1887

Abstract

The PhoB-PhoR two-component system responds to phosphate starvation and induces the expression of many genes. Previous studies suggested that phosphate starvation induces oxidative stress, but the involvement of the PhoB regulon in oxidative stress tolerance has not been clarified. Here, we showed that , one of the PhoB regulon genes, is involved in cell tolerance to a redox-cycling drug, menadione, and HO in stationary-phase cells. A deletion mutant was sensitive to HO when the cells were grown anaerobically or micro-aerobically in the presence of nitrate. Genetic analysis suggested that the gene has a functional relationship with the and genes, among the regulon, at least, a catalase-encoding gene and peroxidase-encoding genes. Overproduction of YtfK resulted in a KatG-dependent decrease of HO concentration in the cell suspension, suggesting that is one of the targets of YtfK. Using a reporter fusion, we showed that YtfK enhances the transcription of although it was not clarified whether YtfK functions directly or not. We also showed that disruption results in reduced viability of stationary-phase cells under phosphate starvation. These results indicated that YtfK is involved in HO tolerance by stimulating directly or indirectly the transcription of at least the catalase gene, and that this system plays an important role in cellular survival during phosphate starvation.

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2017-12-01
2024-11-08
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References

  1. Richards GR, Vanderpool CK. Induction of the Pho regulon suppresses the growth defect of an Escherichia coli sgrS mutant, connecting phosphate metabolism to the glucose-phosphate stress response. J Bacteriol 2012; 194:2520–2530 [View Article][PubMed]
    [Google Scholar]
  2. Wanner BL. Gene regulation by phosphate in enteric bacteria. J Cell Biochem 1993; 51:47–54 [View Article][PubMed]
    [Google Scholar]
  3. Foster JW, Spector MP. How Salmonella survive against the odds. Annu Rev Microbiol 1995; 49:145–174 [View Article][PubMed]
    [Google Scholar]
  4. Hsieh YJ, Wanner BL. Global regulation by the seven-component Pi signaling system. Curr Opin Microbiol 2010; 13:198–203 [View Article][PubMed]
    [Google Scholar]
  5. Yang C, Huang TW, Wen SY, Chang CY, Tsai SF et al. Genome-wide PhoB binding and gene expression profiles reveal the hierarchical gene regulatory network of phosphate starvation in Escherichia coli . PLoS One 2012; 7:e47314 [View Article][PubMed]
    [Google Scholar]
  6. Han JS, Park JY, Lee YS, Thöny B, Hwang DS. PhoB-dependent transcriptional activation of the iciA gene during starvation for phosphate in Escherichia coli. Mol Gen Genet 1999; 262:448–452[PubMed] [Crossref]
    [Google Scholar]
  7. Suziedeliené E, Suziedélis K, Garbenciūté V, Normark S. The acid-inducible asr gene in Escherichia coli: transcriptional control by the phoBR operon. J Bacteriol 1999; 181:2084–2093[PubMed]
    [Google Scholar]
  8. Harris RM, Webb DC, Howitt SM, Cox GB. Characterization of PitA and PitB from Escherichia coli . J Bacteriol 2001; 183:5008–5014 [View Article][PubMed]
    [Google Scholar]
  9. Torriani A. Influence of inorganic phosphate in the formation of phosphatases by Escherichia coli . Biochim Biophys Acta 1960; 38:460–469 [View Article][PubMed]
    [Google Scholar]
  10. Torriani A. From cell membrane to nucleotides: the phosphate regulon in Escherichia coli . Bioessays 1990; 12:371–376 [View Article][PubMed]
    [Google Scholar]
  11. Leung HB, Kvalnes-Krick KL, Meyer SL, Deriel JK, Schramm VL. Structure and regulation of the AMP nucleosidase gene (amn) from Escherichia coli . Biochemistry 1989; 28:8726–8733 [View Article][PubMed]
    [Google Scholar]
  12. Franke S, Grass G, Rensing C, Nies DH. Molecular analysis of the copper-transporting efflux system CusCFBA of Escherichia coli . J Bacteriol 2003; 185:3804–3812 [View Article][PubMed]
    [Google Scholar]
  13. Klein G, Müller-Loennies S, Lindner B, Kobylak N, Brade H et al. Molecular and structural basis of inner core lipopolysaccharide alterations in Escherichia coli: incorporation of glucuronic acid and phosphoethanolamine in the heptose region. J Biol Chem 2013; 288:8111–8127 [View Article][PubMed]
    [Google Scholar]
  14. Moreau PL, Gérard F, Lutz NW, Cozzone P. Non-growing Escherichia coli cells starved for glucose or phosphate use different mechanisms to survive oxidative stress. Mol Microbiol 2001; 39:1048–1060 [View Article][PubMed]
    [Google Scholar]
  15. Moreau PL. Diversion of the metabolic flux from pyruvate dehydrogenase to pyruvate oxidase decreases oxidative stress during glucose metabolism in nongrowing Escherichia coli cells incubated under aerobic, phosphate starvation conditions. J Bacteriol 2004; 186:7364–7368 [View Article][PubMed]
    [Google Scholar]
  16. Imlay JA, Fridovich I. Assay of metabolic superoxide production in Escherichia coli . J Biol Chem 1991; 266:6957–6965[PubMed]
    [Google Scholar]
  17. Messner KR, Imlay JA. The identification of primary sites of superoxide and hydrogen peroxide formation in the aerobic respiratory chain. J Biol Chem 1999; 274:10119–10128 [Crossref]
    [Google Scholar]
  18. Imlay JA. A metabolic enzyme that rapidly produces superoxide, fumarate reductase of Escherichia coli . J Biol Chem 1995; 270:19767–19777[PubMed]
    [Google Scholar]
  19. Fang FC. Antimicrobial reactive oxygen and nitrogen species: concepts and controversies. Nat Rev Microbiol 2004; 2:820–832 [View Article][PubMed]
    [Google Scholar]
  20. Wakimoto S, Nakayama-Imaohji H, Ichimura M, Morita H, Hirakawa H et al. PhoB regulates the survival of Bacteroides fragilis in peritoneal abscesses. PLoS One 2013; 8:e53829 [View Article][PubMed]
    [Google Scholar]
  21. Chekabab SM, Harel J, Dozois CM. Interplay between genetic regulation of phosphate homeostasis and bacterial virulence. Virulence 2014; 5:786–793 [View Article][PubMed]
    [Google Scholar]
  22. Chekabab SM, Jubelin G, Dozois CM, Harel J. PhoB activates Escherichia coli O157:H7 virulence factors in response to inorganic phosphate limitation. PLoS One 2014; 9:e94285 [View Article][PubMed]
    [Google Scholar]
  23. Zheng M, Wang X, Templeton LJ, Smulski DR, Larossa RA et al. DNA microarray-mediated transcriptional profiling of the Escherichia coli response to hydrogen peroxide. J Bacteriol 2001; 183:4562–4570 [View Article][PubMed]
    [Google Scholar]
  24. Baek JH, Lee SY. Novel gene members in the Pho regulon of Escherichia coli . FEMS Microbiol Lett 2006; 264:104–109 [View Article][PubMed]
    [Google Scholar]
  25. Yoshida Y, Sugiyama S, Oyamada T, Yokoyama K, Kim SK et al. Identification of PhoB binding sites of the yibD and ytfK promoter regions in Escherichia coli . J Microbiol 2011; 49:285–289 [View Article][PubMed]
    [Google Scholar]
  26. Lacour S, Landini P. σS-dependent gene expression at the onset of stationary phase in Escherichia coli: function of σS-dependent genes and identification of their promoter sequences. J Bacteriol 2004; 186:7186–7195 [View Article][PubMed]
    [Google Scholar]
  27. Chang AC, Cohen SN. Construction and characterization of amplifiable multicopy DNA cloning vehicles derived from the P15A cryptic miniplasmid. J Bacteriol 1978; 134:1141–1156[PubMed]
    [Google Scholar]
  28. Kato J, Ikeda H. Construction of mini-F plasmid vectors for plasmid shuffling in Escherichia coli . Gene 1996; 170:141–142 [View Article][PubMed]
    [Google Scholar]
  29. Wolff SP. Ferrous ion oxidation in presence of ferric ion indicator xylenol orange for measurement of hydroperoxides. Methods Enzymol 1994; 233:182–189 [Crossref]
    [Google Scholar]
  30. Miller JH. Experiments in molecular genetics Cold Spring Harb NY: Cold Spring Harb Lab; 1972
    [Google Scholar]
  31. Neidhardt FC, Bloch PL, Smith DF. Culture medium for enterobacteria. J Bacteriol 1974; 119:736–747[PubMed]
    [Google Scholar]
  32. Pomposiello PJ, Bennik MH, Demple B. Genome-wide transcriptional profiling of the Escherichia coli responses to superoxide stress and sodium salicylate. J Bacteriol 2001; 183:3890–3902 [View Article][PubMed]
    [Google Scholar]
  33. Schembri MA, Kjaergaard K, Klemm P. Global gene expression in Escherichia coli biofilms. Mol Microbiol 2003; 48:253–267 [View Article][PubMed]
    [Google Scholar]
  34. Bjarnason J, Southward CM, Surette MG. Genomic profiling of iron-responsive genes in Salmonella enterica serovar typhimurium by high-throughput screening of a random promoter library. J Bacteriol 2003; 185:4973–4982 [View Article][PubMed]
    [Google Scholar]
  35. Hassan HM, Fridovich I. Intracellular production of superoxide radical and of hydrogen peroxide by redox active compounds. Arch Biochem Biophys 1979; 196:385–395 [View Article][PubMed]
    [Google Scholar]
  36. St John G, Brot N, Ruan J, Erdjument-Bromage H, Tempst P et al. Peptide methionine sulfoxide reductase from Escherichia coli and Mycobacterium tuberculosis protects bacteria against oxidative damage from reactive nitrogen intermediates. Proc Natl Acad Sci USA 2001; 98:9901–9906 [View Article][PubMed]
    [Google Scholar]
  37. Justino MC, Vicente JB, Teixeira M, Saraiva LM. New genes implicated in the protection of anaerobically grown Escherichia coli against nitric oxide. J Biol Chem 2005; 280:2636–2643 [View Article][PubMed]
    [Google Scholar]
  38. Justino MC, Almeida CC, Teixeira M, Saraiva LM. Escherichia coli Di-iron YtfE protein is necessary for the repair of stress-damaged iron-sulfur clusters. J Biol Chem 2007; 282:10352–10359 [View Article][PubMed]
    [Google Scholar]
  39. Vine CE, Cole JA. Unresolved sources, sinks, and pathways for the recovery of enteric bacteria from nitrosative stress. FEMS Microbiol Lett 2011; 325:99–107 [View Article][PubMed]
    [Google Scholar]
  40. Woodmansee AN, Imlay JA. A mechanism by which nitric oxide accelerates the rate of oxidative DNA damage in Escherichia coli . Mol Microbiol 2003; 49:11–22 [View Article][PubMed]
    [Google Scholar]
  41. Korshunov S, Imlay JA. Two sources of endogenous hydrogen peroxide in Escherichia coli . Mol Microbiol 2010; 75:1389–1401 [View Article][PubMed]
    [Google Scholar]
  42. Gardner PR, Fridovich I. Superoxide sensitivity of the Escherichia coli aconitase. J Biol Chem 1991; 266:19328–19333[PubMed]
    [Google Scholar]
  43. Pan N, Imlay JA. How does oxygen inhibit central metabolism in the obligate anaerobe Bacteroides thetaiotaomicron . Mol Microbiol 2001; 39:1562–1571 [View Article][PubMed]
    [Google Scholar]
  44. Partridge JD, Poole RK, Green J. The Escherichia coli yhjA gene, encoding a predicted cytochrome c peroxidase, is regulated by FNR and OxyR. Microbiology 2007; 153:1499–1509 [View Article][PubMed]
    [Google Scholar]
  45. Lacey MM, Partridge JD, Green J. Escherichia coli K-12 YfgF is an anaerobic cyclic di-GMP phosphodiesterase with roles in cell surface remodelling and the oxidative stress response. Microbiology 2010; 156:2873–2886 [View Article][PubMed]
    [Google Scholar]
  46. Storz G, Tartaglia LA, Ames BN. Transcriptional regulator of oxidative stress-inducible genes: direct activation by oxidation. Science 1990; 248:189–194 [View Article][PubMed]
    [Google Scholar]
  47. Zheng M, Aslund F, Storz G. Activation of the OxyR transcription factor by reversible disulfide bond formation. Science 1998; 279:1718–1722 [View Article][PubMed]
    [Google Scholar]
  48. Liu Y, Bauer SC, Imlay JA. The YaaA protein of the Escherichia coli OxyR regulon lessens hydrogen peroxide toxicity by diminishing the amount of intracellular unincorporated iron. J Bacteriol 2011; 193:2186–2196 [View Article][PubMed]
    [Google Scholar]
  49. Park S, You X, Imlay JA. Substantial DNA damage from submicromolar intracellular hydrogen peroxide detected in Hpx- mutants of Escherichia coli . Proc Natl Acad Sci USA 2005; 102:9317–9322 [View Article][PubMed]
    [Google Scholar]
  50. Christman MF, Morgan RW, Jacobson FS, Ames BN. Positive control of a regulon for defenses against oxidative stress and some heat-shock proteins in Salmonella typhimurium . Cell 1985; 41:753–762 [View Article][PubMed]
    [Google Scholar]
  51. Bagg A, Neilands JB. Ferric uptake regulation protein acts as a repressor, employing iron (II) as a cofactor to bind the operator of an iron transport operon in Escherichia coli . Biochemistry 1987; 26:5471–5477 [View Article][PubMed]
    [Google Scholar]
  52. Zheng M, Doan B, Schneider TD, Storz G. OxyR and SoxRS regulation of fur . J Bacteriol 1999; 181:4639–4643[PubMed]
    [Google Scholar]
  53. Loewen PC, Triggs BL, George CS, Hrabarchuk BE. Genetic mapping of katG, a locus that affects synthesis of the bifunctional catalase-peroxidase hydroperoxidase I in Escherichia coli . J Bacteriol 1985; 162:661–667[PubMed]
    [Google Scholar]
  54. Hoerter JD, Arnold AA, Ward CS, Sauer M, Johnson S et al. Reduced hydroperoxidase (HPI and HPII) activity in the Δfur mutant contributes to increased sensitivity to UVA radiation in Escherichia coli . J Photochem Photobiol B 2005; 79:151–157 [View Article][PubMed]
    [Google Scholar]
  55. Loewen PC, Switala J. Purification and characterization of catalase HPII from Escherichia coli K12. Biochem Cell Biol 1986; 64:638–646 [View Article][PubMed]
    [Google Scholar]
  56. Seaver LC, Imlay JA. Alkyl hydroperoxide reductase is the primary scavenger of endogenous hydrogen peroxide in Escherichia coli . J Bacteriol 2001; 183:7173–7181 [View Article][PubMed]
    [Google Scholar]
  57. Seo SW, Kim D, Latif H, O'Brien EJ, Szubin R et al. Deciphering Fur transcriptional regulatory network highlights its complex role beyond iron metabolism in Escherichia coli . Nat Commun 2014; 5:4910 [View Article][PubMed]
    [Google Scholar]
  58. Seaver LC, Imlay JA. Hydrogen peroxide fluxes and compartmentalization inside growing Escherichia coli . J Bacteriol 2001; 183:7182–7189 [View Article][PubMed]
    [Google Scholar]
  59. Hughes MN, Poole RK. Metal speciation and microbial growth-the hard (and soft) facts. J Gen Microbiol 1991; 137:725–734 [View Article]
    [Google Scholar]
  60. Lee LJ, Barrett JA, Poole RK. Genome-wide transcriptional response of chemostat-cultured Escherichia coli to zinc. J Bacteriol 2005; 187:1124–1134 [View Article][PubMed]
    [Google Scholar]
  61. Brocklehurst KR, Morby AP. Metal-ion tolerance in Escherichia coli: analysis of transcriptional profiles by gene-array technology. Microbiology 2000; 146:2277–2282 [View Article][PubMed]
    [Google Scholar]
  62. Swinger KK, Rice PA. IHF and HU: flexible architects of bent DNA. Curr Opin Struct Biol 2004; 14:28–35 [View Article][PubMed]
    [Google Scholar]
  63. Paytubi S, Madrid C, Forns N, Nieto JM, Balsalobre C et al. YdgT, the Hha paralogue in Escherichia coli, forms heteromeric complexes with H-NS and StpA. Mol Microbiol 2004; 54:251–263 [View Article][PubMed]
    [Google Scholar]
  64. Mclean S, Bowman LA, Sanguinetti G, Read RC, Poole RK. Peroxynitrite toxicity in Escherichia coli K12 elicits expression of oxidative stress responses and protein nitration and nitrosylation. J Biol Chem 2010; 285:20724–20731 [View Article][PubMed]
    [Google Scholar]
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