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Bacterial Regulon Evolution: Distinct Responses and Roles for the Identical OmpR Proteins of Typhimurium and in the Acid Stress Response


Salmonella Typhimurium is closely related to Escherichia coli and they possess identical OmpR DNA binding proteins. S. Typhimurium uses OmpR to control the expression of genes involved in adaptation to acid rather than osmotic stress. OmpR expression increases in response to acid stress in S. Typhimurium but not in E. coli due to structural differences in the ompR regulatory region. S. Typhimurium OmpR controls many genes, few of which are in E. coli. Many OmpR-regulated S. Typhimurium-specific targets have been acquired by horizontal gene transfer and contribute to pathogenesis. During infection, S. Typhimurium adapts to the macrophage vacuole, an acidic niche where S. Typhimurium DNA becomes relaxed. DNA relaxation accompanies acid stress in S. Typhimurium but not E. coli and enhances OmpR binding to DNA. Drug-induced DNA relaxation mimics the effect of acid stress on OmpR binding to DNA. Thus acid-sensitive OmpR activity in S. Typhimurium allows OmpR to control many S. Typhimurium-specific genes through a mechanism that depends on changes to DNA topology. We propose that this allosteric role for DNA, combined with a weak requirement on the part of OmpR for binding site sequence specificity, accommodates flexibility in regulon membership and facilitates bacterial evolution.


Vyšlo v časopise: Bacterial Regulon Evolution: Distinct Responses and Roles for the Identical OmpR Proteins of Typhimurium and in the Acid Stress Response. PLoS Genet 10(3): e32767. doi:10.1371/journal.pgen.1004215
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004215

Souhrn

Salmonella Typhimurium is closely related to Escherichia coli and they possess identical OmpR DNA binding proteins. S. Typhimurium uses OmpR to control the expression of genes involved in adaptation to acid rather than osmotic stress. OmpR expression increases in response to acid stress in S. Typhimurium but not in E. coli due to structural differences in the ompR regulatory region. S. Typhimurium OmpR controls many genes, few of which are in E. coli. Many OmpR-regulated S. Typhimurium-specific targets have been acquired by horizontal gene transfer and contribute to pathogenesis. During infection, S. Typhimurium adapts to the macrophage vacuole, an acidic niche where S. Typhimurium DNA becomes relaxed. DNA relaxation accompanies acid stress in S. Typhimurium but not E. coli and enhances OmpR binding to DNA. Drug-induced DNA relaxation mimics the effect of acid stress on OmpR binding to DNA. Thus acid-sensitive OmpR activity in S. Typhimurium allows OmpR to control many S. Typhimurium-specific genes through a mechanism that depends on changes to DNA topology. We propose that this allosteric role for DNA, combined with a weak requirement on the part of OmpR for binding site sequence specificity, accommodates flexibility in regulon membership and facilitates bacterial evolution.


Zdroje

1. PerezJC, GroismanEA (2009) Evolution of transcriptional regulatory circuits in bacteria. Cell 138: 233–244.

2. RheeJE, ShengW, MorganLK, NoletR, LiaoX, et al. (2008) Amino acids important for DNA recognition by the response regulator OmpR. J Biol Chem 13: 8664–8677.

3. CameronADS, DormanCJ (2012) A fundamental regulatory mechanism operating through OmpR and DNA topology controls expression of Salmonella Pathogenicity islands SPI-1 and SPI-2. PLoS Genet 3: e1002615.

4. KaremK, FosterJW (1993) The influence of DNA topology on the environmental regulation of a pH-regulated locus in Salmonella Typhimurium. Mol Microbiol 10: 75–86.

5. GoldsteinE, DrlicaK (1984) Regulation of bacterial DNA supercoiling: plasmid linking numbers vary with growth temperature. Proc Natl Acad Sci USA 81: 4046–4050.

6. DormanCJ, BarrGC, Ní BhriainN, HigginsCF (1988) DNA supercoiling and the anaerobic and growth phase regulation of tonB gene expression. J Bacteriol 170: 2816–2826.

7. HsiehLS, BurgerRM, DrlicaK (1991) Bacterial DNA supercoiling and [ATP]/[ADP]. Changes associated with a transition to anaerobic growth. J Mol Biol 219: 443–450.

8. HsiehLS, Rouvière-YanivJ, DrlicaK (1991) Bacterial DNA supercoiling and [ATP]/[ADP] ratio: changes associated with salt shock. J Bacteriol 173: 3914–3917.

9. MizunoT, MizushimaS (1990) Signal transduction and gene regulation through the phosphorylation of two regulatory components: the molecular basis for the osmotic regulation of the porin genes. Mol Microbiol 7: 1077–1082.

10. Pratt L, Silhavy TJ, (1995) In: Hoch J, Silhavy TJ editors. Two-component signal transduction. Washington, DC: American Society for Microbiology Press. pp 105–107.

11. RobertsDL, BennettDW, ForstSA (1994) Identification of the site of phosphorylation on the osmosensor, EnvZ, of Escherichia coli. J Biol Chem 269: 8728–8733.

12. Martinez-HackeretE, StockAM (1997) The DNA binding domain of OmpR: crystal structures of a winged helix transcription factor. Structure 5: 109–124.

13. DelgadoJ, ForstS, HarlockerS, InouyeM (1993) Identification of a phosphorylation site and functional analysis of conserved aspartic acid residues of OmpR, a transcriptional activator for ompF and ompC in Escherichia coli.. Mol Microbiol 5: 1037–1047.

14. AlphenWV, LugtenbergB (1977) Influence of osmolarity of the growth medium on the outer membrane protein pattern of Escherichia coli. J Bacteriol 131: 623–630.

15. SarmaV, ReevesP (1977) Genetic locus (ompB) affecting a major outer-membrane protein in Escherichia coli K-12. J Bacteriol 132: 23–27.

16. SlauchJM, GarrettS, JacksonDE, SilhavyTJ (1988) EnvZ functions through OmpR to control porin gene expression in Escherichia coli K-12. J Bacteriol 170: 439–441.

17. WangLC, MorganLK, GodakumburaP, KenneyLJ, AnandGS (2012) The inner membrane histidine kinase EnvZ senses osmolality via helix-coil transitions in the cytoplasm. EMBO J 11: 2648–59.

18. Alpuche-ArandaCM, SwansonJA, LoomisWP, MillerSI (1992) Salmonella Typhimurium activates virulence gene transcription within acidified macrophage phagosomes. Proc Natl Acad Sci USA 89: 10079–10083.

19. RathmanM, SjaastadMD, FalkowS (1996) Acidification of phagosomes containing Salmonella Typhimurium in murine macrophages. Infect Immun 64: 2765–2773.

20. HaragaA, OhlsonMB, MillerSI (2008) Salmonellae interplay with host cells. Nat Rev Microbiol 1: 53–66.

21. SmallP, BlankenhornD, WeltyD, ZinserE, SlonczewskiJL (1994) Acid and base resistance in Escherichia coli and Shigella flexneri: Role of rpoS and growth pH. J Bacteriol 176: 1729–1737.

22. LinJ, LeeIS, FreyJ, SlonczewskiJL, FosterJW (1995) Comparative analysis of extreme acid survival in Salmonella Typhimurium, Shigella flexneri and Escherichia coli. J Bacteriol 177: 4097–4104.

23. DormanCJ, ChatfieldS, HigginsCF, HaywardC, DouganG (1989) Characterization of porin and ompR mutants of a virulent strain of Salmonella Typhimurium: ompR mutants are attenuated in vivo. Infect Immun 57: 2136–2140.

24. OchmanH, SonciniFC, SolomonF, GroismanEA (1996) Identification of a pathogenicity island required for Salmonella survival in host cells. Proc Natl Acad Sci USA 15: 7800–7804.

25. OchmanH, GroismanEA (1996) Distribution of pathogenicity islands in Salmonella spp. Infect Immun 12: 5410–5412.

26. SheaJE, HenselM, GleesonC, HoldenDW (1996) Identification of a virulence locus encoding a second type III secretion system in Salmonella Typhimurium. Proc Natl Acad Sci USA 93: 2593–2597.

27. RhenM, DormanCJ (2005) Hierarchical gene regulators adapt Salmonella Typhimurium to its host milieus. Int J Med Microbiol 294: 487–502.

28. LeeAK, DetweilerCS, FalkowS (2000) OmpR regulates the two-component system SsrA-SsrB in Salmonella pathogenicity island 2. J Bacteriol 182: 771–781.

29. FengX, OropezaR, KenneyLJ (2003) Dual regulation by phospho-OmpR of ssrA/B gene expression in Salmonella pathogenicity island 2. Mol Microbiol 1: 231–247.

30. FassE, GroismanEA (2009) Control of Salmonella pathogenicity island-2 gene expression. Curr Opin Microbiol 12: 199–204.

31. Ó CróinínT, CarrollRK, KellyA, DormanCJ (2006) Roles for DNA supercoiling and the Fis protein in modulation expression of virulence genes during intracellular growth of Salmonella enterica serovar Typhimurium. Mol Microbiol 62: 869–882.

32. BangIS, KimBH, FosterJW, ParkYK (2000) OmpR regulates the stationary-phase acid tolerance response of Salmonella enterica serovar Typhimurium. J Bacteriol 182: 2245–2252.

33. BangIS, AudiaJP, ParkYK, FosterJW (2002) Autoinduction of the ompR response regulator by acid shock and control of the Salmonella typhimurium acid tolerance response. Mol Microbiol 44: 1235–1250.

34. Martinez-FloresI, CanoR, BustamanteVH, CalvaE, PuenteJL (1999) The ompB operon partially determines differential expression of OmpC in Salmonella Typhi and Escherichia coli. J Bacteriol 2: 556–562.

35. LiljestromP, LaamanenI, PalvaET (1988) Structure and expression of the ompB operon, the regulatory locus for the outer membrane porin regulon in Salmonella Typhimurium LT-2. J Mol Biol 201: 663–673.

36. TsuiP, HuangL, FreundlichM (1991) Integration host factor binds specifically to multiple sites in the ompB promoter of Escherichia coli and inhibits transcription. J Bacteriol 173: 5800–5807.

37. HuangKJ, SchieberlJL, IgoMM (1994) A distant upstream site involved in the negative regulation of the Escherichia coli ompF gene. J Bacteriol 5: 1309–1315.

38. KrogerC, DillonSC, CameronADS, PapenfortK, SivasankaranSK, et al. (2012) The transcriptional landscape and small RNAs of Salmonella enterica serovar Typhimurium. Proc Natl Acad Sci USA 20: E1277–1286.

39. MattisonK, OropezaR, ByersN, KenneyLJ (2002) A phosphorylation site mutant of OmpR reveals different binding conformations at ompF and ompC. J Mol Biol 4: 497–511.

40. ForstS, KalveI, DurskiW (1995) Molecular analysis of OmpR binding sequences involved in the regulation of ompF in Escherichia coli. FEMS Microbiol Lett 2: 147–15.

41. HarlockerSL, BergstromL, InouyeM (1995) Tandem binding of six OmpR proteins to the ompF upstream regulatory sequence of Escherichia coli. J Biol Chem 45: 26849–26856.

42. YoshidaT, QinL, EggerLA, InouyeM (2006) Transcription regulation of ompF and ompC by a single transcription factor, OmpR. J Biol Chem 25: 17114–17123.

43. GibsonMM, EllisEM, Graeme-CookKA, HigginsCF (1987) OmpR and EnvZ are pleiotropic regulatory proteins: positive regulation of the tripeptide permease (tppB) of Salmonella Typhimurium. Mol Gen Genet 1: 120–129.

44. GohEB, SiinoDF, IgoMM (2004) The Escherichia coli tppB (ydgR) gene represents a new class of OmpR-regulated genes. J Bacteriol 12: 4019–4024.

45. RomlingU, BianZ, HammarM, SierraltaWD, NormarkS (1998) Curli fibers are highly conserved between Salmonella Typhimurium and Escherichia coli with respect to operon structure and regulation. J Bacteriol 3: 722–731.

46. GerstelU, ParkC, RomlingU (2003) Complex regulation of csgD promoter activity by global regulatory proteins. Mol Microbiol 3: 639–654.

47. Prigent-CombaretC, BrombacherE, VidalO, AmbertA, LejeuneP, et al. (2001) Complex regulatory network controls initial adhesion and biofilm formation in Escherichia coli via regulation of the csgD gene. J Bacteriol 24: 7213–7223.

48. ShinS, ParkC (1995) Modulation of flagellar expression in Escherichia coli by acetyl phosphate and the osmoregulator OmpR. J Bacteriol 16: 4696–4702.

49. GuillierM, GottesmanS (2006) Remodelling of the Escherichia coli outer membrane by two small regulatory RNAs. Mol Microbiol 1: 231–247.

50. PerkinsTT, KingsleyRA, FookesMC, GardnerPP, JamesKD, et al. (2009) A strand-specific RNA-Seq analysis of the transcriptome of the typhoid bacillus Salmonella Typhi. PLoS Genet 7: e1000569.

51. NeelyMN, OlsonER (1996) Kinetics of expression of the Escherichia coli cad operon as a function of pH and lysine. J Bacteriol 178: 5522–5528.

52. KobayashiH, SuzukiT, UnemotoT (1986) Streptococcal cytoplasmic pH is regulated by changes in amount and activity of a proton-translocating ATPase. J Biol Chem 261: 627–630.

53. DouchinV, BohnC, BoulocP (2006) Down-regulation of porins by a small RNA bypasses the essentiality of the regulated intramembrane proteolysis protease RseP in Escherichia coli. J Biol Chem 18: 12253–12259.

54. ClaretL, HughesC (2002) Interaction of the atypical prokaryotic transcription activator FlhD2C2 with early promoters of the flagellar gene hierarchy. J Mol Biol 2: 185–199.

55. LehnenD, BlumerC, PolenT, WackwitzB, WendischVF, et al. (2002) LrhA as a new transcriptional key regulator of flagella, motility and chemotaxis genes in Escherichia coli. Mol Microbiol 2: 521–532.

56. BlumerC, KleefeldA, LehnenD, HeintzM, Dobrindt, etal (2005) Regulation of type 1 fimbriae synthesis and biofilm formation by the transcriptional regulator LrhA of Escherichia coli. Microbiology 10: 3287–3298.

57. KoreaCG, BadouralyR, PrevostMC, GhigoJM, BeloinC (2010) Escherichia coli K-12 possesses multiple cryptic but functional chaperone-usher fimbriae with distinct surface specificities. Environ microbiol 7: 1957–1977.

58. ThomasAD, BoothIR (1992) The regulation of expression of the porin gene ompC by acid pH. J Gen Microbiol 9: 1829–35.

59. YuXJ, McGourtyK, LiuM, UnsworthKE, HoldenDW (2010) pH sensing by intracellular Salmonella induces effector translocation. Science 5981: 1040–3.

60. BajajV, HwangC, LeeCA (1995) hilA is a novel ompR/toxR family member that activates the expression of Salmonella Typhimurium invasion genes. Mol Microbiol 4: 715–727.

61. EllermeierCD, EllermeierJR, SlauchJM (2005) HilD, HilC and RtsA constitute a feed forward loop that controls expression of the SPI1 type three secretion system regulator hilA in Salmonella enterica serovar Typhimurium. Mol Microbiol 3: 691–705.

62. KellyA, GoldbergMD, CarrollRK, DaninoV, HintonJC, et al. (2004) A global role for Fis in the transcriptional control of metabolism and type III secretion in Salmonella enterica serovar Typhimurium. Microbiology 7: 2037–2053.

63. LucchiniS, RowleyG, GoldbergMD, HurdD, HarrisonM, et al. (2006) H-NS mediates the silencing of laterally acquired genes in bacteria. PLoS Pathog 8: e81.

64. DillonSC, CameronAD, HokampK, LucchiniS, HintonJC, et al. (2010) Genome-wide analysis of the H-NS and Sfh regulatory networks in Salmonella Typhimurium identifies a plasmid-encoded transcription silencing mechanism. Mol Microbiol 5: 1250–1265.

65. OsborneSE, CoombesBK (2011) Transcriptional priming of Salmonella pathogenicity Island-2 precedes cellular invasion. PloS One 6: e21648.

66. KuboriT, MatsushimaY, NakamuraD, UralilJ, Lara-TejeroM, et al. (1998) Supramolecular structure of the Salmonella Typhimurium type III protein secretion system. Science 5363: 602–605.

67. FengX, WalthersD, OropezaR, KenneyLJ (2004) The response regulator SsrB activates transcription and binds to a region overlapping OmpR binding sites at Salmonella pathogenicity island 2. Mol Microbiol 54: 823–835.

68. WalthersD, CarrollRK, NavarreWW, LibbySJ, FangFC, et al. (2007) The response regulator SsrB activates expression of diverse Salmonella pathogenicity island 2 promoters and counters silencing by the nucleoid-associated protein H-NS. Mol Microbiol 2: 477–493.

69. Tomljenovic-BerubeAM, MulderDT, WhitesideMD, BrinkmanFS, CoombesBK (2010) Identification of the regulatory logic controlling Salmonella pathoadaptation by the SsrA-SsrB two-component system. PLoS Genet 3: e1000875.

70. GerlachRG, JäckelD, StecherB, WagnerC, LupasA, et al. (2007) Salmonella Pathogenicity Island 4 encodes a giant non-fimbrial adhesin and the cognate type 1 secretion system. Cell Microbiol 9: 1834–1850.

71. WagnerC, PolkeM, GerlachRG, LinkeD, StierhofYD, et al. (2011) Functional dissection of SiiE, a giant non-fimbrial adhesin of Salmonella Typhimurium. Cell Microbiol 13: 1286–1301.

72. CameronAD, StoebelDM, DormanCJ (2011) DNA supercoiling is differentially regulated by environmental factors and FIS in Escherichia coli and Salmonella Typhimurium. Mol Microbiol 80: 85–101.

73. GellertM, O'DeaMH, ItohT, TomizawaJ (1976) Novobiocin and coumermycin inhibit DNA supercoiling catalyzed by DNA gyrase. Proc Natl Acad Sci USA 12: 4474–4478.

74. GroismanEA (2001) The pleiotropic two-component regulatory system PhoP-PhoQ. J Bacteriol 6: 1835–1842.

75. LeeE-J, PontesMH, GroismanEA (2013) A bacterial virulence protein promotes pathogenicity by inhibiting the bacterium's own F1Fo ATP synthase. Cell 154: 146–156.

76. Blanc-PotardAB, GroismanEA (1997) The Salmonella selC locus contains a pathogenicity island mediating intramacrophage survival. EMBO J 17: 5376–5385.

77. BrodskyIE, ErnstRK, MillerSI, FalkowS (2002) mig-14 is a Salmonella gene that plays a role in bacterial resistance to antimicrobial peptides. J Bacteriol 184: 3203–3213.

78. Salgado H, Peralta-Gil M, Gama-Castro S, Santos-Zavaleta A, Muñiz-Rascado L, et al. (2013) RegulonDB v8.0: omics data sets, evolutionary conservation, regulatory phrases, cross-validated gold standards and more. Nucleic Acids Res 41 (Database issue): D203–213.

79. Bailey TL, Boden M, Buske FA, Frith M, Grant CE, et al. (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37 (Web Server issue): W202–208.

80. TuratsinzeJV, Thomas-ChollierM, DefranceM (2008) van HeldenJ (2008) Using RSAT to scan genome sequences for transcription factor binding sites and cis-regulatory modules. Nature protocols 10: 1578–1588.

81. StinconeA, DaudiN, RathmanAS, AntczakP, HendersonI, et al. (2011) A systems biology approach sheds new light on Escherichia coli acid resistance. Nucleic Acids Res 39: 7512–7528.

82. LangB, BlotN, BouffartiguesE, BuckleM, GeertzM, et al. (2007) High-affinity DNA binding sites for H-NS provide a molecular basis for selective silencing within proteobacterial genomes. Nucleic Acids Res 35: 6330–6337.

83. WesterhoffHV, O'DeaMH, MaxwellA, GellertM (1988) DNA supercoiling by DNA gyrase. A static head analysis. Cell Biophys. 12: 157–181.

84. RohsR, WestSM, SosinskyA, Liu P MannRS, et al. (2009) The role of DNA shape in protein-DNA recognition. Nature. 461: 1248–53.

85. VogelHJ, BonnerDM (1956) Acetylornithinase of Escherichia coli: partial purification and some properties. J Biol Chem 1: 97–106.

86. MullerC, BangIS, VelayudhanJ, KarlinseyJ, PapenfortK, et al. (2009) Acid stress activation of the sigma(E) stress response in Salmonella enterica serovar Typhimurium. Mol Microbiol 71: 1228–1238.

87. UrbanJH, VogelJ (2009) A green fluorescent protein (GFP)-based plasmid system to study post-transcriptional control of gene expression in vivo. Methods Mol Biol 540: 301–319.

88. BuckMJ, NobelAB, LiebJD (2005) ChIPOTle: a user-friendly tool for the analysis of ChIP-chip data. Genome Biol 6: R97.

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