1887

Abstract

Toxic agents added into the medium of rapidly growing induce specific stress responses through the activation of specialized transcription factors. Each transcription factor and downstream regulon (e.g. SoxR) are linked to a unique stress (e.g. superoxide stress). Cells starved of phosphate induce several specific stress regulons during the transition to stationary phase when the growth rate is steadily declining. Whereas the regulatory cascades leading to the expression of specific stress regulons are well known in rapidly growing cells stressed by toxic products, they are poorly understood in cells starved of phosphate. The intent of this review is to both describe the unique mechanisms of activation of specialized transcription factors and discuss signalling cascades leading to the induction of specific stress regulons in phosphate-starved cells. Finally, I discuss unique defence mechanisms that could be induced in cells starved of ammonium and glucose.

Keyword(s): CpxR , Kdp , LexA , PtsN , RpoE and SoxR
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.001312
2023-03-27
2024-04-23
Loading full text...

Full text loading...

/deliver/fulltext/micro/169/3/mic001312.html?itemId=/content/journal/micro/10.1099/mic.0.001312&mimeType=html&fmt=ahah

References

  1. Kochanowski K, Gerosa L, Brunner SF, Christodoulou D, Nikolaev YV et al. Few regulatory metabolites coordinate expression of central metabolic genes in Escherichia coli. Mol Syst Biol 2017; 13:903 [View Article] [PubMed]
    [Google Scholar]
  2. Lamarche MG, Wanner BL, Crépin S, Harel J. The phosphate regulon and bacterial virulence: a regulatory network connecting phosphate homeostasis and pathogenesis. FEMS Microbiol Rev 2008; 32:461–473 [View Article] [PubMed]
    [Google Scholar]
  3. Altendorf K, Booth IR, Gralla J, Greie J-C, Rosenthal AZ et al. Osmotic Stress. EcoSal Plus 2009; 3: [View Article]
    [Google Scholar]
  4. Nies DH, Grass G. Transition metal homeostasis. EcoSal Plus 2009; 3: [View Article]
    [Google Scholar]
  5. Krulwich TA, Sachs G, Padan E. Molecular aspects of bacterial pH sensing and homeostasis. Nat Rev Microbiol 2011; 9:330–343 [View Article] [PubMed]
    [Google Scholar]
  6. Ruiz N, Silhavy TJ. Sensing external stress: watchdogs of the Escherichia coli cell envelope. Curr Opin Microbiol 2005; 8:122–126 [View Article]
    [Google Scholar]
  7. Unden G, Steinmetz PA, Degreif-Dünnwald P. The aerobic and anaerobic respiratory chain of Escherichia coli and Salmonella enterica: enzymes and energetics. EcoSal Plus 2014; 6: [View Article] [PubMed]
    [Google Scholar]
  8. Moreau P, Bailone A, Devoret R. Prophage lambda induction of Escherichia coli K12 envA uvrB: a highly sensitive test for potential carcinogens. Proc Natl Acad Sci 1976; 73:3700–3704 [View Article] [PubMed]
    [Google Scholar]
  9. Baharoglu Z, Mazel D. SOS, the formidable strategy of bacteria against aggressions. FEMS Microbiol Rev 2014; 38:1126–1145 [View Article] [PubMed]
    [Google Scholar]
  10. Imlay JA. Where in the world do bacteria experience oxidative stress?. Environ Microbiol 2019; 21:521–530 [View Article] [PubMed]
    [Google Scholar]
  11. Ketcham A, Freddolino PL, Tavazoie S. Intracellular acidification is a hallmark of thymineless death in E. coli. PLoS Genet 2022; 18:e1010456 [View Article] [PubMed]
    [Google Scholar]
  12. Berlett BS, Stadtman ER. Protein oxidation in aging, disease, and oxidative stress. J Biol Chem 1997; 272:20313–20316 [View Article] [PubMed]
    [Google Scholar]
  13. Cadet J, Davies KJA, Medeiros MHG, Di Mascio P, Wagner JR. Formation and repair of oxidatively generated damage in cellular DNA. Free Radic Biol Med 2017; 107:13–34 [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. Imlay JA, Slauch JM. Oxidative stress. EcoSal Plus 2009; 3: [View Article]
    [Google Scholar]
  16. Weber H, Polen T, Heuveling J, Wendisch VF, Hengge R. Genome-wide analysis of the general stress response network in Escherichia coli: sigmaS-dependent genes, promoters, and sigma factor selectivity. J Bacteriol 2005; 187:1591–1603 [View Article] [PubMed]
    [Google Scholar]
  17. Korshunov S, Imlay JA. Detection and quantification of superoxide formed within the periplasm of Escherichia coli. J Bacteriol 2006; 188:6326–6334 [View Article] [PubMed]
    [Google Scholar]
  18. Battesti A, Majdalani N, Gottesman S. The RpoS-mediated general stress response in Escherichia coli. Annu Rev Microbiol 2011; 65:189–213 [View Article]
    [Google Scholar]
  19. Gottesman S. Trouble is coming: signaling pathways that regulate general stress responses in bacteria. J Biol Chem 2019; 294:11685–11700 [View Article] [PubMed]
    [Google Scholar]
  20. Wolfe AJ, Parikh N, Lima BP, Zemaitaitis B. Signal integration by the two-component signal transduction response regulator CpxR. J Bacteriol 2008; 190:2314–2322 [View Article] [PubMed]
    [Google Scholar]
  21. Lima BP, Thanh Huyen TT, Bäsell K, Becher D, Antelmann H et al. Inhibition of acetyl phosphate-dependent transcription by an acetylatable lysine on RNA polymerase. J Biol Chem 2012; 287:32147–32160 [View Article] [PubMed]
    [Google Scholar]
  22. Gopalkrishnan S, Nicoloff H, Ades SE. Co-ordinated regulation of the extracytoplasmic stress factor, sigmaE, with other Escherichia coli sigma factors by (p)ppGpp and DksA may be achieved by specific regulation of individual holoenzymes. Mol Microbiol 2014; 93:479–493 [View Article] [PubMed]
    [Google Scholar]
  23. Sineva E, Savkina M, Ades SE. Themes and variations in gene regulation by extracytoplasmic function (ECF) sigma factors. Current Opin Microbiol 2017; 36:128–137 [View Article]
    [Google Scholar]
  24. Dri A-M, Moreau PL. Phosphate starvation and low temperature as well as ultraviolet irradiation transcriptionally induce the Escherichia coli LexA-controlled gene sfiA. Mol Microbiol 1993; 8:697–706 [View Article] [PubMed]
    [Google Scholar]
  25. Moreau PL. Protective role of the RpoE (σE) and Cpx envelope stress responses against gentamicin killing of nongrowing Escherichia coli incubated under aerobic, phosphate starvation conditions. FEMS Microbiol Lett 2014; 357:151–156 [View Article] [PubMed]
    [Google Scholar]
  26. Moreau PL, Loiseau L. Characterization of acetic acid-detoxifying Escherichia coli evolved under phosphate starvation conditions. Microb Cell Fact 2016; 15:42 [View Article] [PubMed]
    [Google Scholar]
  27. Imlay JA. Transcription factors that defend bacteria against reactive oxygen species. Annu Rev Microbiol 2015; 69:93–108 [View Article] [PubMed]
    [Google Scholar]
  28. 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]
  29. Osterman A. Biogenesis and homeostasis of nicotinamide adenine dinucleotide cofactor. EcoSal Plus 2009; 3: [View Article] [PubMed]
    [Google Scholar]
  30. Romeo T, Snoep JL. Glycolysis and flux control. EcoSal Plus 2005; 1: [View Article] [PubMed]
    [Google Scholar]
  31. Cronan Jr JE, Laporte D, Stewart V. Tricarboxylic acid cycle and glyoxylate bypass. EcoSal Plus 2005; 1: [View Article]
    [Google Scholar]
  32. Korshunov S, Imlay JA. Two sources of endogenous hydrogen peroxide in Escherichia coli. Mol Microbiol 2010; 75:1389–1401 [View Article] [PubMed]
    [Google Scholar]
  33. 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 2005; 102:9317–9322 [View Article] [PubMed]
    [Google Scholar]
  34. Sontz PA, Mui TP, Fuss JO, Tainer JA, Barton JK. DNA charge transport as a first step in coordinating the detection of lesions by repair proteins. Proc Natl Acad Sci 2012; 109:1856–1861 [View Article] [PubMed]
    [Google Scholar]
  35. May KL, Lehman KM, Mitchell AM, Grabowicz M. A stress response monitoring lipoprotein trafficking to the outer membrane. mBio 2019; 10:e00618-19 [View Article]
    [Google Scholar]
  36. Guest RL, Wang J, Wong JL, Raivio TL. A bacterial stress response regulates respiratory protein complexes to control envelope stress adaptation. J Bacteriol 2017; 199:e00153-17 [View Article]
    [Google Scholar]
  37. Mulkidjanian AY, Heberle J, Cherepanov DA. Protons @ interfaces: implications for biological energy conversion. Biochimica et Biophysica Acta 2006; 1757:913–930 [View Article]
    [Google Scholar]
  38. Wolfe AJ. The acetate switch. Microbiol Mol Biol Rev 2005; 69:12–50 [View Article] [PubMed]
    [Google Scholar]
  39. Dri A-M, Moreau PL. Control of the LexA regulon by pH: evidence for a reversible inactivation of the LexA repressor during the growth cycle of Escherichia coli. Mol Microbiol 1994; 12:621–629 [View Article] [PubMed]
    [Google Scholar]
  40. Haverkorn van Rijsewijk BRB, Nanchen A, Nallet S, Kleijn RJ, Sauer U. Large-scale 13C-flux analysis reveals distinct transcriptional control of respiratory and fermentative metabolism in Escherichia coli. Mol Syst Biol 2011; 7:477 [View Article]
    [Google Scholar]
  41. Basan M, Hui S, Okano H, Zhang Z, Shen Y et al. Overflow metabolism in Escherichia coli results from efficient proteome allocation. Nature 2015; 528:99–104 [View Article] [PubMed]
    [Google Scholar]
  42. Cariss SJL, Tayler AE, Avison MB. Defining the growth conditions and promoter-proximal DNA sequences required for activation of gene expression by CreBC in Escherichia coli. J Bacteriol 2008; 190:3930–3939 [View Article] [PubMed]
    [Google Scholar]
  43. McCleary WR, Stock JB. Acetyl phosphate and the activation of two-component response regulators. J Biol Chem 1994; 269:31567–31572 [PubMed]
    [Google Scholar]
  44. Vuppada RK, Hansen CR, Strickland KAP, Kelly KM, McCleary WR. Phosphate signaling through alternate conformations of the PstSCAB phosphate transporter. BMC Microbiol 2018; 18:8 [View Article] [PubMed]
    [Google Scholar]
  45. Guillemet ML, Moreau PL. Activation of the cryptic PhnE permease promotes rapid adaptive evolution in a population of Escherichia coli K-12 starved for phosphate. J Bacteriol 2012; 194:253–260 [View Article] [PubMed]
    [Google Scholar]
  46. Germain E, Guiraud P, Byrne D, Douzi B, Djendli M et al. YtfK activates the stringent response by triggering the alarmone synthetase SpoT in Escherichia coli. Nat Commun 2019; 10:5763 [View Article]
    [Google Scholar]
  47. Fernández-Coll L, Cashel M. Contributions of SpoT hydrolase, SpoT synthetase, and RelA synthetase to carbon source diauxic growth transitions in Escherichia coli. Front Microbiol 2018; 9:1802 [View Article] [PubMed]
    [Google Scholar]
  48. Wu C, Balakrishnan R, Braniff N, Mori M, Manzanarez G et al. Cellular perception of growth rate and the mechanistic origin of bacterial growth law. Proc Natl Acad Sci 2022; 119:e2201585119 [View Article]
    [Google Scholar]
  49. Sanchez-Vazquez P, Dewey CN, Kitten N, Ross W, Gourse RL. Genome-wide effects on Escherichia coli transcription from ppGpp binding to its two sites on RNA polymerase. Proc Natl Acad Sci 2019; 116:8310–8319 [View Article] [PubMed]
    [Google Scholar]
  50. Leblanc SKD, Oates CW, Raivio TL. Characterization of the induction and cellular role of the BaeSR two-component envelope stress response of Escherichia coli. J Bacteriol 2011; 193:3367–3375 [View Article] [PubMed]
    [Google Scholar]
  51. Choudhary KS, Kleinmanns JA, Decker K, Sastry AV, Gao Y et al. Elucidation of regulatory modes for five two-component systems in Escherichia coli reveals novel relationships. mSystems 2020; 5:e00980-20 [View Article]
    [Google Scholar]
  52. Rhodius VA, Suh WC, Nonaka G, West J, Gross CA. Conserved and variable functions of the sigmaE stress response in related genomes. PLoS Biol 2006; 4:e2 [View Article]
    [Google Scholar]
  53. Gur E, Biran D, Ron EZ. Regulated proteolysis in Gram-negative bacteria--how and when?. Nat Rev Microbiol 2011; 9:839–848 [View Article]
    [Google Scholar]
  54. Yakhnin H, Aichele R, Ades SE, Romeo T, Babitzke P. Circuitry linking the global Csr- and σE-dependent cell envelope stress response systems. J Bacteriol 2017; 199:e00484-17 [View Article]
    [Google Scholar]
  55. Camacho MI, Alvarez AF, Chavez RG, Romeo T, Merino E et al. Effects of the global regulator CsrA on the BarA/UvrY two-component signaling system. J Bacteriol 2015; 197:983–991 [View Article] [PubMed]
    [Google Scholar]
  56. Moreau PL. The lysine decarboxylase CadA protects Escherichia coli starved of phosphate against fermentation acids. J Bacteriol 2007; 189:2249–2261 [View Article] [PubMed]
    [Google Scholar]
  57. Sassanfar M, Roberts JW. Nature of the SOS-inducing signal in Escherichia coli. The involvement of DNA replication. J Mol Biol 1990; 212:79–96 [View Article] [PubMed]
    [Google Scholar]
  58. Moreau PL. Effects of overproduction of single-stranded DNA-binding protein on RecA protein-dependent processes in Escherichia coli. J Mol Biol 1987; 194:621–634 [View Article] [PubMed]
    [Google Scholar]
  59. Moreau PL, Carlier M-F. RecA protein-promoted cleavage of LexA repressor in the presence of ADP and structural analogues of inorganic phosphate, the fluoride complexes of aluminum and beryllium. J Biol Chem 1989; 264:2302–2306 [View Article]
    [Google Scholar]
  60. Umezu K, Kolodner RD. Protein interactions in genetic recombination in Escherichia coli. Interactions involving RecO and RecR overcome the inhibition of RecA by single-stranded DNA-binding protein. J Biol Chem 1994; 269:30005–30013 [View Article]
    [Google Scholar]
  61. Bell JC, Liu B, Kowalczykowski SC. Imaging and energetics of single SSB-ssDNA molecules reveal intramolecular condensation and insight into RecOR function. Elife 2015; 4:e08646 [View Article] [PubMed]
    [Google Scholar]
  62. Godoy VG, Jarosz DF, Simon SM, Abyzov A, Ilyin V et al. UmuD and RecA directly modulate the mutagenic potential of the Y family DNA polymerase DinB. Mol Cell 2007; 28:1058–1070 [View Article] [PubMed]
    [Google Scholar]
  63. Joseph AM, Badrinarayanan A. Visualizing mutagenic repair: novel insights into bacterial translesion synthesis. FEMS Microbiol Rev 2020; 44:572–582 [View Article] [PubMed]
    [Google Scholar]
  64. Tuan PM, Gilhooly NS, Marians KJ, Kowalczykowski SC. Direct visualization of translesion DNA synthesis polymerase IV at the replisome. Proc Natl Acad Sci 2022; 119:e2208390119 [View Article]
    [Google Scholar]
  65. Moreau PL. Overproduction of single-stranded-DNA-binding protein specifically inhibits recombination of UV-irradiated bacteriophage DNA in Escherichia coli. J Bacteriol 1988; 170:2493–2500 [View Article] [PubMed]
    [Google Scholar]
  66. Dri A-M, Moreau PL. Properties of RecA441 protein reveal a possible role for RecF and SSB proteins in Escherichia coli. Mol Gen Genet 1991; 227:488–492 [View Article] [PubMed]
    [Google Scholar]
  67. Henrikus SS, Henry C, Ghodke H, Wood EA, Mbele N et al. RecFOR epistasis group: RecF and RecO have distinct localizations and functions in Escherichia coli. Nucleic Acids Res 2019; 47:2946–2965 [View Article] [PubMed]
    [Google Scholar]
  68. Lin L-L, Little JW. Isolation and characterization of noncleavable (ind-) mutants of the lexa repressor of Escherichia coli K-12. J Bacteriol 1988; 170:2163–2173 [View Article]
    [Google Scholar]
  69. Luo Y, Pfuetzner RA, Mosimann S, Paetzel M, Frey EA et al. Crystal structure of lexa: a conformational switch for regulation of self-cleavage. Cell 2001; 106:585–594 [View Article]
    [Google Scholar]
  70. Jones EC, Uphoff S. Single-molecule imaging of LexA degradation in Escherichia coli elucidates regulatory mechanisms and heterogeneity of the SOS response. Nat Microbiol 2021; 6:981–990 [View Article] [PubMed]
    [Google Scholar]
  71. Zhang APP, Pigli YZ, Rice PA. Structure of the LexA-DNA complex and implications for SOS box measurement. Nature 2010; 466:883–886 [View Article] [PubMed]
    [Google Scholar]
  72. Winkelmann I, Uzdavinys P, Kenney IM, Brock J, Meier PF et al. Crystal structure of the Na+/H+ antiporter NhaA at active pH reveals the mechanistic basis for pH sensing. Nat Commun 2022; 13: [View Article]
    [Google Scholar]
  73. Booth JA, Špírek M, Lobie TA, Skarstad K, Krejci L et al. Antibiotic-induced DNA damage results in a controlled loss of pH homeostasis and genome instability. Sci Rep 2020; 10:19422 [View Article] [PubMed]
    [Google Scholar]
  74. Schramke H, Laermann V, Tegetmeyer HE, Brachmann A, Jung K et al. Revisiting regulation of potassium homeostasis in Escherichia coli: the connection to phosphate limitation. MicrobiologyOpen 2017; 6:e00438 [View Article] [PubMed]
    [Google Scholar]
  75. Lüttmann D, Göpel Y, Görke B. The phosphotransferase protein EIIA(Ntr) modulates the phosphate starvation response through interaction with histidine kinase PhoR in Escherichia coli. Mol Microbiol 2012; 86:96–110 [View Article] [PubMed]
    [Google Scholar]
  76. Lee C-R, Park Y-H, Kim M, Kim Y-R, Park S et al. Reciprocal regulation of the autophosphorylation of enzyme INtr by glutamine and α-ketoglutarate in Escherichia coli. Mol Microbiol 2013; 88:473–485 [View Article] [PubMed]
    [Google Scholar]
  77. Euro L, Belevich G, Wikström M, Verkhovskaya M. High affinity cation-binding sites in Complex I from Escherichia coli. Biochim Biophys Acta 2009; 1787:1024–1028 [View Article]
    [Google Scholar]
  78. Sun Z, Cagliero C, Izard J, Chen Y, Zhou YN et al. Density of σ70 promoter-like sites in the intergenic regions dictates the redistribution of RNA polymerase during osmotic stress in Escherichia coli. Nucleic Acids Res 2019; 47:3970–3985 [View Article] [PubMed]
    [Google Scholar]
  79. Anand A, Olson CA, Sastry AV, Patel A, Szubin R et al. Restoration of fitness lost due to dysregulation of the pyruvate dehydrogenase complex is triggered by ribosomal binding site modifications. Cell Rep 2021; 35:108961 [View Article]
    [Google Scholar]
  80. Py B, Moreau PL, Barras F. Fe–S clusters, fragile sentinels of the cell. Current Opin Microbiol 2011; 14:218–223 [View Article]
    [Google Scholar]
  81. Gérard F, Dri A-M, Moreau PL. Role of Escherichia coli RpoS, LexA and H-NS global regulators in metabolism and survival under aerobic, phosphate-starvation conditions. Microbiology 1999; 145:1547–1562 [View Article]
    [Google Scholar]
  82. Anand A, Chen K, Yang L, Sastry AV, Olson CA et al. Adaptive evolution reveals a tradeoff between growth rate and oxidative stress during naphthoquinone-based aerobic respiration. Proc Natl Acad Sci 2019; 116:25287–25292 [View Article] [PubMed]
    [Google Scholar]
  83. Pin C, Rolfe MD, Muñoz-Cuevas M, Hinton JCD, Peck MW et al. Network analysis of the transcriptional pattern of young and old cells of Escherichia coli during lag phase. BMC Syst Biol 2009; 3:108 [View Article]
    [Google Scholar]
  84. Fritz G, Walker N, Gerland U. Heterogeneous timing of gene induction as a regulation strategy. J Mol Biol 2019; 431:4760–4774 [View Article] [PubMed]
    [Google Scholar]
  85. Zamora M, Ziegler CA, Freddolino PL, Wolfe AJ. A thermosensitive, phase-variable epigenetic switch: pap revisited. Microbiol Mol Biol Rev 2020; 84:e00030-17 [View Article]
    [Google Scholar]
  86. Mitchell A, Romano GH, Groisman B, Yona A, Dekel E et al. Adaptive prediction of environmental changes by microorganisms. Nature 2009; 460:220–224 [View Article] [PubMed]
    [Google Scholar]
  87. Vemparala B, Valiya Parambathu A, Saini DK, Dixit NM. An evolutionary paradigm favoring cross talk between bacterial two-component signaling systems. mSystems 2022; 7:e0029822 [View Article]
    [Google Scholar]
  88. Sharma R, Shimada T, Mishra VK, Upreti S, Sardesai AA. Growth inhibition by external potassium of Escherichia coli lacking PtsN (EIIANtr) is caused by potassium limitation mediated by YcgO. J Bacteriol 2016; 198:1868–1882 [View Article] [PubMed]
    [Google Scholar]
  89. Kotte O, Zaugg JB, Heinemann M. Bacterial adaptation through distributed sensing of metabolic fluxes. Mol Syst Biol 2010; 6:6 [View Article]
    [Google Scholar]
  90. Kim D, Seo SW, Gao Y, Nam H, Guzman GI et al. Systems assessment of transcriptional regulation on central carbon metabolism by Cra and CRP. Nucleic Acids Res 2018; 46:2901–2917 [View Article] [PubMed]
    [Google Scholar]
  91. Bley Folly B, Ortega AD, Hubmann G, Bonsing-Vedelaar S, Wijma HJ et al. Assessment of the interaction between the flux-signaling metabolite fructose-1,6-bisphosphate and the bacterial transcription factors CggR and Cra. Mol Microbiol 2018; 109:278–290 [View Article] [PubMed]
    [Google Scholar]
  92. Shimada T, Yamamoto K, Ishihama A. Novel members of the Cra regulon involved in carbon metabolism in Escherichia coli. J Bacteriol 2011; 193:649–659 [View Article] [PubMed]
    [Google Scholar]
  93. Son Y-J, Phue J-N, Trinh LB, Lee SJ, Shiloach J. The role of Cra in regulating acetate excretion and osmotic tolerance in E. coli K-12 and E. coli B at high density growth. Microb Cell Fact 2011; 10:52 [View Article]
    [Google Scholar]
  94. Massé E, Vanderpool CK, Gottesman S. Effect of RyhB small RNA on global iron use in Escherichia coli. J Bacteriol 2005; 187:6962–6971 [View Article] [PubMed]
    [Google Scholar]
  95. 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]
    [Google Scholar]
  96. Fontenot CR, Tasnim H, Valdes KA, Popescu CV, Ding H. Ferric uptake regulator (Fur) reversibly binds a [2Fe-2S] cluster to sense intracellular iron homeostasis in Escherichia coli. J Biol Chem 2020; 295:15454–15463 [View Article]
    [Google Scholar]
  97. Guillemet ML, Moreau PL. Fur-dependent detoxification of organic acids by rpoS mutants during prolonged incubation under aerobic, phosphate starvation conditions. J Bacteriol 2008; 190:5567–5575 [View Article] [PubMed]
    [Google Scholar]
  98. Manuse S, Shan Y, Canas-Duarte SJ, Bakshi S, Sun W-S et al. Bacterial persisters are a stochastically formed subpopulation of low-energy cells. PLoS Biol 2021; 19:e3001194 [View Article]
    [Google Scholar]
  99. Peterson CN, Levchenko I, Rabinowitz JD, Baker TA, Silhavy TJ. RpoS proteolysis is controlled directly by ATP levels in Escherichia coli. Genes Dev 2012; 26:548–553 [View Article] [PubMed]
    [Google Scholar]
  100. Salvail H, Lanthier-Bourbonnais P, Sobota JM, Caza M, Benjamin J-A et al. A small RNA promotes siderophore production through transcriptional and metabolic remodeling. Proc Natl Acad Sci 2010; 107:15223–15228 [View Article] [PubMed]
    [Google Scholar]
  101. Winther KS, Sørensen MA, Svenningsen SL. Polyamines are required for tRNA anticodon modification in Escherichia coli. J Mol Biol 2021; 433:167073 [View Article] [PubMed]
    [Google Scholar]
  102. Ha HC, Sirisoma NS, Kuppusamy P, Zweier JL, Woster PM et al. The natural polyamine spermine functions directly as a free radical scavenger. Proc Natl Acad Sci 1998; 95:11140–11145 [View Article] [PubMed]
    [Google Scholar]
  103. Bauerle MR, Schwalm EL, Booker S. Mechanistic diversity of radical S-adenosylmethionine (SAM)-dependent methylation. J Biol Chem 2015; 290:3995–4002 [View Article]
    [Google Scholar]
  104. Mielecki D, Grzesiuk E. Ada response - a strategy for repair of alkylated DNA in bacteria. FEMS Microbiol Lett 2014; 355:1–11 [View Article] [PubMed]
    [Google Scholar]
  105. Esakova OA, Grove TL, Yennawar NH, Arcinas AJ, Wang B et al. Structural basis for tRNA methylthiolation by the radical SAM enzyme MiaB. Nature 2021; 597:566–570 [View Article] [PubMed]
    [Google Scholar]
  106. Ballesteros M, Fredriksson A, Henriksson J, Nyström T. Bacterial senescence: protein oxidation in non-proliferating cells is dictated by the accuracy of the ribosomes. EMBO J 2001; 20:5280–5289 [View Article] [PubMed]
    [Google Scholar]
  107. Bergholz PW, Noar JD, Buckley DH. Environmental patterns are imposed on the population structure of Escherichia coli after fecal deposition. Appl Environ Microbiol 2011; 77:211–219 [View Article]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.001312
Loading
/content/journal/micro/10.1099/mic.0.001312
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error