59–86. Filloux A. Hethersett. Norwich:: Caister Academic Press;
     [Google Scholar]
  4. Blanco A. G., Sola M., Gomis-Rüth F. X., Coll M.( 2002). Tandem DNA recognition by PhoB, a two-component signal transduction transcriptional activator. Structure 10:701–713 [View Article][PubMed]
     [Google Scholar]
  5. Blanco A. G., Canals A., Bernués J., Solà M., Coll M.( 2011). The structure of a transcription activation subcomplex reveals how σ(70) is recruited to PhoB promoters. EMBO J 30:3776–3785 [View Article][PubMed]
     [Google Scholar]
  6. Bordi C., de Bentzmann S.( 2011). Hacking into bacterial biofilms: a new therapeutic challenge. Ann Intensive Care 1:19 [View Article][PubMed]
     [Google Scholar]
  7. Braun V., Mahren S., Sauter A.( 2006). Gene regulation by transmembrane signaling. Biometals 19:103–113 [View Article][PubMed]
     [Google Scholar]
  8. Canter Cremers H., Spaink H. P., Wijfjes A. H., Pees E., Wijffelman C. A., Okker R. J., Lugtenberg B. J.( 1989). Additional nodulation genes on the Sym plasmid of Rhizobium leguminosarum biovar viciae. Plant Mol Biol 13:163–174 [View Article][PubMed]
     [Google Scholar]
  9. Choi K. H., Schweizer H. P.( 2006). mini-Tn7 insertion in bacteria with single attTn7 sites: example Pseudomonas aeruginosa.. Nat Protoc 1:153–161 [View Article][PubMed]
     [Google Scholar]
  10. Chugani S., Greenberg E. P.( 2007). The influence of human respiratory epithelia on Pseudomonas aeruginosa gene expression. Microb Pathog 42:29–35 [View Article][PubMed]
     [Google Scholar]
  11. de Lorenzo V., Timmis K. N.( 1994). Analysis and construction of stable phenotypes in gram-negative bacteria with Tn5- and Tn10-derived minitransposons. Methods Enzymol 235:386–405 [View Article][PubMed]
     [Google Scholar]
  12. Diniz M. M., Goulart C. L., Barbosa L. C., Farache J., Lery L. M., Pacheco A. B., Bisch P. M., von Krüger W. M.( 2011). Fine-tuning control of phoBR expression in Vibrio cholerae by binding of PhoB to multiple pho boxes. J Bacteriol 193:6929–6938 [View Article][PubMed]
     [Google Scholar]
  13. Escolar L., Pérez-Martín J., de Lorenzo V.( 1999). Opening the iron box: transcriptional metalloregulation by the Fur protein. J Bacteriol 181:6223–6229[PubMed]
     [Google Scholar]
  14. Figurski D. H., Helinski D. R.( 1979). Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans.. Proc Natl Acad Sci U S A 76:1648–1652 [View Article][PubMed]
     [Google Scholar]
  15. Frisk A., Schurr J. R., Wang G., Bertucci D. C., Marrero L., Hwang S. H., Hassett D. J., Schurr M. J.( 2004). Transcriptome analysis of Pseudomonas aeruginosa after interaction with human airway epithelial cells. Infect Immun 72:5433–5438 [View Article][PubMed]
     [Google Scholar]
  16. Guerinot M. L.( 1994). Microbial iron transport. Annu Rev Microbiol 48:743–772 [View Article][PubMed]
     [Google Scholar]
  17. Herrero M., de Lorenzo V., Timmis K. N.( 1990). Transposon vectors containing non-antibiotic resistance selection markers for cloning and stable chromosomal insertion of foreign genes in gram-negative bacteria. J Bacteriol 172:6557–6567[PubMed]
     [Google Scholar]
  18. Hiratsu K., Nakata A., Shinagawa H., Makino K.( 1995). Autophosphorylation and activation of transcriptional activator PhoB of Escherichia coli by acetyl phosphate in vitro.. Gene 161:7–10 [View Article][PubMed]
     [Google Scholar]
  19. Hoang T. T., Karkhoff-Schweizer R. R., Kutchma A. J., Schweizer H. P.( 1998). A broad-host-range Flp-FRT recombination system for site-specific excision of chromosomally-located DNA sequences: application for isolation of unmarked Pseudomonas aeruginosa mutants. Gene 212:77–86 [View Article][PubMed]
     [Google Scholar]
  20. Hoang T. T., Kutchma A. J., Becher A., Schweizer H. P.( 2000). Integration-proficient plasmids for Pseudomonas aeruginosa: site-specific integration and use for engineering of reporter and expression strains. Plasmid 43:59–72 [View Article][PubMed]
     [Google Scholar]
  21. Jensen V., Löns D., Zaoui C., Bredenbruch F., Meissner A., Dieterich G., Münch R., Häussler S.( 2006). RhlR expression in Pseudomonas aeruginosa is modulated by the Pseudomonas quinolone signal via PhoB-dependent and -independent pathways. J Bacteriol 188:8601–8606 [View Article][PubMed]
     [Google Scholar]
  22. Kaniga K., Delor I., Cornelis G. R.( 1991). A wide-host-range suicide vector for improving reverse genetics in gram-negative bacteria: inactivation of the blaA gene of Yersinia enterocolitica.. Gene 109:137–141 [View Article][PubMed]
     [Google Scholar]
  23. Kim S. K., Kimura S., Shinagawa H., Nakata A., Lee K. S., Wanner B. L., Makino K.( 2000). Dual transcriptional regulation of the Escherichia coli phosphate-starvation-inducible psiE gene of the phosphate regulon by PhoB and the cyclic AMP (cAMP)-cAMP receptor protein complex. J Bacteriol 182:5596–5599 [View Article][PubMed]
     [Google Scholar]
  24. Koebnik R.( 2005). TonB-dependent trans-envelope signalling: the exception or the rule?. Trends Microbiol 13:343–347 [View Article][PubMed]
     [Google Scholar]
  25. Lamarche M. G., Wanner B. L., Crépin S., Harel J.( 2008). The phosphate regulon and bacterial virulence: a regulatory network connecting phosphate homeostasis and pathogenesis. FEMS Microbiol Rev 32:461–473 [View Article][PubMed]
     [Google Scholar]
  26. Llamas M. A., Bitter W.( 2010). Cell-surface signaling in Pseudomonas. Molecular Microbiology, Infection and Biodiversity, 59–95 Ramos J. L., Filloux A. New York, USA: : Academic/Plenum;
     [Google Scholar]
  27. Llamas M. A., Mooij M. J., Sparrius M., Vandenbroucke-Grauls C. M., Ratledge C., Bitter W.( 2008). Characterization of five novel Pseudomonas aeruginosa cell-surface signalling systems. Mol Microbiol 67:458–472 [View Article][PubMed]
     [Google Scholar]
  28. Llamas M. A., van der Sar A., Chu B. C., Sparrius M., Vogel H. J., Bitter W.( 2009). A novel extracytoplasmic function (ECF) sigma factor regulates virulence in Pseudomonas aeruginosa.. PLoS Pathog 5:e1000572 [View Article][PubMed]
     [Google Scholar]
  29. Lonetto M. A., Brown K. L., Rudd K. E., Buttner M. J.( 1994). Analysis of the Streptomyces coelicolor sigE gene reveals the existence of a subfamily of eubacterial RNA polymerase sigma factors involved in the regulation of extracytoplasmic functions. Proc Natl Acad Sci U S A 91:7573–7577 [View Article][PubMed]
     [Google Scholar]
  30. Makino K., Amemura M., Kim S. K., Nakata A., Shinagawa H.( 1993). Role of the sigma 70 subunit of RNA polymerase in transcriptional activation by activator protein PhoB in Escherichia coli.. Genes Dev 7:149–160 [View Article][PubMed]
     [Google Scholar]
  31. Miller J. H.( 1972). Experiments in Molecular Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
     [Google Scholar]
  32. Newman J. R., Fuqua C.( 1999). Broad-host-range expression vectors that carry the L-arabinose-inducible Escherichia coli araBAD promoter and the araC regulator. Gene 227:197–203 [View Article][PubMed]
     [Google Scholar]
  33. Ochsner U. A., Vasil M. L.( 1996). Gene repression by the ferric uptake regulator in Pseudomonas aeruginosa: cycle selection of iron-regulated genes. Proc Natl Acad Sci U S A 93:4409–4414 [View Article][PubMed]
     [Google Scholar]
  34. Ochsner U. A., Wilderman P. J., Vasil A. I., Vasil M. L.( 2002). GeneChip expression analysis of the iron starvation response in Pseudomonas aeruginosa: identification of novel pyoverdine biosynthesis genes. Mol Microbiol 45:1277–1287 [View Article][PubMed]
     [Google Scholar]
  35. Potvin E., Sanschagrin F., Levesque R. C.( 2008). Sigma factors in Pseudomonas aeruginosa.. FEMS Microbiol Rev 32:38–55 [View Article][PubMed]
     [Google Scholar]
  36. Schalk I. J., Yue W. W., Buchanan S. K.( 2004). Recognition of iron-free siderophores by TonB-dependent iron transporters. Mol Microbiol 54:14–22 [View Article][PubMed]
     [Google Scholar]
  37. Spaink H. P., Okker R. J. H., Wijffelman C. A., Pees E., Lugtenberg B. J. J.( 1987). Promoters in the nodulation region of the Rhizobium leguminosarum Syn plasmid pRL1JI. Plant Mol Biol 9:27–39 [View Article]
     [Google Scholar]
  38. Wanner B. L.( 1993). Gene regulation by phosphate in enteric bacteria. J Cell Biochem 51:47–54 [View Article][PubMed]
     [Google Scholar]
  39. Winsor G. L., Lam D. K., Fleming L., Lo R., Whiteside M. D., Yu N. Y., Hancock R. E., Brinkman F. S.( 2011). Pseudomonas Genome Database: improved comparative analysis and population genomics capability for Pseudomonas genomes. Nucleic Acids Res 39:Database issueD596–D600 [View Article][PubMed]
     [Google Scholar]
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Phosphate starvation relayed by PhoB activates the expression of the Pseudomonas aeruginosa σvreI ECF factor and its target genes
Microbiology 159, 1315 (2013); https://doi.org/10.1099/mic.0.067645-0
/content/journal/micro/10.1099/mic.0.067645-0
/content/journal/micro/10.1099/mic.0.067645-0
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