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Volume 158, Issue 1

P signal transduction proteins: pivotal players in post-translational control of nitrogenase activity Free

Abstract

The fixation of atmospheric nitrogen by the prokaryotic enzyme nitrogenase is an energy- expensive process and consequently it is tightly regulated at a variety of levels. In many diazotrophs this includes post-translational regulation of the enzyme’s activity, which has been reported in both bacteria and archaea. The best understood response is the short-term inactivation of nitrogenase in response to a transient rise in ammonium levels in the environment. A number of proteobacteria species effect this regulation through reversible ADP-ribosylation of the enzyme, but other prokaryotes have evolved different mechanisms. Here we review current knowledge of post-translational control of nitrogenase and show that, for the response to ammonium, the P signal transduction proteins act as key players.

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2012-01-01
2024-04-19
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References

  1. Akentieva N. ( 2008). Formation of a cross-linking complex of dinitrogenase reductase-activating glycohydrolase (DRAG) with membrane proteins from Rhodospirillum rubrum chromatophores. Biochemistry (Mosc) 73:171–177 [View Article][PubMed]
     [Google Scholar]
  2. Araújo L. M., Huergo L. F., Invitti A. L., Gimenes C. I., Bonatto A. C., Monteiro R. A., Souza E. M., Pedrosa F. O., Chubatsu L. S. ( 2008). Different responses of the GlnB and GlnZ proteins upon in vitro uridylylation by the Azospirillum brasilense GlnD protein. Braz J Med Biol Res 41:289–294 [View Article][PubMed]
     [Google Scholar]
  3. Berthold C. L., Wang H., Nordlund S., Högbom M. ( 2009). Mechanism of ADP-ribosylation removal revealed by the structure and ligand complexes of the dimanganese mono-ADP-ribosylhydrolase DraG. Proc Natl Acad Sci U S A 106:14247–14252 [View Article][PubMed]
     [Google Scholar]
  4. Burris R. H., Wilson P. W. ( 1946). Ammonia as an intermediate in nitrogen fixation by Azotobacter . J Bacteriol 52:505–512
     [Google Scholar]
  5. Burris R. G., Hartmann A., Zhang Y., Fu H. ( 1991). Control of nitrogenase in Azospirillum sp. Plant Soil 137:127–134 [View Article]
     [Google Scholar]
  6. Chow T. J., Tabita F. R. ( 1994). Reciprocal light-dark transcriptional control of nif and rbc expression and light-dependent posttranslational control of nitrogenase activity in Synechococcus sp. strain RF-1. J Bacteriol 176:6281–6285[PubMed]
     [Google Scholar]
  7. Conroy M. J., Durand A., Lupo D., Li X. D., Bullough P. A., Winkler F. K., Merrick M. ( 2007). The crystal structure of Escherichia coli AmtB–GlnK complex reveals how GlnK regulates the ammonia channel. Proc Natl Acad Sci U S A 104:1213–1218 [CrossRef]
     [Google Scholar]
  8. Coutts G., Thomas G., Blakey D., Merrick M. ( 2002). Membrane sequestration of the signal transduction protein GlinK by the ammonium transporter AmtB. EMBO J 21:1–10 [CrossRef]
     [Google Scholar]
  9. de Zamaroczy M. ( 1998). Structural homologues PII and PZ of Azospirillum brasilense provide intracellular signalling for selective regulation of various nitrogen-dependent functions. Mol Microbiol 29:449–463 [View Article][PubMed]
     [Google Scholar]
  10. de Zamaroczy M., Paquelin A., Elmerich C. ( 1993). Functional organization of the glnB–glnA cluster of Azospirillum brasilense . J Bacteriol 175:2507–2515[PubMed]
     [Google Scholar]
  11. Desnoues N., Lin M., Guo X., Ma L., Carreño-Lopez R., Elmerich C. ( 2003). Nitrogen fixation genetics and regulation in a Pseudomonas stutzeri strain associated with rice. Microbiology 149:2251–2262 [View Article][PubMed]
     [Google Scholar]
  12. Dodsworth J. A., Leigh J. A. ( 2006). Regulation of nitrogenase by 2-oxoglutarate-reversible, direct binding of a PII-like nitrogen sensor protein to dinitrogenase. Proc Natl Acad Sci U S A 103:9779–9784 [View Article][PubMed]
     [Google Scholar]
  13. Dodsworth J. A., Leigh J. A. ( 2007). NifI inhibits nitrogenase by competing with Fe protein for binding to the MoFe protein. Biochem Biophys Res Commun 364:378–382 [View Article][PubMed]
     [Google Scholar]
  14. Dodsworth J. A., Cady N. C., Leigh J. A. ( 2005). 2-Oxoglutarate and the PII homologues NifI1 and NifI2 regulate nitrogenase activity in cell extracts of Methanococcus maripaludis . Mol Microbiol 56:1527–1538 [View Article][PubMed]
     [Google Scholar]
  15. 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 [View Article][PubMed]
     [Google Scholar]
  16. Durner J., Böhm I., Hilz H., Böger P. ( 1994). Posttranslational modification of nitrogenase. Differences between the purple bacterium Rhodospirillum rubrum and the cyanobacterium Anabaena variabilis . Eur J Biochem 220:125–130 [View Article][PubMed]
     [Google Scholar]
  17. Ekman M., Tollbäck P., Bergman B. ( 2008). Proteomic analysis of the cyanobacterium of the Azolla symbiosis: identity, adaptation, and NifH modification. J Exp Bot 59:1023–1034 [View Article][PubMed]
     [Google Scholar]
  18. Enkh-Amgalan J., Kawasaki H., Seki T. ( 2006). Molecular evolution of the nif gene cluster carrying nifI1 and nifI2 genes in the Gram-positive phototrophic bacterium Heliobacterium chlorum . Int J Syst Evol Microbiol 56:65–74 [View Article][PubMed]
     [Google Scholar]
  19. 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 [View Article][PubMed]
     [Google Scholar]
  20. Fokina O., Chellamuthu V. R., Forchhammer K., Zeth K. ( 2010). Mechanism of 2-oxoglutarate signaling by the Synechococcus elongatus PII signal transduction protein. Proc Natl Acad Sci U S A 107:19760–19765 [View Article][PubMed]
     [Google Scholar]
  21. Forchhammer K. ( 2008). PII signal transducers: novel functional and structural insights. Trends Microbiol 16:65–72 [View Article][PubMed]
     [Google Scholar]
  22. Fu H., Burris R. H. ( 1989). Ammonium inhibition of nitrogenase activity in Herbaspirillum seropedicae . J Bacteriol 171:3168–3175[PubMed]
     [Google Scholar]
  23. Fu H., Burris R. H., Roberts G. P. ( 1990a). Reversible ADP-ribosylation is demonstrated to be a regulatory mechanism in prokaryotes by heterologous expression. Proc Natl Acad Sci U S A 87:1720–1724 [View Article][PubMed]
     [Google Scholar]
  24. Fu H. A., Fitzmaurice W. P., Roberts G. P., Burris R. H. ( 1990b). Cloning and expression of draTG genes from Azospirillum lipoferum . Gene 86:95–98 [View Article][PubMed]
     [Google Scholar]
  25. Gallon J. R., Cheng J., Dougherty L. J., Gallon V. A., Hilz H., Pederson D. M., Richards H. M., Rüggeberg S., Smith C. J. ( 2000). A novel covalent modification of nitrogenase in a cyanobacterium. FEBS Lett 468:231–233 [View Article][PubMed]
     [Google Scholar]
  26. Gruswitz F., O’Connell J. III, Stroud R. M. ( 2007). Inhibitory complex of the transmembrane ammonia channel, AmtB, and the cytosolic regulatory protein, GlnK, at 1.96 A. Proc Natl Acad Sci U S A 104:42–47 [View Article][PubMed]
     [Google Scholar]
  27. Halbleib C. M., Ludden P. W. ( 1999). Characterization of the interaction of dinitrogenase reductase-activating glycohydrolase from Rhodospirillum rubrum with bacterial membranes. Arch Microbiol 172:51–58 [View Article][PubMed]
     [Google Scholar]
  28. Halbleib C. M., Zhang Y., Roberts G. P., Ludden P. W. ( 2000a). Effects of perturbations of the nitrogenase electron transfer chain on reversible ADP-ribosylation of nitrogenase Fe protein in Klebsiella pneumoniae strains bearing the Rhodospirillum rubrum dra operon. J Bacteriol 182:3681–3687 [View Article][PubMed]
     [Google Scholar]
  29. Halbleib C. M., Zhang Y., Ludden P. W. ( 2000b). Regulation of dinitrogenase reductase ADP-ribosyltransferase and dinitrogenase reductase-activating glycohydrolase by a redox-dependent conformational change of nitrogenase Fe protein. J Biol Chem 275:3493–3500 [View Article][PubMed]
     [Google Scholar]
  30. Hallenbeck P. C. ( 1992). Mutations affecting nitrogenase switch-off in Rhodobacter capsulatus . Biochim Biophys Acta 1118:161–168 [View Article][PubMed]
     [Google Scholar]
  31. Hartmann L. S., Barnum S. R. ( 2010). Inferring the evolutionary history of Mo-dependent nitrogen fixation from phylogenetic studies of nifK and nifDK. . J Mol Evol 71:70–85 [View Article][PubMed]
     [Google Scholar]
  32. Hartmann A., Fu H., Burris R. H. ( 1986). Regulation of nitrogenase activity by ammonium chloride in Azospirillum spp. . J Bacteriol 165:864–870[PubMed]
     [Google Scholar]
  33. Hottiger M. O., Hassa P. O., Lüscher B., Schüler H., Koch-Nolte F. ( 2010). Toward a unified nomenclature for mammalian ADP-ribosyltransferases. Trends Biochem Sci 35:208–219 [View Article][PubMed]
     [Google Scholar]
  34. Huergo L. F., Souza E. M., Steffens M. B. R., Yates M. G., Pedrosa F. O., Chubatsu L. S. ( 2003). Regulation of glnB gene promoter expression in Azospirillum brasilense by the NtrC protein. FEMS Microbiol Lett 223:33–40 [View Article][PubMed]
     [Google Scholar]
  35. Huergo L. F., Filipaki A., Chubatsu L. S., Yates M. G., Steffens M. B. R., Pedrosa F. O., Souza E. M. ( 2005). Effect of the over-expression of PII and PZ proteins on the nitrogenase activity of Azospirillum brasilense . FEMS Microbiol Lett 253:47–54 [View Article][PubMed]
     [Google Scholar]
  36. Huergo L. F., Chubatsu L. S., Souza E. M., Pedrosa F. O., Steffens M. B. R., Merrick M. ( 2006a). Interactions between PII proteins and the nitrogenase regulatory enzymes DraT and DraG in Azospirillum brasilense . FEBS Lett 580:5232–5236 [View Article][PubMed]
     [Google Scholar]
  37. Huergo L. F., Souza E. M., Araujo M. S., Pedrosa F. O., Chubatsu L. S., Steffens M. B. R., Merrick M. ( 2006b). ADP-ribosylation of dinitrogenase reductase in Azospirillum brasilense is regulated by AmtB-dependent membrane sequestration of DraG. Mol Microbiol 59:326–337 [View Article][PubMed]
     [Google Scholar]
  38. Huergo L. F., Merrick M., Pedrosa F. O., Chubatsu L. S., Araujo L. M., Souza E. M. ( 2007). Ternary complex formation between AmtB, GlnZ and the nitrogenase regulatory enzyme DraG reveals a novel facet of nitrogen regulation in bacteria. Mol Microbiol 66:1523–1535[PubMed]
     [Google Scholar]
  39. Huergo L. F., Merrick M., Monteiro R. A., Chubatsu L. S., Steffens M. B. R., Pedrosa F. O., Souza E. M. ( 2009). In vitro interactions between the PII proteins and the nitrogenase regulatory enzymes dinitrogenase reductase ADP-ribosyltransferase (DraT) and dinitrogenase reductase-activating glycohydrolase (DraG) in Azospirillum brasilense . J Biol Chem 284:6674–6682 [View Article][PubMed]
     [Google Scholar]
  40. Huergo L. F., Noindorf L., Gimenes C., Lemgruber R. S. P., Cordellini D. F., Falarz L. J., Cruz L. M., Monteiro R. A., Pedrosa F. O. et al. ( 2010). Proteomic analysis of Herbaspirillum seropedicae reveals ammonium-induced AmtB-dependent membrane sequestration of PII proteins. FEMS Microbiol Lett 308:40–47 [View Article][PubMed]
     [Google Scholar]
  41. Inoue A., Shigematsu T., Hidaka M., Masaki H., Uozumi T. ( 1996). Cloning, sequencing and transcriptional regulation of the draT and draG genes of Azospirillum lipoferum FS. Gene 170:101–106 [View Article][PubMed]
     [Google Scholar]
  42. Javelle A., Merrick M. ( 2005). Complex formation between AmtB and GlnK: an ancestral role in prokaryotic nitrogen control. Biochem Soc Trans 33:170–172 [View Article][PubMed]
     [Google Scholar]
  43. Jiang P., Ninfa A. J. ( 2007). Escherichia coli PII signal transduction protein controlling nitrogen assimilation acts as a sensor of adenylate energy charge in vitro . Biochemistry 46:12979–12996 [View Article][PubMed]
     [Google Scholar]
  44. Jiang P., Ninfa A. J. ( 2009). Sensation and signaling of α-ketoglutarate and adenylylate energy charge by the Escherichia coli PII signal transduction protein require cooperation of the three ligand-binding sites within the PII trimer. Biochemistry 48:11522–11531 [View Article][PubMed]
     [Google Scholar]
  45. Jiang P., Peliska J. A., Ninfa A. J. ( 1998). 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 [View Article][PubMed]
     [Google Scholar]
  46. 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[PubMed]
     [Google Scholar]
  47. 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[PubMed]
     [Google Scholar]
  48. Kessler P. S., Leigh J. A. ( 1999). Genetics of nitrogen regulation in Methanococcus maripaludis . Genetics 152:1343–1351[PubMed]
     [Google Scholar]
  49. Kessler P. S., Daniel C., Leigh J. A. ( 2001). Ammonia switch-off of nitrogen fixation in the methanogenic archaeon Methanococcus maripaludis: mechanistic features and requirement for the novel GlnB homologues, NifI1 and NifI2. . J Bacteriol 183:882–889 [View Article][PubMed]
     [Google Scholar]
  50. Khademi S., O’Connell J. III, Remis J., Robles-Colmenares Y., Miercke L. J. W., Stroud R. M. ( 2004). Mechanism of ammonia transport by Amt/MEP/Rh: structure of AmtB at 1.35 Å. Science 305:1587–1594 [View Article][PubMed]
     [Google Scholar]
  51. Kim K., Zhang Y., Roberts G. P. ( 2004). Characterization of altered regulation variants of dinitrogenase reductase-activating glycohydrolase from Rhodospirillum rubrum . FEBS Lett 559:84–88 [View Article][PubMed]
     [Google Scholar]
  52. Klassen G., de Souza E. M., Yates M. G., Rigo L. U., Inaba J., Pedrosa F. O. ( 2001). Control of nitrogenase reactivation by the GlnZ protein in Azospirillum brasilense . J Bacteriol 183:6710–6713 [View Article][PubMed]
     [Google Scholar]
  53. Klassen G., Souza E. M., Yates M. G., Rigo L. U., Costa R. M., Inaba J., Pedrosa F. O. ( 2005). Nitrogenase switch-off by ammonium ions in Azospirillum brasilense requires the GlnB nitrogen signal-transducing protein. Appl Environ Microbiol 71:5637–5641 [View Article][PubMed]
     [Google Scholar]
  54. Koch-Nolte F., Kernstock S., Mueller-Dieckmann C., Weiss M. S., Haag F. ( 2008). Mammalian ADP-ribosyltransferases and ADP-ribosylhydrolases. Front Biosci 13:6716–6729 [View Article][PubMed]
     [Google Scholar]
  55. Laane C., Krone W., Konings W., Haaker H., Veeger C. ( 1980). Short-term effect of ammonium chloride on nitrogen fixation by Azotobacter vinelandii and by bacteroids of Rhizobium leguminosarum . Eur J Biochem 103:39–46 [View Article][PubMed]
     [Google Scholar]
  56. Leigh J. A., Dodsworth J. A. ( 2007). Nitrogen regulation in bacteria and archaea. Annu Rev Microbiol 61:349–377 [View Article][PubMed]
     [Google Scholar]
  57. Li X. D., Huergo L. F., Gasperina A., Pedrosa F. O., Merrick M., Winkler F. K. ( 2009). Crystal structure of dinitrogenase reductase-activating glycohydrolase (DraG) reveals conservation in the ADP-ribosylhydrolase fold and specific features in the ADP-ribose-binding pocket. J Mol Biol 390:737–746 [View Article][PubMed]
     [Google Scholar]
  58. 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[PubMed]
     [Google Scholar]
  59. Ljungström E., Yates M. G., Nordlund S. ( 1989). Purification of the activating enzyme for the Fe-protein of nitrogenase from Azospirillum brasilense . Biochim Biophys Acta 994:210–214 [View Article]
     [Google Scholar]
  60. Lobo A. L., Zinder S. H. ( 1988). Diazotrophy and nitrogenase activity in the archaebacterium Methanosarcina barkeri 227. Appl Environ Microbiol 54:1656–1661[PubMed]
     [Google Scholar]
  61. Lobo A. L., Zinder S. H. ( 1990). Nitrogenase in the archaebacterium Methanosarcina barkeri 227. J Bacteriol 172:6789–6796[PubMed]
     [Google Scholar]
  62. Lowery R. G., Ludden P. W. ( 1988). Purification and properties of dinitrogenase reductase ADP-ribosyltransferase from the photosynthetic bacterium Rhodospirillum rubrum . J Biol Chem 263:16714–16719[PubMed]
     [Google Scholar]
  63. Ludden P. W., Burris R. H. ( 1976). Activating factor for the iron protein of nitrogenase from Rhodospirillum rubrum . Science 194:424–426 [View Article][PubMed]
     [Google Scholar]
  64. Martin D. E., Reinhold-Hurek B. ( 2002). Distinct roles of PII-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 [View Article][PubMed]
     [Google Scholar]
  65. Martin D. E., Hurek T., Reinhold-Hurek B. ( 2000). Occurrence of three PII-like signal transmitter proteins in the diazotrophic proteobacterium Azoarcus sp. BH72. Mol Microbiol 38:276–288 [View Article][PubMed]
     [Google Scholar]
  66. Masepohl B., Krey R., Klipp W. ( 1993). The draTG gene region of Rhodobacter capsulatus is required for post-translational regulation of both the molybdenum and the alternative nitrogenase. J Gen Microbiol 139:2667–2675[PubMed] [CrossRef]
     [Google Scholar]
  67. Noindorf L., Rego F. G. M., Baura V. A., Monteiro R. A., Wassem R., Cruz L. M., Rigo L. U., Souza E. M., Steffens M. B. et al. ( 2006). Characterization of the orf1glnKamtB operon of Herbaspirillum seropedicae . Arch Microbiol 185:55–62 [View Article][PubMed]
     [Google Scholar]
  68. Noindorf L., Bonatto A. C., Monteiro R. A., Souza E. M., Rigo L. U., Pedrosa F. O., Steffens M. B. R., Chubatsu L. S. ( 2011). Role of PII proteins in nitrogen fixation control of Herbaspirillum seropedicae strain SmR1. BMC Microbiol 11:8 [View Article][PubMed]
     [Google Scholar]
  69. Nordlund S. ( 2000). Regulation of nitrogenase activity in phototrophic bacteria by reversible covalent modification. Prokaryotic nitrogen fixation: a model system for analysis of biological processes149–167 Triplett E. W. Wymondham, UK: Horizon Scientific Press;
     [Google Scholar]
  70. Norén A., Nordlund S. ( 1994). Changes in the NAD(P)H concentration caused by addition of nitrogenase ‘switch-off’ effectors in Rhodospirillum rubrum G-9, as measured by fluorescence. FEBS Lett 356:43–45 [View Article][PubMed]
     [Google Scholar]
  71. 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[PubMed]
     [Google Scholar]
  72. Norén A., Soliman A., Nordlund S. ( 1997). The role of NAD+ as a signal during nitrogenase switch-off in Rhodospirillum rubrum . Biochem J 322:829–832[PubMed]
     [Google Scholar]
  73. Oetjen J., Reinhold-Hurek B. ( 2009). Characterization of the DraT/DraG system for posttranslational regulation of nitrogenase in the endophytic betaproteobacterium Azoarcus sp. strain BH72. J Bacteriol 191:3726–3735 [View Article][PubMed]
     [Google Scholar]
  74. 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[PubMed]
     [Google Scholar]
  75. Pawlowski A., Riedel K. U., Klipp W., Dreiskemper P., Gross 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 [View Article][PubMed]
     [Google Scholar]
  76. Pierrard J., Ludden P. W., Roberts G. P. ( 1993). Posttranslational regulation of nitrogenase in Rhodobacter capsulatus: existence of two independent regulatory effects of ammonium. J Bacteriol 175:1358–1366[PubMed]
     [Google Scholar]
  77. Pope M. R., Murrell S. A., Ludden P. W. ( 1985). Covalent modification of the iron protein of nitrogenase from Rhodospirillum rubrum by adenosine diphosphoribosylation of a specific arginine residue. Proc Natl Acad Sci U S A 82:3173–3177 [View Article][PubMed]
     [Google Scholar]
  78. Pope M. R., Saari L. L., Ludden P. W. ( 1986). N-Glycohydrolysis of adenosine diphosphoribosyl arginine linkages by dinitrogenase reductase activating glycohydrolase (activating enzyme) from Rhodospirillum rubrum . J Biol Chem 261:10104–10111[PubMed]
     [Google Scholar]
  79. Radchenko M. V., Thornton J., Merrick M. ( 2010). Control of AmtB–GlnK complex formation by intracellular levels of ATP, ADP, and 2-oxoglutarate. J Biol Chem 285:31037–31045 [View Article][PubMed]
     [Google Scholar]
  80. Rajendran C., Gerhardt E. C. M., Bjelicc S., Gaspenina A., Scardelii M., Pearosa F. P., Chubatsu L. S., Merrick M., Souza E. M. et al. ( 2011). Crystal structure of the GlnZ–DraG complex reveals a different form of PII-target interaction. Proc Natl Acad Sci U S A
     [Google Scholar]
  81. Rodrigues T. E., Souza V. E., Monteiro R. A., Gerhardt E. C., Araújo L. M., Chubatsu L. S., Souza E. M., Pedrosa F. O., Huergo L. F. ( 2011). In vitro interaction between the ammonium transport protein AmtB and partially uridylylated forms of the PII protein GlnZ. Biochim Biophys Acta 1814:1203–1209[PubMed] [CrossRef]
     [Google Scholar]
  82. Saari L. L., Triplett E. W., Ludden P. W. ( 1984). Purification and properties of the activating enzyme for iron protein of nitrogenase from the photosynthetic bacterium Rhodospirillum rubrum . J Biol Chem 259:15502–15508[PubMed]
     [Google Scholar]
  83. Saari L. L., Pope M. R., Murrell S. A., Ludden P. W. ( 1986). Studies on the activating enzyme for iron protein of nitrogenase from Rhodospirillum rubrum . J Biol Chem 261:4973–4977[PubMed]
     [Google Scholar]
  84. Sant’Anna F. H., Trentini D. B., de Souto Weber S., Cecagno R., da Silva S. C., Schrank I. S. ( 2009). The PII superfamily revised: a novel group and evolutionary insights. J Mol Evol 68:322–336 [View Article][PubMed]
     [Google Scholar]
  85. Schindelin H., Kisker C., Schlessman J. L., Howard J. B., Rees D. C. ( 1997). Structure of ADP x AIF4−-stabilized nitrogenase complex and its implications for signal transduction. Nature 387:370–376 [View Article][PubMed]
     [Google Scholar]
  86. Seefeldt L. C., Hoffman B. M., Dean D. R. ( 2009). Mechanism of Mo-dependent nitrogenase. Annu Rev Biochem 78:701–722 [View Article][PubMed]
     [Google Scholar]
  87. Teixeira P. F., Jonsson A., Frank M., Wang H., Nordlund S. ( 2008). Interaction of the signal transduction protein GlnJ with the cellular targets AmtB1, GlnE and GlnD in Rhodospirillum rubrum: dependence on manganese, 2-oxoglutarate and the ADP/ATP ratio. Microbiology 154:2336–2347 [View Article][PubMed]
     [Google Scholar]
  88. Teixeira P. F., Wang H., Nordlund S. ( 2010). Nitrogenase switch-off and regulation of ammonium assimilation in response to light deprivation in Rhodospirillum rubrum are influenced by the nitrogen source used during growth. J Bacteriol 192:1463–1466 [View Article][PubMed]
     [Google Scholar]
  89. Tremblay P. L., Hallenbeck P. C. ( 2008). Ammonia-induced formation of an AmtB–GlnK complex is not sufficient for nitrogenase regulation in the photosynthetic bacterium Rhodobacter capsulatus . J Bacteriol 190:1588–1594 [View Article][PubMed]
     [Google Scholar]
  90. Tremblay P. L., Hallenbeck P. C. ( 2009). Of blood, brains and bacteria, the Amt/Rh transporter family: emerging role of Amt as a unique microbial sensor. Mol Microbiol 71:12–22 [View Article][PubMed]
     [Google Scholar]
  91. Tremblay P. L., Drepper T., Masepohl B., Hallenbeck P. C. ( 2007). Membrane sequestration of PII proteins and nitrogenase regulation in the photosynthetic bacterium Rhodobacter capsulatus . J Bacteriol 189:5850–5859 [View Article][PubMed]
     [Google Scholar]
  92. Truan D., Huergo L. F., Chubatsu L. S., Merrick M., Li X. D., Winkler F. K. ( 2010). A new PII protein structure identifies the 2-oxoglutarate binding site. J Mol Biol 400:531–539 [View Article][PubMed]
     [Google Scholar]
  93. 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[PubMed]
     [Google Scholar]
  94. Vintila S., Selao T., Norén A., Bergman B., El-Shehawy R. ( 2011). Characterization of nifH gene expression, modification and rearrangement in Nodularia spumigena strain AV1. FEMS Microbiol Ecol 77:449–459 [View Article][PubMed]
     [Google Scholar]
  95. 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 [View Article][PubMed]
     [Google Scholar]
  96. Wolfe D. M., Zhang Y., Roberts G. P. ( 2007). Specificity and regulation of interaction between the PII and AmtB1 proteins in Rhodospirillum rubrum . J Bacteriol 189:6861–6869 [View Article][PubMed]
     [Google Scholar]
  97. Xu Y., Cheah E., Carr P. D., van Heeswijk W. C., Westerhoff H. V., Vasudevan S. G., Ollis D. L. ( 1998). GlnK, a PII-homologue: structure reveals ATP binding site and indicates how the T-loops may be involved in molecular recognition. J Mol Biol 282:149–165 [View Article][PubMed]
     [Google Scholar]
  98. Xu Y., Carr P. D., Huber T., Vasudevan S. G., Ollis D. L. ( 2001). The structure of the PII-ATP complex. Eur J Biochem 268:2028–2037 [View Article][PubMed]
     [Google Scholar]
  99. 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 [View Article][PubMed]
     [Google Scholar]
  100. Yakunin A. F., Fedorov A. S., Laurinavichene T. V., Glaser V. M., Egorov N. S., Tsygankov A. A., Zinchenko V. V., Hallenbeck P. C. ( 2001). Regulation of nitrogenase in the photosynthetic bacterium Rhodobacter sphaeroides containing draTG and nifHDK genes from Rhodobacter capsulatus . Can J Microbiol 47:206–212[PubMed] [CrossRef]
     [Google Scholar]
  101. Yoch D. C., Li J. D., Hu C. Z., Scholin C. ( 1988). Ammonia switch-off of nitrogenase from Rhodobacter sphaeroides and Methylosinus trichosporium: no evidence for Fe protein modification. Arch Microbiol 150:1–5 [View Article][PubMed]
     [Google Scholar]
  102. Yuan J., Doucette C. D., Fowler W. U., Feng X. J., Piazza M., Rabitz H. A., Wingreen N. S., Rabinowitz J. D. ( 2009). Metabolomics-driven quantitative analysis of ammonia assimilation in E. coli . Mol Syst Biol 5:302 [View Article][PubMed]
     [Google Scholar]
  103. Zhang Y., Burris R. H., Roberts G. P. ( 1992). Cloning, sequencing, mutagenesis, and functional characterization of draT and draG genes from Azospirillum brasilense . J Bacteriol 174:3364–3369[PubMed]
     [Google Scholar]
  104. 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[PubMed]
     [Google Scholar]
  105. Zhang Y., Burris R. H., Ludden P. W., Roberts G. P. ( 1994). Posttranslational regulation of nitrogenase activity in Azospirillum brasilense ntrBC mutants: ammonium and anaerobic switch-off occurs through independent signal transduction pathways. J Bacteriol 176:5780–5787[PubMed]
     [Google Scholar]
  106. 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[PubMed]
     [Google Scholar]
  107. Zhang Y., Burris R. H., Ludden P. W., Roberts G. P. ( 1996). Presence of a second mechanism for the posttranslational regulation of nitrogenase activity in Azospirillum brasilense in response to ammonium. J Bacteriol 178:2948–2953[PubMed]
     [Google Scholar]
  108. 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 [View Article][PubMed]
     [Google Scholar]
  109. 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 [View Article][PubMed]
     [Google Scholar]
  110. Zhang Y., Pohlmann E. L., Ludden P. W., Roberts G. P. ( 2001). Functional characterization of three GlnB homologs in the photosynthetic bacterium Rhodospirillum rubrum: roles in sensing ammonium and energy status. J Bacteriol 183:6159–6168 [View Article][PubMed]
     [Google Scholar]
  111. 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 [View Article][PubMed]
     [Google Scholar]
  112. Zhang Y., Wolfe D. M., Pohlmann E. L., Conrad M. C., Roberts G. P. ( 2006). Effect of AmtB homologues on the post-translational regulation of nitrogenase activity in response to ammonium and energy signals in Rhodospirillum rubrum . Microbiology 152:2075–2089 [View Article][PubMed]
     [Google Scholar]
  113. Zhang Y., Pohlmann E. L., Roberts G. P. ( 2009). Effect of perturbation of ATP level on the activity and regulation of nitrogenase in Rhodospirillum rubrum. . J Bacteriol 191:5526–5537 [View Article][PubMed]
     [Google Scholar]
  114. 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 [View Article][PubMed]
     [Google Scholar]
  115. Zinchenko V., Churin Y., Shestopalov V., Shestakov S. ( 1994). Nucleotide sequence and characterization of the Rhodobacter sphaeroides glnB and glnA genes. Microbiology 140:2143–2151 [View Article][PubMed]
     [Google Scholar]
  116. Zumft W. G., Castillo F. ( 1978). Regulatory properties of the nitrogenase from Rhodopseudomonas palustris . Arch Microbiol 117:53–60 [View Article][PubMed]
     [Google Scholar]
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PII signal transduction proteins: pivotal players in post-translational control of nitrogenase activity
Microbiology 158, 176 (2012); https://doi.org/10.1099/mic.0.049783-0
/content/journal/micro/10.1099/mic.0.049783-0
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