Nitrogen and carbon status are integrated at the transcriptional level by the nitrogen regulator NtrC in vivo

mBio

Volumn 4, Issue 6, 2013, Pages

  Schumacher, Jörg ^a   Behrends, Volker ^a   Pan, Zhensheng ^a   Brown, Dan R ^a   Heydenreich, Franziska ^a   Lewis, Matthew R ^a   Bennett, Mark H ^a   Razzaghi, Banafsheh ^a   Komorowski, Michal ^b   Barahona, Mauricio ^a   Stumpf, Michael P H ^a   Wigneshweraraj, Sivaramesh ^a   Bundy, Jacob G ^a   Buck, Martin ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b INSTITUTE OF FUNDAMENTAL TECHNOLOGICAL RESEARCH   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

2 OXOGLUTARIC ACID; CARBON; GLUTAMINE; NITROGEN; NITROGEN REGULATORY PROTEIN; PROTEIN NTRC; STIMULATORY GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG; AMMONIUM DERIVATIVE; ESCHERICHIA COLI PROTEIN; GLNG PROTEIN, E COLI; TRANSCRIPTION FACTOR;

ARTICLE; CONTROLLED STUDY; GENE; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GLNA GENE; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; TRANSCRIPTION REGULATION; ESCHERICHIA COLI; GENETICS; METABOLISM;

AMMONIUM COMPOUNDS; CARBON; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; GLUTAMINE; NITROGEN; PII NITROGEN REGULATORY PROTEINS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84891587558     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.00881-13     Document Type: Article

References (60)

1. Reitzer L. 2003. Nitrogen assimilation and global regulation in Escherichia coli. Annu. Rev. Microbiol. 57:155-176.
2. Yan D. 2007. Protection of the glutamate pool concentration in enteric bacteria. Proc. Natl. Acad. Sci. U. S. A. 104:9475-9480.
3. Helling RB. 1994. Why does Escherichia coli have two primary pathways for synthesis of glutamate? J. Bacteriol. 176:4664-4668.
4. Brown MS, Segal A, Stadtman ER. 1971. Modulation of glutamine synthetase adenylylation and deadenylylation is mediated by metabolic transformation of the P II -regulatory protein. Proc. Natl. Acad. Sci. U. S. A. 68:2949-2953.
5. Okano H, Hwa T, Lenz P, Yan D. 2010. Reversible adenylylation of glutamine synthetase is dynamically counterbalanced during steady-state growth of Escherichia coli. J. Mol. Biol. 404:522-536.
6. Jiang P, Ninfa AJ. 1999. Regulation of autophosphorylation of Escherichia coli nitrogen regulator II by the PII signal transduction protein. J. Bacteriol. 181:1906-1911.
7. Jiang P, Ninfa AJ. 2009. Alpha-ketoglutarate controls the ability of the Escherichia coli PII signal transduction protein to regulate the activities of NRII (NrB) but does not control the binding of PII to NRII. Biochemistry 48:11514-11521.
8. Zimmer DP, Soupene E, Lee HL, Wendisch VF, Khodursky AB, Peter BJ, Bender RA, Kustu S. 2000. Nitrogen regulatory protein C-controlled genes of Escherichia coli: scavenging as a defense against nitrogen limitation. Proc. Natl. Acad. Sci. U. S. A. 97:14674-14679.
9. Rombel I, North A, Hwang I, Wyman C, Kustu S. 1998. The bacterial enhancer-binding protein NtrC as a molecular machine. Cold Spring Harb. Symp. Quant. Biol. 63:157-166.
10. Schumacher J, Zhang X, Jones S, Bordes P, Buck M. 2004. ATPdependent transcriptional activation by bacterial PspF AAA protein. J. Mol. Biol. 338:863-875.
11. Rappas M, Schumacher J, Niwa H, Buck M, Zhang X. 2006. Structural basis of the nucleotide driven conformational changes in the AAA domain of transcription activator PspF. J. Mol. Biol. 357:481-492.
12. Wigneshweraraj S, Bose D, Burrows PC, Joly N, Schumacher J, Rappas M, Pape T, Zhang X, Stockley P, Severinov K, Buck M. 2008. Modus operandi of the bacterial RNA polymerase containing the sigma54 promoter-specificity factor. Mol. Microbiol. 68:538-546.
13. Ninfa AJ, Magasanik B. 1986. Covalent modification of the glnG product, NRI, by the glnL product, NRII, regulates the transcription of the glnALG operon in Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 83:5909-5913.
14. Mao XJ, Huo YX, Buck M, Kolb A, Wang YP. 2007. Interplay between CRP-cAMP and PII-Ntr systems forms novel regulatory network between carbon metabolism and nitrogen assimilation in Escherichia coli. Nucleic Acids Res. 35:1432-1440.
15. Atkinson MR, Ninfa AJ. 1998. Role of the GlnK signal transduction protein in the regulation of nitrogen assimilation in Escherichia coli. Mol. Microbiol. 29:431-447.
16. Atkinson MR, Pattaramanon N, Ninfa AJ. 2002. Governor of the glnAp2 promoter of Escherichia coli. Mol. Microbiol. 46:1247-1257.
17. van Heeswijk WC, Molenaar D, Hoving S, Westerhoff HV. 2009. The pivotal regulator GlnB of Escherichia coli is engaged in subtle and contextdependent control. FEBS J. 276:3324-3340.
18. Shiau SP, Schneider BL, Gu W, Reitzer LJ. 1992. Role of nitrogen regulator I (NtrC), the transcriptional activator of glnA in enteric bacteria, in reducing expression of glnA during nitrogen-limited growth. J. Bacteriol. 174:179-185.
19. Sasse-Dwight S, Gralla JD. 1988. Probing the Escherichia coli glnALG upstream activation mechanism in vivo. Proc. Natl. Acad. Sci. U. S. A. 85:8934-8938.
20. Bender RA, Magasanik B. 1977. Regulatory mutations in the Klebsiella aerogenes structural gene for glutamine synthetase. J. Bacteriol. 132: 100-105.
21. Willis RC, Iwata KK, Furlong CE. 1975. Regulation of glutamine transport in Escherichia coli. J. Bacteriol. 122:1032-1037.
22. Ikeda TP, Shauger AE, Kustu S. 1996. Salmonella typhimurium apparently perceives external nitrogen limitation as internal glutamine limitation. J. Mol. Biol. 259:589-607.
23. Soupene E, van Heeswijk WC, Plumbridge J, Stewart V, Bertenthal D, Lee H, Prasad G, Paliy O, Charernnoppakul P, Kustu S. 2003. Physiological studies of Escherichia coli strain MG1655: growth defects and apparent cross-regulation of gene expression. J. Bacteriol. 185:5611-5626.
24. Bennett BD, Kimball EH, Gao M, Osterhout R, Van Dien SJ, Rabinowitz JD. 2009. Absolute metabolite concentrations and implied enzyme active site occupancy in Escherichia coli. Nat. Chem. Biol. 5:593-599.
25. Rothstein DM, Pahel G, Tyler B, Magasanik B. 1980. Regulation of expression from the glnA promoter of Escherichia coli in the absence of glutamine synthetase. Proc. Natl. Acad. Sci. U. S. A. 77:7372-7376.
26. Thakur CS, Brown ME, Sama JN, Jackson ME, Dayie TK. 2010. Growth of wildtype and mutant E. coli strains in minimal media for optimal production of nucleic acids for preparing labeled nucleotides. Appl. Microbiol. Biotechnol. 88:771-779.
27. Kashket ER, Brodie AF. 1962. Effects of near-ultraviolet irradiation on growth and oxidative metabolism of bacteria. J. Bacteriol. 83:1094-1100.
28. Vijayendran C, Polen T, Wendisch VF, Friehs K, Niehaus K, Flaschel E. 2007. The plasticity of global proteome and genome expression analyzed in closely related W3110 and MG1655 strains of a well-studied model organism, Escherichia coli-K12. J. Biotechnol. 128:747-761.
29. Maharjan RP, Ferenci T. 2005. Metabolomic diversity in the species Escherichia coli and its relationship to genetic population structure. Metabolomics 1:235-242.
30. Kim M, Zhang Z, Okano H, Yan D, Groisman A, Hwa T. 2012. Need-based activation of ammonium uptake in Escherichia coli. Mol. Syst. Biol. 8:616.
31. Reitzer LJ, Magasanik B. 1986. Transcription of glnA in E. coli is stimulated by activator bound to sites far from the promoter. Cell 45:785-792.
32. Pahel G, Rothstein DM, Magasanik B. 1982. Complex glnA-glnL-glnG operon of Escherichia coli. J. Bacteriol. 150:202-213.
33. Volkman BF, Lipson D, Wemmer DE, Kern D. 2001. Two-state allosteric behavior in a single-domain signaling protein. Science 291:2429-2433.
34. Picotti P, Aebersold R. 2012. Selected reaction monitoring-based proteomics: workflows, potential, pitfalls and future directions. Nat. Methods 9:555-566.
35. Elschenbroich S, Kislinger T. 2011. Targeted proteomics by selected reaction monitoring mass spectrometry: applications to systems biology and biomarker discovery. Mol. Biosyst. 7:292-303.
36. Ishihama Y, Schmidt T, Rappsilber J, Mann M, Hartl FU, Kerner MJ, Frishman D. 2008. Protein abundance profiling of the Escherichia coli cytosol. BMC Genomics 9:102.
37. Lu P, Vogel C, Wang R, Yao X, Marcotte EM. 2007. Absolute protein expression profiling estimates the relative contributions of transcriptional and translational regulation. Nat. Biotechnol. 25:117-124.
38. Kubitschek HE, Friske JA. 1986. Determination of bacterial cell volume with the Coulter counter. J. Bacteriol. 168:1466-1467.
39. Kamberov ES, Atkinson MR, Chandran P, Ninfa AJ. 1994. Effect of mutations in Escherichia coli glnL (ntrB), encoding nitrogen regulator II (NRII or NtrB), on the phosphatase activity involved in bacterial nitrogen regulation. J. Biol. Chem. 269:28294-28299.
40. Yan D, Kustu S. 1999. "Switch I" mutant forms of the bacterial enhancerbinding protein NtrC that perturb the response to DNA. Proc. Natl. Acad. Sci. U. S. A. 96:13142-13146.
41. De Carlo S, Chen B, Hoover TR, Kondrashkina E, Nogales E, Nixon BT. 2006. The structural basis for regulated assembly and function of the transcriptional activator NtrC. Genes Dev. 20:1485-1495.
42. Atkinson MR, Blauwkamp TA, Bondarenko V, Studitsky V, Ninfa AJ. 2002. Activation of the glnA, glnK, and nac promoters as Escherichia coli undergoes the transition from nitrogen excess growth to nitrogen starvation. J. Bacteriol. 184:5358-5363.
43. Magasanik B. 1989. Regulation of transcription of the glnALG operon of Escherichia coli by protein phosphorylation. Biochimie 71:1005-1012.
44. Neidhardt FC, Curtiss R, III, Ingraham JL, Lin EC, Low KB, Magasanik B, Reznikoff WS, Riley M, Schaechter M, Umbarger HE. 1996. Escherichia coli and Salmonella: cellular and molecular biology, 2nd ed. ASM Press, Washington, DC.
45. Witmer MR, Palmieri-Young D, Villafranca JJ. 1994. Probing the catalytic roles of n2-site glutamate residues in Escherichia coli glutamine synthetase by mutagenesis. Protein Sci. 3:1746-1759.
46. Sharkey MA, Oliveira TF, Engel PC, Khan AR. 2013. Structure of NADP-dependent glutamate dehydrogenase from Escherichia coli: reflections on the basis of coenzyme specificity in the family of glutamate dehydrogenases. FEBS J. 280(18):4681-4692. doi:10.1111/febs.12439.
47. You C, Okano H, Hui S, Zhang Z, Kim M, Gunderson CW, Wang YP, Lenz P, Yan D, Hwa T. 2013. Coordination of bacterial proteome with metabolism by cyclic AMP signalling. Nature 500:301-306.
48. Buck M, Bose D, Burrows P, Cannon W, Joly N, Pape T, Rappas M, Schumacher J, Wigneshweraraj S, Zhang X. 2006. A second paradigm for gene activation in bacteria. Biochem. Soc. Trans. 34:1067-1071.
49. Goss TJ, Perez-Matos A, Bender RA. 2001. Roles of glutamate synthase, gltBD, and gltF in nitrogen metabolism of Escherichia coli and Klebsiella aerogenes. J. Bacteriol. 183:6607-6619.
50. Miller JH. 1992. A short course in bacterial genetics: a laboratory manual and handbook for Escherichia coli and related bacteria. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
51. Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, Baba M, Datsenko KA, Tomita M, Wanner BL, Mori H. 2006. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol. Syst. Biol. 2:.00082006.
52. Atlas RM. 2010. Handbook of microbiological media, vol 1. CRC Press, Boca Raton, FL.
53. Bender RA, Macaluso A, Magasanik B. 1976. Glutamate dehydrogenase: genetic mapping and isolation of regulatory mutants of Klebsiella aerogenes. J. Bacteriol. 127:141-148.
54. Bolten CJ, Kiefer P, Letisse F, Portais JC, Wittmann C. 2007. Sampling for metabolome analysis of microorganisms. Anal. Chem. 79:3843-3849.
55. Behrends V, Williams KJ, Jenkins VA, Robertson BD, Bundy JG. 2012. Free glucosylglycerate is a novel marker of nitrogen stress in Mycobacterium smegmatis. J. Proteome Res. 11:3888-3896.
56. Beckonert O, Keun HC, Ebbels TM, Bundy J, Holmes E, Lindon JC, Nicholson JK. 2007. Metabolic profiling, metabolomic and metabonomic procedures for NMR spectroscopy of urine, plasma, serum and tissue extracts. Nat. Protoc. 2:2692-2703.
57. Behrends V, Ebbels TM, Williams HD, Bundy JG. 2009. Time-resolved metabolic footprinting for nonlinear modeling of bacterial substrate utilization. Appl. Environ. Microbiol. 75:2453-2463.
58. Ulrich EL, Akutsu H, Doreleijers JF, Harano Y, Ioannidis YE, Lin J, Livny M, Mading S, Maziuk D, Miller Z, Nakatani E, Schulte CF, Tolmie DE, Kent Wenger R, Yao H, Markley JL. 2008. BioMagResBank. Nucleic Acids Res. 36:D402-D408.
59. Spagou K, Wilson ID, Masson P, Theodoridis G, Raikos N, Coen M, Holmes E, Lindon JC, Plumb RS, Nicholson JK, Want EJ. 2011. HILIC-UPLC-MS for exploratory urinary metabolic profiling in toxicological studies. Anal. Chem. 83:382-390.
60. Behrends V, Tredwell GD, Bundy JG. 2011. A software complement to AMDIS for processing GC-MS metabolomic data. Anal. Biochem. 415: 206-208.