1887

Abstract

The AmtB protein transports uncharged NH into the cell, but it also interacts with the nitrogen regulatory protein P, which in turn regulates a variety of proteins involved in nitrogen fixation and utilization. Three P homologues, GlnB, GlnK and GlnJ, have been identified in the photosynthetic bacterium , and they have roles in at least four overlapping and distinct functions, one of which is the post-translational regulation of nitrogenase activity. In , nitrogenase activity is tightly regulated in response to addition or energy depletion (shift to darkness), and this regulation is catalysed by the post-translational regulatory system encoded by . Two homologues, and , have been identified in , and they are linked with and , respectively. Mutants lacking AmtB are defective in their response to both addition and darkness, while mutants lacking AmtB show little effect on the regulation of nitrogenase activity. These responses to darkness and appear to involve different signal transduction pathways, and the poor response to darkness does not seem to be an indirect result of perturbation of internal pools of nitrogen. It is also shown that AmtB is necessary to sequester detectable amounts GlnJ to the cell membrane. These results suggest that some element of the AmtB-P regulatory system senses energy deprivation and a consistent model for the integration of nitrogen, carbon and energy signals by P is proposed. Other results demonstrate a degree of specificity in interaction of AmtB with the different P homologues in . Such interaction specificity might be important in explaining the way in which P proteins regulate processes involved in nitrogen acquisition and utilization.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.28903-0
2006-07-01
2024-04-18
Loading full text...

Full text loading...

/deliver/fulltext/micro/152/7/2075.html?itemId=/content/journal/micro/10.1099/mic.0.28903-0&mimeType=html&fmt=ahah

References

  1. Andrade S. L, Dickmanns A, Ficner R, Einsle O. 2005; Crystal structure of the archaeal ammonium transporter Amt-1 from Archaeoglobus fulgidus . Proc Natl Acad Sci U S A 102:14994–14999 [CrossRef]
    [Google Scholar]
  2. Arcondéguy T, Lawson D, Merrick M. 2000; Two residues in the T-loop of GlnK determine NifL-dependent nitrogen control of nif gene expression. J Biol Chem 275:38452–38456 [CrossRef]
    [Google Scholar]
  3. Arcondéguy T, Jack R, Merrick M. 2001; PII signal transduction proteins, pivotal players in microbial nitrogen control. Microbiol Mol Biol Rev 65:80–105 [CrossRef]
    [Google Scholar]
  4. Atkinson M. R, Ninfa A. J. 1998; Role of the GlnK signal transduction protein in the regulation of nitrogen assimilation in Escherichia coli . Mol Microbiol 29:431–447 [CrossRef]
    [Google Scholar]
  5. Atkinson M. R, Ninfa A. J. 1999; Characterization of the GlnK protein of Escherichia coli . Mol Microbiol 32:301–313 [CrossRef]
    [Google Scholar]
  6. Atkinson M. R, Blauwkamp T. A, Ninfa A. J. 2002; Context-dependent functions of the PII and GlnK signal transduction proteins in Escherichia coli . J Bacteriol 184:5364–5375 [CrossRef]
    [Google Scholar]
  7. Bender R. A, Janssen K. A, Resnick A. D, Blumenberg M, Foor F, Magasanik B. 1977; Biochemical parameters of glutamine synthetase from Klebsiella aerogenes . J Bacteriol 129:1001–1009
    [Google Scholar]
  8. Blakey D, Leech A, Thomas G. H, Coutts G, Findlay K, Merrick M. 2002; Purification of the Escherichia coli ammonium transporter AmtB reveals a trimeric stoichiometry. Biochem J 364:527–535 [CrossRef]
    [Google Scholar]
  9. Blauwkamp T. A, Ninfa A. J. 2002; Physiological role of the GlnK signal transduction protein of Escherichia coli : survival of nitrogen starvation. Mol Microbiol 46:203–214 [CrossRef]
    [Google Scholar]
  10. Blauwkamp T. A, Ninfa A. J. 2003; Antagonism of PII signalling by the AmtB protein of Escherichia coli . Mol Microbiol 48:1017–1028 [CrossRef]
    [Google Scholar]
  11. Coutts G, Thomas G, Blakey D, Merrick M. 2002; Membrane sequestration of the signal transduction protein GlnK by the ammonium transporter AmtB. EMBO J 21:536–545 [CrossRef]
    [Google Scholar]
  12. Detsch C, Stülke J. 2003; Ammonium utilization in Bacillus subtilis : transport and regulatory functions of NrgA and NrgB. Microbiology 149:3289–3297 [CrossRef]
    [Google Scholar]
  13. Ditta G, Schmidhauser T, Yakobson E, Lu P, Liang X.-W, Finlay D. R, Guiney D, Helinski D. R. 1985; Plasmids related to the broad host range vector, pRK290, useful for gene cloning and for monitoring gene expression. Plasmid 13:149–153 [CrossRef]
    [Google Scholar]
  14. Drepper T, Gross S, Yakunin A. F, Hallenbeck P. C, Masepohl B, Klipp W. 2003; Role of GlnB and GlnK in ammonium control of both nitrogenase systems in the phototrophic bacterium Rhodobacter capsulatus . Microbiology 149:2203–2212 [CrossRef]
    [Google Scholar]
  15. Fitzmaurice W. P, Saari L. L, Lowery R. G, Ludden P. W, Roberts G. P. 1989; Genes coding for the reversible ADP-ribosylation system of dinitrogenase reductase from Rhodospirillum rubrum . Mol Gen Genet 218:340–347 [CrossRef]
    [Google Scholar]
  16. Forchhammer K. 2004; Global carbon/nitrogen control by P[sub]II[/sub] signal transduction in cyanobacteria: from signals to targets. FEMS Microbiol Rev 28:319–333 [CrossRef]
    [Google Scholar]
  17. Grunwald S. K, Lies D. P, Roberts G. P, Ludden P. W. 1995; Posttranslational regulation of nitrogenase in Rhodospirillum rubrum strains overexpressing the regulatory enzymes dinitrogenase reductase ADP-ribosyltransferase and dinitrogenase reductase activating glycohydrolase. J Bacteriol 177:628–635
    [Google Scholar]
  18. He L, Soupene E, Ninfa A, Kustu S. 1998; Physiological role for the GlnK protein of enteric bacteria: relief of NifL inhibition under nitrogen-limiting conditions. J Bacteriol 180:6661–6667
    [Google Scholar]
  19. Hisbergues M, Jeanjean R, Joset F, Tandeau de Marsac N, Bédu S. 1999; Protein PII regulates both inorganic carbon and nitrate uptake and is modified by a redox signal in Synechocystis PCC 6803. FEBS Lett 463:216–220 [CrossRef]
    [Google Scholar]
  20. Howitt S. M, Udvardi M. K. 2000; Structure, function and regulation of ammonium transporters in plants. Biochim Biophys Acta 1465152–170 [CrossRef]
    [Google Scholar]
  21. Huergo L. F, Souza E. M, Steffens M. B, Yates M. G, Pedrosa F. O, Chubatsu L. S. 2005; Effects of over-expression of the regulatory enzymes DraT and DraG on the ammonium-dependent post-translational regulation of nitrogenase reductase in Azospirillum brasilense . Arch Microbiol 183:209–217 [CrossRef]
    [Google Scholar]
  22. Huergo L. F, Souza E. M, Araujo M. S, Pedrosa F. O, Chubatsu L. S, Steffens M. B. R, Merrick M. 2006; ADP-ribosylation of dinitrogenase reductase in Azospirillum brasilense is regulated by AmtB-dependent membrane sequestration of DraG. Mol Microbiol 59:326–337 [CrossRef]
    [Google Scholar]
  23. Ikeda T. P, Shauger A. E, Kustu S. 1996; Salmonella typhimurium apparently perceives external nitrogen limitation as internal glutamine limitation. J Mol Biol 259:589–607 [CrossRef]
    [Google Scholar]
  24. Jack R, De Zamaroczy M, Merrick M. 1999; The signal transduction protein GlnK is required for NifL-dependent nitrogen control of nif gene expression in Klebsiella pneumoniae . J Bacteriol 181:1156–1162
    [Google Scholar]
  25. Javelle A, Severi E, Thornton J, Merrick M. 2004; Ammonium sensing in Escherichia coli . Role of the ammonium transporter AmtB and AmtB-GlnK complex formation. J Biol Chem 279:8530–8538 [CrossRef]
    [Google Scholar]
  26. Javelle A, Thomas G, Marini A. M, Kramer R, Merrick M. 2005; In vivo functional characterization of the Escherichia coli ammonium channel AmtB: evidence for metabolic coupling of AmtB to glutamine synthetase. Biochem J 390:215–222 [CrossRef]
    [Google Scholar]
  27. Jiang P, Peliska J. A, Ninfa A. J. 1998a; The regulation of Escherichia coli glutamine synthetase revisited: role of 2-ketoglutarate in the regulation of glutamine synthetase adenylylation state. Biochemistry 37:12802–12810 [CrossRef]
    [Google Scholar]
  28. Jiang P, Peliska J. A, Ninfa A. J. 1998b; 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. Biochemistry 37:12782–12794 [CrossRef]
    [Google Scholar]
  29. Johansson B. C, Gest H. 1977; Adenylylation/deadenylylation control of the glutamine synthetase of Rhodopseudomonas capsulata . Eur J Biochem 81:365–371 [CrossRef]
    [Google Scholar]
  30. Kamberov E. S, Atkinson M. R, Ninfa A. J. 1995; The Escherichia coli PII signal transduction protein is activated upon binding 2-ketoglutarate and ATP. J Biol Chem 270:17797–17807 [CrossRef]
    [Google Scholar]
  31. Kanemoto R. H, Ludden P. W. 1984; Effect of ammonia, darkness, and phenazine methosulfate on whole-cell nitrogenase activity and Fe protein modification in Rhodospirillum rubrum . J Bacteriol 158:713–720
    [Google Scholar]
  32. Kanemoto R. H, Ludden P. W. 1987; Amino acid concentrations in Rhodospirillum rubrum during expression and switch-off of nitrogenase activity. J Bacteriol 169:3035–3043
    [Google Scholar]
  33. Kennedy C, Drummond M. H. 1985; The use of cloned nif regulatory elements from Klebsiella pneumoniae to examine nif regulation in Azotobacter vinelandii . J Gen Microbiol 131:1787–1795
    [Google Scholar]
  34. Khademi S, O'Connell J., 3rd, Remis J, Robles-Colmenares Y, Miercke L. J, Stroud R. M. 2004; Mechanism of ammonia transport by Amt/MEP/Rh: structure of AmtB at 1.35 Å. Science 305:1587–1594 [CrossRef]
    [Google Scholar]
  35. Klassen G, de Souza E. M, Yates M. G, Rigo L. U, Inaba J, Pedrosa Fde O. 2001; Control of nitrogenase reactivation by the GlnZ protein in Azospirillum brasilense . J Bacteriol 183:6710–6713 [CrossRef]
    [Google Scholar]
  36. Klopprogge K, Grabbe R, Hoppert M, Schmitz R. A. 2002; Membrane association of Klebsiella pneumoniae NifL is affected by molecular oxygen and combined nitrogen. Arch Microbiol 177:223–234 [CrossRef]
    [Google Scholar]
  37. Lehman L. J, Roberts G. P. 1991; Identification of an alternative nitrogenase system in Rhodospirillum rubrum . J Bacteriol 173:5705–5711
    [Google Scholar]
  38. Li J. D, Hu C. Z, Yoch D. C. 1987; Changes in amino acid and nucleotide pools of Rhodospirillum rubrum during switch-off of nitrogenase activity initiated by NH4+ or darkness. J Bacteriol 169:231–237
    [Google Scholar]
  39. Liang J. H, Nielsen G. M, Lies D. P, Burris R. H, Roberts G. P, Ludden P. W. 1991; Mutations in the draT and draG genes of Rhodospirillum rubrum result in loss of regulation of nitrogenase by reversible ADP-ribosylation. J Bacteriol 173:6903–6909
    [Google Scholar]
  40. Lies D. P. 1994 Genetic manipulation and the overexpression analysis of posttranslational nitrogen fixation regulation in Rhodospirillum rubrum PhD thesis University of Wisconsin-Madison; Madison, WI, USA:
    [Google Scholar]
  41. Little R, Reyes-Ramirez F, Zhang Y, Dixon R, van Heeswijk W. C. 2000; Signal transduction to the Azotobacter vinelandii NIFL-NIFA regulatory system is influenced directly by interaction with 2-oxoglutarate and the PII regulatory protein. EMBO J 19:6041–6050 [CrossRef]
    [Google Scholar]
  42. Little R, Colombo V, Leech A, Dixon R. 2002; Direct interaction of the NifL regulatory protein with the GlnK signal transducer enables the Azotobacter vinelandii NifL-NifA regulatory system to respond to conditions replete for nitrogen. J Biol Chem 277:15472–15481 [CrossRef]
    [Google Scholar]
  43. Margués S, Mérida A, Candau P, Florencio F. J. 1992; Light-mediated regulation of glutamine synthetase activity in the unicellular cyanobacterium Synechocystis sp. PCC 6301. Planta 187:247–253
    [Google Scholar]
  44. Marini A. M, Urrestarazu A, Beauwens R, Andre B. 1997; The Rh (Rhesus) blood group polypeptides are related to NH4+ transporters. Trends Biochem Sci 22:460–461 [CrossRef]
    [Google Scholar]
  45. Martin D. E, Reinhold-Hurek B. 2002; Distinct roles of P[sub]II[/sub]-like signal transmitter proteins and amtB in regulation of nif gene expression, nitrogenase activity, and posttranslational modification of NifH in Azoarcus sp. strain BH72. J Bacteriol 184:2251–2259 [CrossRef]
    [Google Scholar]
  46. Meletzus D, Rudnick P, Doetsch N, Green A, Kennedy C. 1998; Characterization of the glnK-amtB operon of Azotobacter vinelandii . J Bacteriol 180:3260–3264
    [Google Scholar]
  47. Michel-Reydellet N, Desnoues N, Elmerich C, Kaminski P. A, de Zamaroczy M. 1998; Characterisation of the glnK-amtB operon and the involvement of AmtB in methylammonium uptake in Azorhizobium caulinodans . Mol Gen Genet 258:671–677 [CrossRef]
    [Google Scholar]
  48. Ninfa A. J, Atkinson M. R. 2000; PII signal transduction proteins. Trends Microbiol 8:172–179 [CrossRef]
    [Google Scholar]
  49. Ninfa A. J, Jiang P. 2005; PII signal transduction proteins: sensors of α -ketoglutarate that regulate nitrogen metabolism. Curr Opin Microbiol 8:168–173 [CrossRef]
    [Google Scholar]
  50. Ninfa A. J, Atkinson M. R, Kamberov E. S, Feng J, Ninfa E. G. 1995; Control of nitrogen assimilation by the NR[sub]I[/sub]-NR[sub]II[/sub] two-component system of enteric bacteria. In Two-Component Signal Transduction pp  147–158 Edited by Hoch J. A., Silhavy T. J. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  51. Nordlund S, Höglund L. 1986; Studies of the adenylate and pyridine nucleotide pools during nitrogenase ‘switch-off’ in Rhodospirillum rubrum . Plant Soil 90:203–209 [CrossRef]
    [Google Scholar]
  52. Nordlund S, Kanemoto R. H, Murrell S. A, Ludden P. W. 1985; Properties and regulation of glutamine synthetase from Rhodospirillum rubrum . J Bacteriol 161:13–17
    [Google Scholar]
  53. Norén A., Nordlund S. 1997; Dinitrogenase reductase-activating glycohydrolase can be released from chromatophores of Rhodospirillum rubrum by treatment with MgGDP. J Bacteriol 179:7872–7874
    [Google Scholar]
  54. Paul T. D, Ludden P. W. 1984; Adenine nucleotide levels in Rhodospirillum rubrum during switch-off of whole-cell nitrogenase activity. Biochem J 224:961–969
    [Google Scholar]
  55. Paul B. J, Ross W, Gaal T, Gourse R. L. 2004; rRNA transcription in Escherichia coli . Annu Rev Genet 38:749–770 [CrossRef]
    [Google Scholar]
  56. Pawlowski A, Riedel K. U, Klipp W, Dreiskemper P, Grob S, Bierhoff H, Drepper T, Masepohl B. 2003; Yeast two-hybrid studies on interaction of proteins involved in regulation of nitrogen fixation in the phototrophic bacterium Rhodobacter capsulatus . J Bacteriol 185:5240–5247 [CrossRef]
    [Google Scholar]
  57. Reitzer L. 2003; Nitrogen assimilation and global regulation in Escherichia coli . Annu Rev Microbiol 57:155–176 [CrossRef]
    [Google Scholar]
  58. Reyes J. C, Florencio F. J. 1995; Electron transport controls transcription of the glutamine synthetase gene (glnA) from the cyanobacterium Synechocystis sp. PCC 6803. Plant Mol Biol 27:789–799 [CrossRef]
    [Google Scholar]
  59. Reyes J. C, Crespo J. L, Garcia-Dominguez M, Florencio F. J. 1995; Electron transport controls glutamine synthetase activity in the facultative heterotrophic cyanobacterium Synechocystis sp. PCC 6803. Plant Physiol 109:899–905
    [Google Scholar]
  60. Rudnick P, Kunz C, Gunatilaka M. K, Hines E. R, Kennedy C. 2002; Role of GlnK in NifL-mediated regulation of NifA activity in Azotobacter vinelandii . J Bacteriol 184:812–820 [CrossRef]
    [Google Scholar]
  61. Saier M. H., Jr, Eng B. H, Fard S. 15 other authors 1999; Phylogenetic characterization of novel transport protein families revealed by genome analyses. Biochim Biophys Acta 1422:1–56 [CrossRef]
    [Google Scholar]
  62. Schägger H, von Jagow G. 1987; Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal Biochem 166:368–379 [CrossRef]
    [Google Scholar]
  63. Schneider D. A, Gaal T, Gourse R. L. 2002; NTP-sensing by rRNA promoters in Escherichia coli is direct. Proc Natl Acad Sci U S A 99:8602–8607 [CrossRef]
    [Google Scholar]
  64. Schweizer H. P. 1993; Small broad-host-range gentamycin resistance gene cassettes for site-specific insertion and deletion mutagenesis. BioTechniques 15:831–834
    [Google Scholar]
  65. Simon R, Priefer U. B, Pühler A. 1983; A broad host range mobilization system for in vivo genetic engineering: tranposon mutagenesis in Gram negative bacteria. Bio/Technology 1:784–791 [CrossRef]
    [Google Scholar]
  66. Soupene E, He L, Yan D, Kustu S. 1998; Ammonia acquisition in enteric bacteria: physiological role of the ammonium/methylammonium transport B (AmtB) protein. Proc Natl Acad Sci U S A 95:7030–7034 [CrossRef]
    [Google Scholar]
  67. Soupene E, Ramirez R. M, Kustu S. 2001; Evidence that fungal MEP proteins mediate diffusion of the uncharged species NH[sub]3[/sub] across the cytoplasmic membrane. Mol Cell Biol 21:5733–5741 [CrossRef]
    [Google Scholar]
  68. Soupene E, Lee H, Kustu S. 2002a; Ammonium/methylammonium transport (Amt) proteins facilitate diffusion of NH[sub]3[/sub] bidirectionally. Proc Natl Acad Sci U S A 99:3926–3931 [CrossRef]
    [Google Scholar]
  69. Soupene E, Chu T, Corbin R. W, Hunt D. F, Kustu S. 2002b; Gas channels for NH[sub]3[/sub]: proteins from hyperthermophiles complement an Escherichia coli mutant. J Bacteriol 184:3396–3400 [CrossRef]
    [Google Scholar]
  70. Stadtman E. R. 2001; The story of glutamine synthetase regulation. J Biol Chem 276:44357–44364 [CrossRef]
    [Google Scholar]
  71. Stips J, Thummer R, Neumann M, Schmitz R. A. 2004; GlnK effects complex formation between NifA and NifL in Klebsiella pneumoniae . Eur J Biochem 271:3379–3388 [CrossRef]
    [Google Scholar]
  72. Strösser J, Lüdke A, Schaffer S, Burkovski A, Krämer R. 2004; Regulation of GlnK activity: modification, membrane sequestration and proteolysis as regulatory principles in the network of nitrogen control in Corynebacterium glutamicum . Mol Microbiol 54:132–147 [CrossRef]
    [Google Scholar]
  73. Sweet W. J, Burris R. H. 1981; Inhibition of nitrogenase activity by NH4+ in Rhodospirillum rubrum . J Bacteriol 145:824–831
    [Google Scholar]
  74. Tanigawa R, Shirokane M, Maeda Si S, Omata T, Tanaka K, Takahashi H. 2002; Transcriptional activation of NtcA-dependent promoters of Synechococcus sp. PCC 7942 by 2-oxoglutarate in vitro . Proc Natl Acad Sci U S A 99:4251–4255 [CrossRef]
    [Google Scholar]
  75. Thomas G, Coutts G, Merrick M. 2000a; The glnKamtB operon. A conserved gene pair in prokaryotes. Trends Genet 16:11–14
    [Google Scholar]
  76. Thomas G. H, Mullins J. G, Merrick M. 2000b; Membrane topology of the Mep/Amt family of ammonium transporters. Mol Microbiol 37:331–344 [CrossRef]
    [Google Scholar]
  77. Van Dommelen A, Keijers V, Vanderleyden J, de Zamaroczy M. 1998; (Methyl)ammonium transport in the nitrogen-fixing bacterium Azospirillum brasilense . J Bacteriol 180:2652–2659
    [Google Scholar]
  78. van Heeswijk W. C, Hoving S, Molenaar D, Stegeman B, Kahn D, Westerhoff H. V. 1996; An alternative P[sub]II[/sub] protein in the regulation of glutamine synthetase in Escherichia coli . Mol Microbiol 21:133–146 [CrossRef]
    [Google Scholar]
  79. Vieira J, Messing J. 1982; The pUC plasmids, an M13mp7-derived system for insertion mutagenesis and sequencing with synthetic universal primers. Gene 19:259–268 [CrossRef]
    [Google Scholar]
  80. Wang H, Franke C. C, Nordlund S, Norén A. 2005; Reversible membrane association of dinitrogenase reductase activating glycohydrolase in the regulation of nitrogenase activity in Rhodospirillum rubrum ; dependence on GlnJ and AmtB1. FEMS Microbiol Lett 253:273–279 [CrossRef]
    [Google Scholar]
  81. Yakunin A. F, Hallenbeck P. C. 2002; AmtB is necessary for NH4+-induced nitrogenase switch-off and ADP-ribosylation in Rhodobacter capsulatus . J Bacteriol 184:4081–4088 [CrossRef]
    [Google Scholar]
  82. Yoch D. C, Gotto J. W. 1982; Effect of light intensity and inhibitors of nitrogen assimilation on NH4+ inhibition of nitrogenase activity in Rhodospirillum rubrum and Anabaena sp. J Bacteriol 151:800–806
    [Google Scholar]
  83. Zhang Y, Burris R. H, Ludden P. W, Roberts G. P. 1993; Posttranslational regulation of nitrogenase activity by anaerobiosis and ammonium in Azospirillum brasilense . J Bacteriol 175:6781–6788
    [Google Scholar]
  84. Zhang Y, Burris R. H, Ludden P. W, Roberts G. P. 1995; Comparison studies of dinitrogenase reductase ADP-ribosyl transferase/dinitrogenase reductase activating glycohydrolase regulatory systems in Rhodospirillum rubrum and Azospirillum brasilense . J Bacteriol 177:2354–2359
    [Google Scholar]
  85. Zhang Y, Burris R. H, Ludden P. W, Roberts G. P. 1997; Regulation of nitrogen fixation in Azospirillum brasilense . FEMS Microbiol Lett 152:195–204 [CrossRef]
    [Google Scholar]
  86. Zhang Y, Pohlmann E. L, Ludden P. W, Roberts G. P. 2000; Mutagenesis and functional characterization of the glnB , glnA , and nifA genes from the photosynthetic bacterium Rhodospirillum rubrum . J Bacteriol 182:983–992 [CrossRef]
    [Google Scholar]
  87. Zhang Y, Pohlmann E. L, Ludden P. W, Roberts G. P. 2001a; Functional characterization of three GlnB homologs in the photosynthetic bacterium Rhodospirillum rubrum : roles in sensing ammonium and energy status. J Bacteriol 183:6159–6168 [CrossRef]
    [Google Scholar]
  88. Zhang Y, Pohlmann E. L, Halbleib C. M, Ludden P. W, Roberts G. P. 2001b; Effect of P[sub]II[/sub] and its homolog GlnK on reversible ADP-ribosylation of dinitrogenase reductase by heterologous expression of the Rhodospirillum rubrum dinitrogenase reductase ADP-ribosyl transferase-dinitrogenase reductase-activating glycohydrolase regulatory system in Klebsiella pneumoniae . J Bacteriol 183:1610–1620 [CrossRef]
    [Google Scholar]
  89. Zhang Y, Pohlmann E. L, Ludden P. W, Roberts G. P. 2003; Regulation of nitrogen fixation by multiple P[sub]II[/sub] homologs in the photosynthetic bacterium Rhodospirillum rubrum . Symbiosis 35:85–100
    [Google Scholar]
  90. Zhang Y, Pohlmann E. L, Roberts G. P. 2004; Identification of critical residues in GlnB for its activation of NifA activity in the photosynthetic bacterium Rhodospirillum rubrum . Proc Natl Acad Sci U S A 101:2782–2787 [CrossRef]
    [Google Scholar]
  91. Zhang Y, Pohlmann E. L, Roberts G. P. 2005; GlnD is essential for NifA activation, NtrB/NtrC-regulated gene expression, and posttranslational regulation of nitrogenase activity in the photosynthetic, nitrogen-fixing bacterium Rhodospirillum rubrum . J Bacteriol 187:1254–1265 [CrossRef]
    [Google Scholar]
  92. Zheng L, Kostrewa D, Winkler F. K, Li X.-D, Bernèche S. 2004; The mechanism of ammonia transport based on the crystal structure of AmtB of Escherichia coli . Proc Natl Acad Sci U S A 101:17090–17095 [CrossRef]
    [Google Scholar]
  93. Zhu Y, Conrad M. C, Zhang Y, Roberts G. P. 2006; Identification of Rhodospirillum rubrum GlnB variants that are altered in their ability to interact with different targets in response to nitrogen-status signals. J Bacteriol 188:1866–1874 [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.28903-0
Loading
/content/journal/micro/10.1099/mic.0.28903-0
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