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PMID: 15883881 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Comparison of the PhoPQ regulon in Escherichia coli and Salmonella typhimurium.

Journal of molecular evolution ·Vol. 60 ·No. 4 ·2005-04-00 ·Pages 462-74

Monsieurs P, De Keersmaecker S, Navarre WW, Bader MW, De Smet F, McClelland M, Fang FC, De Moor B, Vanderleyden J, Marchal K

Abstract

The PhoPQ two-component system acts as a transcriptional regulator that responds to Mg(2+) starvation both in Escherichia coli and Salmonella typhimurium (Garcia et al. 1996; Kato et al. 1999). By monitoring the availability of extracellular Mg(2+), this two-component system allows S. typhimurium to sense the transition from an extracellular environment to a subcellular location. Concomitantly with this transition, a set of virulence factors essential for survival in the intracellular environment is activated by the PhoPQ system (Groisman et al. 1989; Miller et al. 1989). Compared to nonpathogenic strains, such as E. coli K12, the PhoPQ regulon in pathogens must contain target genes specifically contributing to the virulence phenotype. To verify this hypothesis, we compared the composition of the PhoPQ regulon between E. coli and S. typhimurium using a combination of expression experiments and motif data. PhoPQ-dependent genes in both organisms were identified from PhoPQ-related microarray experiments. To distinguish between direct and indirect targets, we searched for the presence of the regulatory motif in the promoter region of the identified PhoPQ-dependent genes. This allowed us to reconstruct the direct PhoPQ-dependent regulons in E. coli K12 and S. typhimurium LT2. Comparison of both regulons revealed a very limited overlap of PhoPQ-dependent genes between both organisms. These results suggest that the PhoPQ system has acquired a specialized function during evolution in each of these closely related species that allows adaptation to the specificities of their lifestyles (e.g., pathogenesis in S. typhimurium).

MeSH Terms
Bacterial Proteins/genetics Base Sequence Escherichia coli/genetics Escherichia coli Proteins/genetics Oligonucleotide Array Sequence Analysis Regulon Salmonella typhimurium/genetics Sequence Homology, Nucleic Acid
Chemicals
Bacterial Proteins Escherichia coli Proteins PhoP protein, E coli PhoQ protein, Bacteria PhoP protein, Bacteria
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Monsieurs Pieter
ESAT-SCD, K.U. Leuven, Kasteelpark Arenberg 10, 3001, Leuven-Heverlee, Belgium.
De Keersmaecker Sigrid
Navarre William W
Bader Martin W
De Smet Frank
McClelland Michael
Fang Ferric C
De Moor Bart
Vanderleyden Jos
Marchal Kathleen
References (54)
54 references, click to expand
  1. Bacterial virulence gene regulation: an evolutionary perspective.
    Annu Rev Microbiol. 2000;54:519-65 PMID: 11018137
  2. Closing the loop: the PmrA/PmrB two-component system negatively controls expression of its posttranscriptional activator PmrD.
    Proc Natl Acad Sci U S A. 2003 Apr 15;100(8):4706-11 PMID: 12676988
  3. Two-component regulatory systems can interact to process multiple environmental signals.
    J Bacteriol. 1996 Dec;178(23):6796-801 PMID: 8955299
  4. Molecular basis of the interaction of Salmonella with the intestinal mucosa.
    Clin Microbiol Rev. 1999 Jul;12(3):405-28 PMID: 10398673
  5. The Salmonella typhi melittin resistance gene pqaB affects intracellular growth in PMA-differentiated U937 cells, polymyxin B resistance and lipopolysaccharide.
    Microbiology. 1999 Feb;145 ( Pt 2):367-78 PMID: 10075419
  6. Mutants of Salmonella typhimurium that cannot survive within the macrophage are avirulent.
    Proc Natl Acad Sci U S A. 1986 Jul;83(14):5189-93 PMID: 3523484
  7. Characterization of the Salmonella typhimurium pagC/pagD chromosomal region.
    J Bacteriol. 1995 Sep;177(17):5040-7 PMID: 7665482
  8. Constitutive expression of the phoP regulon attenuates Salmonella virulence and survival within macrophages.
    J Bacteriol. 1990 May;172(5):2485-90 PMID: 2185222
  9. Molecular analysis of the Escherichia coli phoP-phoQ operon.
    J Bacteriol. 1992 Jan;174(2):492-8 PMID: 1729240
  10. The Salmonella selC locus contains a pathogenicity island mediating intramacrophage survival.
    EMBO J. 1997 Sep 1;16(17):5376-85 PMID: 9311997
  11. Testing for differentially-expressed genes by maximum-likelihood analysis of microarray data.
    J Comput Biol. 2000;7(6):805-17 PMID: 11382363
  12. Molecular genetic analysis of a locus required for resistance to antimicrobial peptides in Salmonella typhimurium.
    EMBO J. 1993 Nov;12(11):4053-62 PMID: 8223423
  13. Salmonella enterica serovar typhimurium invasion is repressed in the presence of bile.
    Infect Immun. 2000 Dec;68(12):6763-9 PMID: 11083793
  14. The pleiotropic two-component regulatory system PhoP-PhoQ.
    J Bacteriol. 2001 Mar;183(6):1835-42 PMID: 11222580
  15. A two-component regulatory system (phoP phoQ) controls Salmonella typhimurium virulence.
    Proc Natl Acad Sci U S A. 1989 Jul;86(13):5054-8 PMID: 2544889
  16. A Salmonella typhimurium virulence protein is similar to a Yersinia enterocolitica invasion protein and a bacteriophage lambda outer membrane protein.
    J Bacteriol. 1991 Jan;173(1):86-93 PMID: 1846140
  17. MgtC as a horizontally-acquired virulence factor of intracellular bacterial pathogens: evidence from molecular phylogeny and comparative genomics.
    J Mol Evol. 2003 Oct;57(4):479-86 PMID: 14708580
  18. Salmonella typhimurium phoP virulence gene is a transcriptional regulator.
    Proc Natl Acad Sci U S A. 1989 Sep;86(18):7077-81 PMID: 2674945
  19. GenBank.
    Nucleic Acids Res. 2003 Jan 1;31(1):23-7 PMID: 12519940
  20. Novel mode of transcription regulation of divergently overlapping promoters by PhoP, the regulator of two-component system sensing external magnesium availability.
    Mol Microbiol. 2002 Jul;45(2):423-38 PMID: 12123454
  21. A low pH-inducible, PhoPQ-dependent acid tolerance response protects Salmonella typhimurium against inorganic acid stress.
    J Bacteriol. 1998 May;180(9):2409-17 PMID: 9573193
  22. Mg2+ as an extracellular signal: environmental regulation of Salmonella virulence.
    Cell. 1996 Jan 12;84(1):165-74 PMID: 8548821
  23. Statistical significance for genomewide studies.
    Proc Natl Acad Sci U S A. 2003 Aug 5;100(16):9440-5 PMID: 12883005
  24. virK, somA and rcsC are important for systemic Salmonella enterica serovar Typhimurium infection and cationic peptide resistance.
    Mol Microbiol. 2003 Apr;48(2):385-400 PMID: 12675799
  25. Systematic determination of genetic network architecture.
    Nat Genet. 1999 Jul;22(3):281-5 PMID: 10391217
  26. Resistance to host antimicrobial peptides is necessary for Salmonella virulence.
    Proc Natl Acad Sci U S A. 1992 Dec 15;89(24):11939-43 PMID: 1465423
  27. Regulation of Salmonella typhimurium virulence gene expression by cationic antimicrobial peptides.
    Mol Microbiol. 2003 Oct;50(1):219-30 PMID: 14507376
  28. Molecular characterization of the PhoP-PhoQ two-component system in Escherichia coli K-12: identification of extracellular Mg2+-responsive promoters.
    J Bacteriol. 1999 Sep;181(17):5516-20 PMID: 10464230
  29. Characterization of the bacterial sensor protein PhoQ. Evidence for distinct binding sites for Mg2+ and Ca2+.
    J Biol Chem. 1997 Jan 17;272(3):1440-3 PMID: 8999810
  30. Transcriptional autoregulation of the Salmonella typhimurium phoPQ operon.
    J Bacteriol. 1995 Aug;177(15):4364-71 PMID: 7543474
  31. In silico identification and experimental validation of PmrAB targets in Salmonella typhimurium by regulatory motif detection.
    Genome Biol. 2004;5(2):R9 PMID: 14759259
  32. A new approach to decoding life: systems biology.
    Annu Rev Genomics Hum Genet. 2001;2:343-72 PMID: 11701654
  33. Molecular genetic analysis of the Escherichia coli phoP locus.
    J Bacteriol. 1992 Jan;174(2):486-91 PMID: 1530848
  34. An efficient algorithm for large-scale detection of protein families.
    Nucleic Acids Res. 2002 Apr 1;30(7):1575-84 PMID: 11917018
  35. Molecular basis of the magnesium deprivation response in Salmonella typhimurium: identification of PhoP-regulated genes.
    J Bacteriol. 1996 Sep;178(17):5092-9 PMID: 8752324
  36. Adaptive acidification tolerance response of Salmonella typhimurium.
    J Bacteriol. 1990 Feb;172(2):771-8 PMID: 2404956
  37. A powerful non-homology method for the prediction of operons in prokaryotes.
    Bioinformatics. 2002;18 Suppl 1:S329-36 PMID: 12169563
  38. Inactivation of the sapA to sapF locus of Erwinia chrysanthemi reveals common features in plant and animal bacterial pathogenesis.
    Plant Cell. 1998 Jun;10(6):917-24 PMID: 9634580
  39. Genome-specific higher-order background models to improve motif detection.
    Trends Microbiol. 2003 Feb;11(2):61-6 PMID: 12598125
  40. Molecular characterization of the Mg2+-responsive PhoP-PhoQ regulon in Salmonella enterica.
    J Bacteriol. 2003 Nov;185(21):6287-94 PMID: 14563863
  41. A higher-order background model improves the detection of promoter regulatory elements by Gibbs sampling.
    Bioinformatics. 2001 Dec;17(12):1113-22 PMID: 11751219
  42. Balancing false positives and false negatives for the detection of differential expression in malignancies.
    Br J Cancer. 2004 Sep 13;91(6):1160-5 PMID: 15354216
  43. A Salmonella locus that controls resistance to microbicidal proteins from phagocytic cells.
    Science. 1989 Feb 24;243(4894 Pt 1):1059-62 PMID: 2646710
  44. Identification and molecular characterization of the Mg2+ stimulon of Escherichia coli.
    J Bacteriol. 2003 Jul;185(13):3696-702 PMID: 12813061
  45. PhoP-PhoQ-regulated loci are required for enhanced bile resistance in Salmonella spp.
    Infect Immun. 1999 Apr;67(4):1614-22 PMID: 10084994
  46. Regulation of lipid A modifications by Salmonella typhimurium virulence genes phoP-phoQ.
    Science. 1997 Apr 11;276(5310):250-3 PMID: 9092473
  47. RegulonDB (version 4.0): transcriptional regulation, operon organization and growth conditions in Escherichia coli K-12.
    Nucleic Acids Res. 2004 Jan 1;32(Database issue):D303-6 PMID: 14681419
  48. A PhoP-regulated outer membrane protease of Salmonella enterica serovar typhimurium promotes resistance to alpha-helical antimicrobial peptides.
    J Bacteriol. 2000 Jul;182(14):4077-86 PMID: 10869088
  49. A Gibbs sampling method to detect overrepresented motifs in the upstream regions of coexpressed genes.
    J Comput Biol. 2002;9(2):447-64 PMID: 12015892
  50. Oxygen requirement for the biosynthesis of the S-2-hydroxymyristate moiety in Salmonella typhimurium lipid A. Function of LpxO, A new Fe2+/alpha-ketoglutarate-dependent dioxygenase homologue.
    J Biol Chem. 2000 Oct 20;275(42):32940-9 PMID: 10903325
  51. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs.
    Nucleic Acids Res. 1997 Sep 1;25(17):3389-402 PMID: 9254694
  52. Complete genome sequence of a multiple drug resistant Salmonella enterica serovar Typhi CT18.
    Nature. 2001 Oct 25;413(6858):848-52 PMID: 11677608
  53. PmrA-PmrB-regulated genes necessary for 4-aminoarabinose lipid A modification and polymyxin resistance.
    Mol Microbiol. 1998 Mar;27(6):1171-82 PMID: 9570402
  54. Operons in Escherichia coli: genomic analyses and predictions.
    Proc Natl Acad Sci U S A. 2000 Jun 6;97(12):6652-7 PMID: 10823905
Article Info
Journal
Journal of molecular evolution
Abbr.
J Mol Evol
ISSN
0022-2844
Published
2005-04-00
Pages
462-74
Language
English
Region
Germany
NLM ID
0360051
Subset
IM
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