1887

Abstract

Inorganic polyphosphate (polyP) is synthesized by bacteria under stressful environmental conditions and acts by a variety of mechanisms to promote cell survival. While the kinase that synthesizes polyP (PPK, encoded by the gene) is well known, transcription is not activated by environmental stress and little is understood about how environmental stress signals lead to polyP accumulation. Previous work has shown that the transcriptional regulators DksA, RpoN (σ) and RpoE (σ) positively regulate polyP production, but not transcription, in . In this work, we examine the role of the alternative sigma factor RpoN and nitrogen starvation stress response pathways in controlling polyP synthesis. We show that the RpoN enhancer binding proteins GlnG and GlrR impact polyP production, and uncover a new role for the nitrogen phosphotransferase regulator PtsN (EIIA) as a positive regulator of polyP production, acting upstream of DksA, downstream of RpoN and apparently independently of RpoE. However, neither these regulatory proteins nor common nitrogen metabolites appear to act directly on PPK, and the precise mechanism(s) by which polyP production is modulated after stress remain(s) unclear. Unexpectedly, we also found that the genes that impact polyP production vary depending on the composition of the rich media in which the cells were grown before exposure to polyP-inducing stress. These results constitute progress towards deciphering the regulatory networks driving polyP production under stress, and highlight the remarkable complexity of this regulation and its connections to a broad range of stress-sensing pathways.

Keyword(s): EIIANtr , polyP , PtsN and RpoN
Funding
This study was supported by the:
  • National Institute of General Medical Sciences (Award GM124590)
    • Principle Award Recipient: MichaelJeffrey Gray
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2022-04-28
2024-04-18
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References

  1. Denoncourt A, Downey M. Model systems for studying polyphosphate biology: a focus on microorganisms. Curr Genet 2021; 67:331–346 [View Article] [PubMed]
    [Google Scholar]
  2. Desfougères Y, Saiardi A, Azevedo C. Inorganic polyphosphate in mammals: where’s Wally?. Biochem Soc Trans 2020; 48:95–101 [View Article] [PubMed]
    [Google Scholar]
  3. Albi T, Serrano A. Inorganic polyphosphate in the microbial world. Emerging roles for a multifaceted biopolymer. World J Microbiol Biotechnol 2016; 32:27 [View Article] [PubMed]
    [Google Scholar]
  4. Beaufay F, Quarles E, Franz A, Katamanin O, Wholey WY et al. Polyphosphate functions in vivo as an iron chelator and Fenton reaction inhibitor. mBio 2020; 11:e01017-20 [View Article] [PubMed]
    [Google Scholar]
  5. Dai S, Xie Z, Wang B, Yu N, Zhao J et al. Dynamic polyphosphate metabolism coordinating with manganese ions defends against oxidative stress in the extreme bacterium Deinococcus radiodurans. Appl Environ Microbiol 2021; 87:e02785-20 [View Article] [PubMed]
    [Google Scholar]
  6. Gray MJ, Jakob U. Oxidative stress protection by polyphosphate--new roles for an old player. Curr Opin Microbiol 2015; 24:1–6 [View Article] [PubMed]
    [Google Scholar]
  7. Xie L, Jakob U. Inorganic polyphosphate, a multifunctional polyanionic protein scaffold. J Biol Chem 2019; 294:2180–2190 [View Article] [PubMed]
    [Google Scholar]
  8. Racki LR, Tocheva EI, Dieterle MG, Sullivan MC, Jensen GJ et al. Polyphosphate granule biogenesis is temporally and functionally tied to cell cycle exit during starvation in Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 2017; 114:E2440–E2449 [View Article] [PubMed]
    [Google Scholar]
  9. Gross MH, Konieczny I. Polyphosphate induces the proteolysis of ADP-bound fraction of initiator to inhibit DNA replication initiation upon stress in Escherichia coli. Nucleic Acids Res 2020; 48:5457–5466 [View Article] [PubMed]
    [Google Scholar]
  10. Beaufay F, Amemiya HM, Guan J, Basalla J, Meinen BA et al. Polyphosphate drives bacterial heterochromatin formation. Sci Adv 2021; 7:eabk0233 [View Article] [PubMed]
    [Google Scholar]
  11. Gautam LK, Sharma P, Capalash N. Bacterial polyphosphate kinases revisited: role in pathogenesis and therapeutic potential. Curr Drug Targets 2019; 20:292–301 [View Article] [PubMed]
    [Google Scholar]
  12. Rao NN, Gómez-García MR, Kornberg A. Inorganic polyphosphate: essential for growth and survival. Annu Rev Biochem 2009; 78:605–647 [View Article] [PubMed]
    [Google Scholar]
  13. Bowlin MQ, Gray MJ. Inorganic polyphosphate in host and microbe biology. Trends Microbiol 2021; 29:1013–1023 [View Article] [PubMed]
    [Google Scholar]
  14. Suess PM, Chinea LE, Pilling D, Gomer RH. Extracellular polyphosphate promotes macrophage and fibrocyte differentiation, inhibits leukocyte proliferation, and acts as a chemotactic agent for neutrophils. J Immunol 2019; 203:493–499 [View Article] [PubMed]
    [Google Scholar]
  15. Roewe J, Stavrides G, Strueve M, Sharma A, Marini F et al. Bacterial polyphosphates interfere with the innate host defense to infection. Nat Commun 2020; 11:4035 [View Article] [PubMed]
    [Google Scholar]
  16. Rijal R, Cadena LA, Smith MR, Carr JF, Gomer RH. Polyphosphate is an extracellular signal that can facilitate bacterial survival in eukaryotic cells. Proc Natl Acad Sci U S A 2020; 117:31923–31934 [View Article] [PubMed]
    [Google Scholar]
  17. McDonald B, Davis RP, Kim S-J, Tse M, Esmon CT et al. Platelets and neutrophil extracellular traps collaborate to promote intravascular coagulation during sepsis in mice. Blood 2017; 129:1357–1367 [View Article] [PubMed]
    [Google Scholar]
  18. Peng L, Zeng L, Jin H, Yang L, Xiao Y et al. Discovery and antibacterial study of potential PPK1 inhibitors against uropathogenic E. coli. J Enzyme Inhib Med Chem 2020; 35:1224–1232 [View Article] [PubMed]
    [Google Scholar]
  19. Neville N, Roberge N, Ji X, Stephen P, Lu JL et al. A dual-specificity inhibitor targets polyphosphate kinase 1 and 2 enzymes to attenuate virulence of Pseudomonas aeruginosa. mBio 2021; 12:e0059221 [View Article] [PubMed]
    [Google Scholar]
  20. Bravo-Toncio C, Álvarez JA, Campos F, Ortíz-Severín J, Varas M et al. Dictyostelium discoideum as a surrogate host-microbe model for antivirulence screening in Pseudomonas aeruginosa PAO1. Int J Antimicrob Agents 2016; 47:403–409 [View Article] [PubMed]
    [Google Scholar]
  21. Dahl J-U, Gray MJ, Bazopoulou D, Beaufay F, Lempart J et al. The anti-inflammatory drug mesalamine targets bacterial polyphosphate accumulation. Nat Microbiol 2017; 2:16267 [View Article] [PubMed]
    [Google Scholar]
  22. Ault-Riché D, Fraley CD, Tzeng CM, Kornberg A. Novel assay reveals multiple pathways regulating stress-induced accumulations of inorganic polyphosphate in Escherichia coli. J Bacteriol 1998; 180:1841–1847 [View Article] [PubMed]
    [Google Scholar]
  23. Gray MJ, Wholey W-Y, Wagner NO, Cremers CM, Mueller-Schickert A et al. Polyphosphate is a primordial chaperone. Mol Cell 2014; 53:689–699 [View Article] [PubMed]
    [Google Scholar]
  24. Yoo NG, Dogra S, Meinen BA, Tse E, Haefliger J et al. Polyphosphate stabilizes protein unfolding intermediates as soluble amyloid-like oligomers. J Mol Biol 2018; 430:4195–4208 [View Article] [PubMed]
    [Google Scholar]
  25. Morohoshi T, Maruo T, Shirai Y, Kato J, Ikeda T et al. Accumulation of inorganic polyphosphate in phoU mutants of Escherichia coli and Synechocystis sp. strain PCC6803. Appl Environ Microbiol 2002; 68:4107–4110 [View Article] [PubMed]
    [Google Scholar]
  26. Kuroda A, Murphy H, Cashel M, Kornberg A. Guanosine tetra- and pentaphosphate promote accumulation of inorganic polyphosphate in Escherichia coli. J Biol Chem 1997; 272:21240–21243 [View Article] [PubMed]
    [Google Scholar]
  27. Akiyama M, Crooke E, Kornberg A. An exopolyphosphatase of Escherichia coli. The enzyme and its ppx gene in a polyphosphate operon. J Biol Chem 1993; 268:633–639
    [Google Scholar]
  28. Gray MJ. Interactions between DksA and stress-responsive alternative sigma factors control inorganic polyphosphate accumulation in Escherichia coli. J Bacteriol 2020; 202:e00133-20 [View Article] [PubMed]
    [Google Scholar]
  29. Rudat AK, Pokhrel A, Green TJ, Gray MJ. Mutations in Escherichia coli polyphosphate kinase that lead to dramatically increased in vivo polyphosphate levels. J Bacteriol 2018; 200:e00697-17 [View Article] [PubMed]
    [Google Scholar]
  30. Gray MJ. Inorganic polyphosphate accumulation in Escherichia coli is regulated by DksA but not by (p)ppGpp. J Bacteriol 2019; 201:e00664-18 [View Article] [PubMed]
    [Google Scholar]
  31. Danson AE, Jovanovic M, Buck M, Zhang X. Mechanisms of σ54-dependent transcription initiation and regulation. J Mol Biol 2019; 431:3960–3974 [View Article]
    [Google Scholar]
  32. Riordan JT, Mitra A. Regulation of Escherichia coli pathogenesis by alternative sigma factor N. EcoSal Plus 2017; 7: [View Article] [PubMed]
    [Google Scholar]
  33. Keseler IM, Mackie A, Santos-Zavaleta A, Billington R, Bonavides-Martínez C et al. The EcoCyc database: reflecting new knowledge about Escherichia coli K-12. Nucleic Acids Res 2017; 45:D543–D550 [View Article] [PubMed]
    [Google Scholar]
  34. van Heeswijk WC, Westerhoff HV, Boogerd FC. Nitrogen assimilation in Escherichia coli: putting molecular data into a systems perspective. Microbiol Mol Biol Rev 2013; 77:628–695 [View Article] [PubMed]
    [Google Scholar]
  35. Göpel Y, Görke B. Interaction of lipoprotein QseG with sensor kinase QseE in the periplasm controls the phosphorylation state of the two-component system QseE/QseF in Escherichia coli. PLoS Genet 2018; 14:e1007547 [View Article] [PubMed]
    [Google Scholar]
  36. Reichenbach B, Göpel Y, Görke B. Dual control by perfectly overlapping sigma 54- and sigma 70- promoters adjusts small RNA GlmY expression to different environmental signals. Mol Microbiol 2009; 74:1054–1070 [View Article]
    [Google Scholar]
  37. Klein G, Stupak A, Biernacka D, Wojtkiewicz P, Lindner B et al. Multiple transcriptional factors regulate transcription of the rpoE gene in Escherichia coli under different growth conditions and when the lipopolysaccharide biosynthesis is defective. J Biol Chem 2016; 291:22999–23019 [View Article]
    [Google Scholar]
  38. Pflüger-Grau K, Görke B. Regulatory roles of the bacterial nitrogen-related phosphotransferase system. Trends Microbiol 2010; 18:205–214 [View Article]
    [Google Scholar]
  39. Guo B, Bi Y. Cloning PCR products. an overview. Methods Mol Biol 2002; 192:111–119 [View Article]
    [Google Scholar]
  40. Sambrook J, Fritsch EF, Maniatis T. Molecular Cloning: A Laboratory Manual, 2nd ed. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press; 1989
    [Google Scholar]
  41. Bertani G. Studies on lysogenesis. I. The mode of phage liberation by lysogenic Escherichia coli. J Bacteriol 1951; 62:293–300 [View Article] [PubMed]
    [Google Scholar]
  42. Choi J, Kim H, Chang Y, Yoo W, Kim D et al. Programmed delay of a virulence circuit promotes Salmonella pathogenicity. mBio 2019; 10:e00291-19 [View Article] [PubMed]
    [Google Scholar]
  43. Daimon Y, Narita S, Akiyama Y. Activation of toxin-antitoxin system toxins suppresses lethality caused by the loss of σE in Escherichia coli. J Bacteriol 2015; 197:2316–2324 [View Article] [PubMed]
    [Google Scholar]
  44. Chen I-MA, Chu K, Palaniappan K, Ratner A, Huang J et al. The IMG/M data management and analysis system v.6.0: new tools and advanced capabilities. Nucleic Acids Res 2021; 49:D751–D763 [View Article] [PubMed]
    [Google Scholar]
  45. Santos-Zavaleta A, Salgado H, Gama-Castro S, Sánchez-Pérez M, Gómez-Romero L et al. RegulonDB v 10.5: tackling challenges to unify classic and high throughput knowledge of gene regulation in E. coli K-12. Nucleic Acids Res 2019; 47:D212–D220 [View Article] [PubMed]
    [Google Scholar]
  46. Blattner FR, Plunkett G, Bloch CA, Perna NT, Burland V et al. The complete genome sequence of Escherichia coli K-12. Science 1997; 277:1453–1462 [View Article]
    [Google Scholar]
  47. Silhavy TJ, Berman ML, Enquist LW. Experiments with Gene Fusions Cold Spring Harbor, NY: Cold Spring Harbor Laboratory; 1984
    [Google Scholar]
  48. Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y et al. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol 2006; 2:0008 [View Article]
    [Google Scholar]
  49. Datsenko KA, Wanner BL. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 2000; 97:6640–6645 [View Article]
    [Google Scholar]
  50. Blauwkamp TA, Ninfa AJ. Physiological role of the GlnK signal transduction protein of Escherichia coli: survival of nitrogen starvation. Mol Microbiol 2002; 46:203–214 [View Article]
    [Google Scholar]
  51. Uzzau S, Figueroa-Bossi N, Rubino S, Bossi L. Epitope tagging of chromosomal genes in Salmonella. Proc Natl Acad Sci U S A 2001; 98:15264–15269 [View Article] [PubMed]
    [Google Scholar]
  52. Bonocora RP, Smith C, Lapierre P, Wade JT. Genome-scale mapping of Escherichia coli σ54 reveals widespread, conserved intragenic binding. PLoS Genet 2015; 11:10 [View Article] [PubMed]
    [Google Scholar]
  53. Guzman LM, Belin D, Carson MJ, Beckwith J. Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol 1995; 177:4121–4130 [View Article] [PubMed]
    [Google Scholar]
  54. Watson JF, García-Nafría J. In vivo DNA assembly using common laboratory bacteria: A re-emerging tool to simplify molecular cloning. J Biol Chem 2019; 294:15271–15281 [View Article] [PubMed]
    [Google Scholar]
  55. De Genst EJ, Guilliams T, Wellens J, O’Day EM, Waudby CA et al. Structure and properties of a complex of α-synuclein and a single-domain camelid antibody. J Mol Biol 2010; 402:326–343 [View Article] [PubMed]
    [Google Scholar]
  56. Huang Y, Zhang L. An in vitro single-primer site-directed mutagenesis method for use in biotechnology. Methods Mol Biol 2017; 1498:375–383 [View Article] [PubMed]
    [Google Scholar]
  57. Karimova G, Pidoux J, Ullmann A, Ladant D. A bacterial two-hybrid system based on a reconstituted signal transduction pathway. Proc Natl Acad Sci U S A 1998; 95:5752–5756 [View Article] [PubMed]
    [Google Scholar]
  58. Pokhrel A, Lingo JC, Wolschendorf F, Gray MJ. Assaying for inorganic polyphosphate in bacteria. J Vis Exp 2019; 2019:143 [View Article] [PubMed]
    [Google Scholar]
  59. Neidhardt FC, Bloch PL, Smith DF. Culture medium for enterobacteria. J Bacteriol 1974; 119:736–747 [View Article] [PubMed]
    [Google Scholar]
  60. Wurst H, Kornberg A. A soluble exopolyphosphatase of Saccharomyces cerevisiae. purification and characterization. J Biol Chem 1994; 269:10996–11001 [View Article]
    [Google Scholar]
  61. Christ JJ, Blank LM. Enzymatic quantification and length determination of polyphosphate down to a chain length of two. Anal Biochem 2018; 548:82–90 [View Article] [PubMed]
    [Google Scholar]
  62. Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 2008; 3:1101–1108 [View Article] [PubMed]
    [Google Scholar]
  63. Bennett BD, Kimball EH, Gao M, Osterhout R, Van Dien SJ et al. Absolute metabolite concentrations and implied enzyme active site occupancy in Escherichia coli. Nat Chem Biol 2009; 5:593–599 [View Article] [PubMed]
    [Google Scholar]
  64. Schaefer J, Jovanovic G, Kotta-Loizou I, Buck M. Single-step method for β-galactosidase assays in Escherichia coli using a 96-well microplate reader. Anal Biochem 2016; 503:56–57 [View Article] [PubMed]
    [Google Scholar]
  65. Pillai-Kastoori L, Schutz-Geschwender AR, Harford JA. A systematic approach to quantitative Western blot analysis. Anal Biochem 2020; 593:113608 [View Article] [PubMed]
    [Google Scholar]
  66. Kurien BT, Scofield RH. Introduction to protein blotting. Methods Mol Biol 2009; 536:9–22 [View Article]
    [Google Scholar]
  67. Schneider CA, Rasband WS, Eliceiri KW. NIH image to imagej: 25 years of image analysis. Nat Methods 2012; 9:671–675 [View Article]
    [Google Scholar]
  68. Ikeda TP, Shauger AE, Kustu S. Salmonella typhimurium apparently perceives external nitrogen limitation as internal glutamine limitation. J Mol Biol 1996; 259:589–607 [View Article]
    [Google Scholar]
  69. Huergo LF, Dixon R. The emergence of 2-oxoglutarate as a master regulator metabolite. Microbiol Mol Biol Rev 2015; 79:419–435 [View Article]
    [Google Scholar]
  70. Atkinson MR, Blauwkamp TA, Ninfa AJ. Context-dependent functions of the PII and glnk signal transduction proteins in Escherichia coli. J Bacteriol 2002; 184:5364–5375 [View Article]
    [Google Scholar]
  71. Gosztolai A, Schumacher J, Behrends V, Bundy JG, Heydenreich F et al. GlnK facilitates the dynamic regulation of bacterial nitrogen assimilation. Biophys J 2017; 112:2219–2230 [View Article] [PubMed]
    [Google Scholar]
  72. Forchhammer K, Lüddecke J. Sensory properties of the PII signalling protein family. FEBS J 2016; 283:425–437 [View Article] [PubMed]
    [Google Scholar]
  73. Maeda K, Westerhoff HV, Kurata H, Boogerd FC. Ranking network mechanisms by how they fit diverse experiments and deciding on E. coli’s ammonium transport and assimilation network. NPJ Syst Biol Appl 2019; 5:14 [View Article] [PubMed]
    [Google Scholar]
  74. Blauwkamp TA, Ninfa AJ. Antagonism of PII signalling by the AmtB protein of Escherichia coli. Mol Microbiol 2003; 48:1017–1028 [View Article] [PubMed]
    [Google Scholar]
  75. Rodionova IA, Goodacre N, Babu M, Emili A, Uetz P et al. The nitrogen regulatory PII protein (GlnB) and N-acetylglucosamine 6-phosphate epimerase (NanE) allosterically activate glucosamine 6-phosphate deaminase (NagB) in Escherichia coli. J Bacteriol 2018; 200:e00691-17 [View Article] [PubMed]
    [Google Scholar]
  76. Schubert C, Zedler S, Strecker A, Unden G. L-Aspartate as a high-quality nitrogen source in Escherichia coli: Regulation of L-aspartase by the nitrogen regulatory system and interaction of L-aspartase with GlnB. Mol Microbiol 2021; 115:526–538 [View Article]
    [Google Scholar]
  77. Atkinson MR, Ninfa AJ. Role of the glnk signal transduction protein in the regulation of nitrogen assimilation in Escherichia coli. Mol Microbiol 1998; 29:431–447 [View Article]
    [Google Scholar]
  78. Sezonov G, Joseleau-Petit D, D’Ari R. Escherichia coli physiology in luria-bertani broth. J Bacteriol 2007; 189:8746–8749 [View Article]
    [Google Scholar]
  79. Yakhnin H, Aichele R, Ades SE, Romeo T, Babitzke P. Circuitry linking the global csr- and sigma(E)-dependent cell envelope stress response systems. J Bacteriol 2017; 199:23 [View Article]
    [Google Scholar]
  80. Hews CL, Cho T, Rowley G, Raivio TL. Maintaining integrity under stress: envelope stress response regulation of pathogenesis in gram-negative bacteria. Front Cell Infect Microbiol 2019; 9:313 [View Article]
    [Google Scholar]
  81. Khan MA, Durica-Mitic S, Göpel Y, Heermann R, Görke B. Small RNA-binding protein RapZ mediates cell envelope precursor sensing and signaling in Escherichia coli. EMBO J 2020; 39:e103848 [View Article] [PubMed]
    [Google Scholar]
  82. Durica-Mitic S, Göpel Y, Amman F, Görke B. Adaptor protein RapZ activates endoribonuclease RNase E by protein-protein interaction to cleave a small regulatory RNA. RNA 2020; 26:1198–1215 [View Article] [PubMed]
    [Google Scholar]
  83. Teplyakov A, Leriche C, Obmolova G, Badet B, Badet-Denisot MA. From Lobry de Bruyn to enzyme-catalyzed ammonia channelling: molecular studies of D-glucosamine-6P synthase. Nat Prod Rep 2002; 19:60–69 [View Article] [PubMed]
    [Google Scholar]
  84. Mouilleron S, Badet-Denisot MA, Badet B, Golinelli-Pimpaneau B. Dynamics of glucosamine-6-phosphate synthase catalysis. Arch Biochem Biophys 2011; 505:1–12 [View Article] [PubMed]
    [Google Scholar]
  85. Yoo W, Choi J, Park B, Byndloss MX, Ryu S. A nitrogen metabolic enzyme provides Salmonella fitness advantage by promoting utilization of microbiota-derived carbon source. ACS Infect Dis 2021; 7:1208–1220 [View Article] [PubMed]
    [Google Scholar]
  86. Yoo W, Yoon H, Seok YJ, Lee CR, Lee HH et al. Fine-tuning of amino sugar homeostasis by EIIA(Ntr) in Salmonella Typhimurium. Sci Rep 2016; 6:33055 [View Article]
    [Google Scholar]
  87. Kim HJ, Lee CR, Kim M, Peterkofsky A, Seok YJ. Dephosphorylated npr of the nitrogen PTS regulates lipid A biosynthesis by direct interaction with lpxd. Biochem Biophys Res Commun 2011; 409:556–561 [View Article]
    [Google Scholar]
  88. Lee J, Park YH, Kim YR, Seok YJ, Lee CR. Dephosphorylated NPr is involved in an envelope stress response of Escherichia coli. Microbiology (Reading) 2015; 161:1113–1123 [View Article]
    [Google Scholar]
  89. Choi J, Ryu S. Regulation of iron uptake by fine-tuning the iron responsiveness of the iron sensor Fur. Appl Environ Microbiol 2019; 85:e03026-18 [View Article]
    [Google Scholar]
  90. Deutscher J, Aké FMD, Derkaoui M, Zébré AC, Cao TN et al. The bacterial phosphoenolpyruvate:carbohydrate phosphotransferase system: regulation by protein phosphorylation and phosphorylation-dependent protein-protein interactions. Microbiol Mol Biol Rev 2014; 78:231–256 [View Article]
    [Google Scholar]
  91. 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]
  92. Rabus R, Reizer J, Paulsen I, Saier MH. Enzyme I(Ntr) from Escherichia coli. A novel enzyme of the phosphoenolpyruvate-dependent phosphotransferase system exhibiting strict specificity for its phosphoryl acceptor, NPr. J Biol Chem 1999; 274:26185–26191 [View Article] [PubMed]
    [Google Scholar]
  93. Karstens K, Zschiedrich CP, Bowien B, Stülke J, Görke B. Phosphotransferase protein EIIANtr interacts with SpoT, a key enzyme of the stringent response, in Ralstonia eutropha H16. Microbiology (Reading) 2014; 160:711–722 [View Article] [PubMed]
    [Google Scholar]
  94. Mörk-Mörkenstein M, Heermann R, Göpel Y, Jung K, Görke B. Non-canonical activation of histidine kinase KdpD by phosphotransferase protein PtsN through interaction with the transmitter domain. Mol Microbiol 2017; 106:54–73 [View Article] [PubMed]
    [Google Scholar]
  95. Rajagopala SV, Sikorski P, Kumar A, Mosca R, Vlasblom J et al. The binary protein-protein interaction landscape of Escherichia coli. Nat Biotechnol 2014; 32:285–290 [View Article] [PubMed]
    [Google Scholar]
  96. Hu P, Janga SC, Babu M, Díaz-Mejía JJ, Butland G et al. Global functional atlas of Escherichia coli encompassing previously uncharacterized proteins. PLoS Biol 2009; 7:e96 [View Article] [PubMed]
    [Google Scholar]
  97. Alonso-López D, Campos-Laborie FJ, Gutiérrez MA, Lambourne L, Calderwood MA et al. APID database: redefining protein-protein interaction experimental evidences and binary interactomes. Database (Oxford) 2019; 2019: [View Article] [PubMed]
    [Google Scholar]
  98. Arifuzzaman M, Maeda M, Itoh A, Nishikata K, Takita C et al. Large-scale identification of protein-protein interaction of Escherichia coli K-12. Genome Res 2006; 16:686–691 [View Article] [PubMed]
    [Google Scholar]
  99. Wang L, Yan J, Wise MJ, Liu Q, Asenso J et al. Distribution patterns of polyphosphate metabolism pathway and its relationships with bacterial durability and virulence. Front Microbiol 2018; 9:782 [View Article] [PubMed]
    [Google Scholar]
  100. Achbergerová L, Nahálka J. Polyphosphate--an ancient energy source and active metabolic regulator. Microb Cell Fact 2011; 10:63 [View Article] [PubMed]
    [Google Scholar]
  101. Gottesman S. Trouble is coming: signaling pathways that regulate general stress responses in bacteria. J Biol Chem 2019; 294:11685–11700 [View Article]
    [Google Scholar]
  102. Schellhorn HE. Function, evolution, and composition of the RpoS regulon in Escherichia coli. Front Microbiol 2020; 11:560099 [View Article]
    [Google Scholar]
  103. Saha S, Lach SR, Konovalova A. Homeostasis of the Gram-negative cell envelope. Curr Opin Microbiol 2021; 61:99–106 [View Article]
    [Google Scholar]
  104. Rao NN, Liu S, Kornberg A. Inorganic polyphosphate in Escherichia coli: the phosphate regulon and the stringent response. J Bacteriol 1998; 180:2186–2193 [View Article]
    [Google Scholar]
  105. 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]
  106. Hayden JD, Ades SE. The extracytoplasmic stress factor, sigmae, is required to maintain cell envelope integrity in Escherichia coli. PloS one 2008; 3:e1573 [View Article]
    [Google Scholar]
  107. 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]
    [Google Scholar]
  108. Lüttmann D, Heermann R, Zimmer B, Hillmann A, Rampp IS et al. Stimulation of the potassium sensor KdpD kinase activity by interaction with the phosphotransferase protein IIA(Ntr) in Escherichia coli. Mol Microbiol 2009; 72:978–994 [View Article]
    [Google Scholar]
  109. Lee CR, Cho SH, Kim HJ, Kim M, Peterkofsky A et al. Potassium mediates Escherichia coli enzyme IIA(Ntr) -dependent regulation of sigma factor selectivity. Mol Microbiol 2010; 78:1468–1483 [View Article]
    [Google Scholar]
  110. Lee CR, Cho SH, Yoon MJ, Peterkofsky A, Seok YJ. Escherichia coli enzyme IIANtr regulates the K+ transporter trka. Proc Natl Acad Sci USA 2007; 104:4124–4129 [View Article]
    [Google Scholar]
  111. Grillo-Puertas M, Rintoul MR, Rapisarda VA. PhoB activation in non-limiting phosphate condition by the maintenance of high polyphosphate levels in the stationary phase inhibits biofilm formation in Escherichia coli. Microbiology (Reading) 2016; 162:1000–1008 [View Article] [PubMed]
    [Google Scholar]
  112. Hirota R, Motomura K, Nakai S, Handa T, Ikeda T et al. Stable polyphosphate accumulation by a pseudo-revertant of an Escherichia coli phoU mutant. Biotechnol Lett 2013; 35:695–701 [View Article] [PubMed]
    [Google Scholar]
  113. Gravina F, Degaut FL, Gerhardt ECM, Pedrosa FO, Souza EM et al. The protein-protein interaction network of the Escherichia coli EIIANtr regulatory protein reveals a role in cell motility and metabolic control. Res Microbiol 2021; 172:103882 [View Article] [PubMed]
    [Google Scholar]
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