Integration of antagonistic signals in the regulation of nitrogen assimilation in Escherichia coli.

Publisher Summary To maintain balanced metabolism, Escherichia coli must coordinate the assimilation of nitrogen with the assimilation of carbon and other essential nutrients. This coordination is accomplished in part by a signal transduction system that measures the signals of carbon and nitrogen status and regulates the activity of glutamine synthetase (GS) and the transcription of nitrogen-regulated (Ntr) genes, whose products facilitate the use of poor nitrogen sources. The key sensory components of this signal transduction system are the uridylyltransferase/ uridylyl-removing enzyme (UTase/UR), PII protein, and adenylyltransferase (ATase) that regulates GS by reversible adenylylation. This chapter discusses the current state of understanding of these signal-transducing proteins and the mechanisms by which they detect and transduce the signals of nitrogen and carbon status. It also discusses the physiology of the response to nitrogen and carbon availability and presents an overview of the signal transduction system.

[1]  S. Kustu,et al.  Mutations that alter the covalent modification of glutamine synthetase in Salmonella typhimurium , 1978, Journal of bacteriology.

[2]  Ann M Stock,et al.  Two-component signal transduction. , 2000, Annual review of biochemistry.

[3]  R. Conaway,et al.  Transcription : mechanisms and regulation , 1994 .

[4]  J. Gralla,et al.  Probing the Escherichia coli glnALG upstream activation mechanism in vivo. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[5]  S. Kustu,et al.  Salmonella typhimurium apparently perceives external nitrogen limitation as internal glutamine limitation. , 1996, Journal of molecular biology.

[6]  J. Hoch,et al.  A phosphotransferase activity of the Bacillus subtilis sporulation protein Spo0F that employs phosphoramidate substrates. , 1996, Biochemistry.

[7]  A. Wedel,et al.  Oligomerization of NTRC at the glnA enhancer is required for transcriptional activation. , 1993, Genes & development.

[8]  D. Szeto,et al.  Function of a bacterial activator protein that binds to transcriptional enhancers. , 1989, Science.

[9]  A. Ninfa,et al.  Effect of mutations in Escherichia coli glnL (ntrB), encoding nitrogen regulator II (NRII or NtrB), on the phosphatase activity involved in bacterial nitrogen regulation. , 1994, The Journal of biological chemistry.

[10]  T. Silhavy,et al.  Mutations That Alter the Kinase and Phosphatase Activities of the Two-Component Sensor EnvZ , 1998, Journal of bacteriology.

[11]  E. Stadtman Discovery of glutamine synthetase cascade. , 1990, Methods in enzymology.

[12]  W. Gu,et al.  Role of nitrogen regulator I (NtrC), the transcriptional activator of glnA in enteric bacteria, in reducing expression of glnA during nitrogen-limited growth , 1992, Journal of bacteriology.

[13]  A. Ninfa,et al.  The regulation of Escherichia coli glutamine synthetase revisited: role of 2-ketoglutarate in the regulation of glutamine synthetase adenylylation state. , 1998, Biochemistry.

[14]  S. Rhee,et al.  Cascade control of Escherichia coli glutamine synthetase. Purification and properties of PII uridylyltransferase and uridylyl-removing enzyme. , 1983, The Journal of biological chemistry.

[15]  B. Magasanik,et al.  Transcription of glnA by purified Escherichia coli components: core RNA polymerase and the products of glnF, glnG, and glnL. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[16]  A. Ninfa,et al.  Activation of transcription initiation from the nac promoter of Klebsiella aerogenes , 1995, Journal of bacteriology.

[17]  P. B. Chock,et al.  Interconvertible enzyme cascades in cellular regulation. , 1980, Annual review of biochemistry.

[18]  B. Magasanik,et al.  Regulation of the synthesis of glutamine synthetase by the PII protein in Klebsiella aerogenes. , 1980, Proceedings of the National Academy of Sciences of the United States of America.

[19]  P D Carr,et al.  X-ray structure of the signal transduction protein from Escherichia coli at 1.9 A. , 1996, Acta crystallographica. Section D, Biological crystallography.

[20]  A. Ninfa,et al.  Characterization of Escherichia coli glnL mutations affecting nitrogen regulation , 1992, Journal of bacteriology.

[21]  E. Stadtman,et al.  Regulation of glutamine synthetase. VII. Adenylyl glutamine synthetase: a new form of the enzyme with altered regulatory and kinetic properties. , 1967, Proceedings of the National Academy of Sciences of the United States of America.

[22]  I. H. Segel Enzyme Kinetics: Behavior and Analysis of Rapid Equilibrium and Steady-State Enzyme Systems , 1975 .

[23]  B. Magasanik,et al.  Activation of the dephosphorylation of nitrogen regulator I-phosphate of Escherichia coli , 1995, Journal of bacteriology.

[24]  F. Neidhardt,et al.  Escherichia Coli and Salmonella: Typhimurium Cellular and Molecular Biology , 1987 .

[25]  Autophosphorylation and phosphatase activities of the oxygen-sensing protein FixL of Rhizobium meliloti are coordinately regulated by oxygen. , 1993, The Journal of biological chemistry.

[26]  Probing interactions of the homotrimeric PII signal transduction protein with its receptors by use of PII heterotrimers formed in vitro from wild-type and mutant subunits , 1997, Journal of bacteriology.

[27]  A. Ninfa,et al.  Mutational analysis of the bacterial signal-transducing protein kinase/phosphatase nitrogen regulator II (NRII or NtrB) , 1993, Journal of bacteriology.

[28]  Chris Sander,et al.  DNA polymerase β belongs to an ancient nucleotidyltransferase superfamily , 1995 .

[29]  A. Ninfa,et al.  Covalent modification of the glnG product, NRI, by the glnL product, NRII, regulates the transcription of the glnALG operon in Escherichia coli. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[30]  B. Magasanik,et al.  Transcription of glnA in E. coli is stimulated by activator bound to sites far from the promoter , 1986, Cell.

[31]  R. Bender,et al.  The product of the Klebsiella aerogenes nac (nitrogen assimilation control) gene is sufficient for activation of the hut operons and repression of the gdh operon , 1993, Journal of bacteriology.

[32]  B. Magasanik,et al.  Gene order of the histidine utilization (hut) operons in Klebsiella aerogenes , 1975, Journal of bacteriology.

[33]  A. Ninfa,et al.  Initiation of transcription at the bacterial glnAp2 promoter by purified E. coli components is facilitated by enhancers , 1987, Cell.

[34]  A. Ninfa,et al.  Enzymological characterization of the signal-transducing uridylyltransferase/uridylyl-removing enzyme (EC 2.7.7.59) of Escherichia coli and its interaction with the PII protein. , 1998, Biochemistry.

[35]  E. Stadtman,et al.  Regulation of Escherichia coli glutamine synthetase. , 1989, Advances in enzymology and related areas of molecular biology.

[36]  A. Ninfa,et al.  Role of phosphorylated metabolic intermediates in the regulation of glutamine synthetase synthesis in Escherichia coli , 1992, Journal of bacteriology.

[37]  Daniel Kahn,et al.  An alternative PII protein in the regulation of glutamine synthetase in Escherichia coli , 1996, Molecular microbiology.

[38]  K. Forchhammer,et al.  Phosphorylation of the PII protein (glnB gene product) in the cyanobacterium Synechococcus sp. strain PCC 7942: analysis of in vitro kinase activity , 1995, Journal of bacteriology.

[39]  H. Westerhoff,et al.  The genes of the glutamine synthetase adenylylation cascade are not regulated by nitrogen in Escherichia coli , 1993, Molecular microbiology.

[40]  S. Francis,et al.  Cascade control of E. coli glutamine synthetase. II. Metabolite regulation of the enzymes in the cascade. , 1978, Archives of biochemistry and biophysics.

[41]  Robert B. Bourret,et al.  Histidine phosphorylation and phosphoryl group transfer in bacterial chemotaxis , 1988, Nature.

[42]  B. Magasanik,et al.  Complex glnA-glnL-glnG operon of Escherichia coli , 1982, Journal of bacteriology.

[43]  A. Ninfa,et al.  The Escherichia coli PII Signal Transduction Protein Is Activated upon Binding 2-Ketoglutarate and ATP (*) , 1995, The Journal of Biological Chemistry.

[44]  J. Stock,et al.  Phosphorylation of bacterial response regulator proteins by low molecular weight phospho-donors. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[45]  S. Kustu,et al.  In vitro transcription of the nitrogen fixation regulatory operon nifLA of Klebsiella pneumoniae , 1987, Journal of bacteriology.

[46]  P. Senior,et al.  Regulation of nitrogen metabolism in Escherichia coli and Klebsiella aerogenes: studies with the continuous-culture technique , 1975, Journal of Bacteriology.

[47]  V. Weiss,et al.  Phosphorylation of nitrogen regulator I (NRI) of Escherichia coli. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[48]  H V Westerhoff,et al.  The two opposing activities of adenylyl transferase reside in distinct homologous domains, with intramolecular signal transduction , 1997, The EMBO journal.

[49]  D. Koshland,et al.  Phosphorylation site of NtrC, a protein phosphatase whose covalent intermediate activates transcription , 1992, Journal of bacteriology.

[50]  B. Magasanik,et al.  Expression of glnA in Escherichia coli is regulated at tandem promoters. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[51]  The glnB region of the Escherichia coli chromosome , 1993, Journal of bacteriology.

[52]  A. Ninfa,et al.  Is acetyl phosphate a global signal in Escherichia coli? , 1993, Journal of bacteriology.

[53]  Repression of the Klebsiella aerogenes nac promoter , 1995, Journal of bacteriology.

[54]  B. Magasanik,et al.  Role of glnB and glnD gene products in regulation of the glnALG operon of Escherichia coli , 1985, Journal of bacteriology.

[55]  S. Kustu,et al.  Protein kinase and phosphoprotein phosphatase activities of nitrogen regulatory proteins NTRB and NTRC of enteric bacteria: roles of the conserved amino-terminal domain of NTRC. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[56]  L. Pedersen,et al.  Structural investigation of the antibiotic and ATP-binding sites in kanamycin nucleotidyltransferase. , 1995, Biochemistry.

[57]  D. Court,et al.  Cloning and organization of the abc and mdl genes of Escherichia coli: relationship to eukaryotic multidrug resistance. , 1993, Gene.

[58]  A J Ninfa,et al.  Reconstitution of the signal-transduction bicyclic cascade responsible for the regulation of Ntr gene transcription in Escherichia coli. , 1998, Biochemistry.

[59]  A. Ninfa,et al.  Mutations in the glnG gene of Escherichia coli that result in increased activity of nitrogen regulator I , 1989, Journal of bacteriology.

[60]  Samuel H. Wilson,et al.  Structures of ternary complexes of rat DNA polymerase beta, a DNA template-primer, and ddCTP. , 1994, Science.

[61]  A. Zelenetz,et al.  gltB gene and regulation of nitrogen metabolism by glutamine synthetase in Escherichia coli , 1978, Journal of bacteriology.

[62]  A. Ninfa,et al.  Structure/function analysis of the PII signal transduction protein of Escherichia coli: genetic separation of interactions with protein receptors , 1997, Journal of bacteriology.

[63]  S. Kustu,et al.  Constitutive forms of the enhancer-binding protein NtrC: evidence that essential oligomerization determinants lie in the central activation domain. , 1995, Journal of molecular biology.

[64]  J. Hirschman,et al.  Products of nitrogen regulatory genes ntrA and ntrC of enteric bacteria activate glnA transcription in vitro: evidence that the ntrA product is a sigma factor. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[65]  L. M. Albright,et al.  Rhizobium meliloti ntrA (rpoN) gene is required for diverse metabolic functions , 1987, Journal of bacteriology.

[66]  A. Ninfa,et al.  Mechanism of autophosphorylation of Escherichia coli nitrogen regulator II (NRII or NtrB): trans-phosphorylation between subunits , 1993, Journal of bacteriology.

[67]  S. Kustu,et al.  The phosphorylated form of the enhancer-binding protein NTRC has an ATPase activity that is essential for activation of transcription , 1991, Cell.

[68]  P. B. Chock,et al.  Allosteric regulation of monocyclic interconvertible enzyme cascade systems: use of Escherichia coli glutamine synthetase as an experimental model. , 1978, Proceedings of the National Academy of Sciences of the United States of America.

[69]  E. Stadtman,et al.  [29] Glutamine synthetase from Escherichia coli , 1985 .

[70]  B. Magasanik,et al.  Physical and genetic characterization of the glnA--glnG region of the Escherichia coli chromosome. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[71]  A. Ninfa,et al.  Reversible uridylylation of the Escherichia coli PII signal transduction protein regulates its ability to stimulate the dephosphorylation of the transcription factor nitrogen regulator I (NRI or NtrC). , 1994, The Journal of biological chemistry.

[72]  A. Ninfa,et al.  Identification of the site of autophosphorylation of the bacterial protein kinase/phosphatase NRII. , 1991, The Journal of biological chemistry.

[73]  S. Hoving,et al.  An additional PII in Escherichia coli: a new regulatory protein in the glutamine synthetase cascade. , 1995, FEMS microbiology letters.

[74]  B. Magasanik Genetic control of nitrogen assimilation in bacteria. , 1982, Annual Review of Genetics.

[75]  A. Ninfa,et al.  Role of the GlnK signal transduction protein in the regulation of nitrogen assimilation in Escherichia coli , 1998, Molecular microbiology.

[76]  A. Wolfe,et al.  Regulation of acetyl phosphate synthesis and degradation, and the control of flagellar expression in Escherichia coli , 1994, Molecular microbiology.