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

Journal of Bacteriology

Volumn 187, Issue 4, 2005, Pages 1254-1265

  Zhang, Yaoping ^a   Pohlmann, Edward L ^a   Roberts, Gary P ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMMONIA; BACTERIAL PROTEIN; GLUTAMATE AMMONIA LIGASE; GLUTAMIC ACID; HEXOSE 1 PHOSPHATE URIDYLYLTRANSFERASE; NITROGEN; NITROGENASE; PROTEIN GLND; PROTEIN NIFA; PROTEIN NTRB; PROTEIN NTRC; UNCLASSIFIED DRUG;

ALLELE; ARTICLE; AZOTOBACTER VINELANDII; BACTERIAL GENE; CONTROLLED STUDY; CULTURE MEDIUM; DNA SEQUENCE; ENZYME ACTIVITY; GENE EXPRESSION; GLND GENE; IMMUNOBLOTTING; IN VIVO STUDY; NIF GENE; NITROGEN FIXATION; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN PROCESSING; RHODOSPIRILLUM RUBRUM;

AMMONIA; BACTERIAL PROTEINS; CULTURE MEDIA; DNA MUTATIONAL ANALYSIS; GENE DELETION; GENE EXPRESSION REGULATION, BACTERIAL; GENETIC COMPLEMENTATION TEST; GLUTAMATE SYNTHASE; GLUTAMIC ACID; NITROGEN; NITROGEN FIXATION; NITROGENASE; NUCLEOTIDYLTRANSFERASES; PROTEIN STRUCTURE, TERTIARY; RHODOSPIRILLUM RUBRUM; SEQUENCE DELETION; TRANSCRIPTION FACTORS;

EID: 14544269387     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.187.4.1254-1265.2005     Document Type: Article

References (64)

1. Albright, L. M., E. Huala, and F. M. Ausubel. 1989. Prokaryotic signal transduction mediated by sensor and regulator protein pairs. Annu. Rev. Genet. 13:311-336.
2. Aravind, L., and E. V. Koonin. 1998. The HD domain defines a new superfamily of metal-dependent phosphohydrolases. Trends Biochem. Sci. 23:469-472.
3. Arcondéguy, T., R. Jack, and M. Merrick. 2001. PII signal transduction proteins privotal players in microbial nitrogen control. Microbiol. Mol. Biol. Rev. 65:80-105.
4. Atkinson, M. R., and A. J. Ninfa. 1999. Characterization of the GlnK protein of Escherichia coli. Mol. Microbiol. 32:301-313.
5. Bateman, A., E. Birney, L. Cerruti, R. Durbin, L. Etwiller, S. R. Eddy, S. Griffiths-Jones, K. L. Howe, M. Marshall, and E. L. Sonnhammer. 2002. The Pfam protein families database. Nucleic Acids Res. 30:276-280.
6. Berger, D. K., F. Narberhaus, and S. Kustu. 1994. The isolated catalytic domain of NIFA, a bacterial enhancer-binding protein, activates transcription in vitro: activation is inhibited by NIFL. Proc. Natl. Acad. Sci. USA. 91:103-107.
7. Bloom, F. R., M. S. Levin, F. Foor, and B. Tyler. 1978. Regulation of glutamine synthetase formation in Escherichia coli: characterization of mutants lacking the uridylyltransferase. J. Bacteriol. 134:569-577.
8. II, the ntrBC products, and processing of the glnBA mRNA in Rhodospirillum rubrum. J. Bacteriol. 181:6530-6534.
9. Chipman, D. M., and B. Shaanan. 2001. The ACT domain family. Curr. Opin. Struct. Biol. 11:694-700.
10. Colnaghi, R., P. Rudnick, L. He, A. Green, D. Van, E. Larson, and C. Kennedy. 2001. Lethality of glnD null mutations in Azotobacter vinelandii is suppressible by prevention of glutamine synthetase adenylylation. Microbiology 147:1267-1276.
11. Ditta, G., T. Schmidhauser, E. Yakobson, P. Lu, X.-W. Liang, D. R. Finlay, D. Guiney, and D. R. Helinski. 1985. Plasmids related to the broad host range vector, pRK290, useful for gene cloning and for monitoring gene expression. Plasmid 13:149-153.
12. Edwards, R., and M. Merrick. 1995. The role of uridylyltransferase in the control of Klebsiella pneumoniae nif gene regulation. Mol. Gen. Genet. 247:189-198.
13. Fitzmaurice, W. P., L. L. Saari, R. G. Lowery, P. W. Ludden, and G. P. Roberts. 1989. Genes coding for the reversible ADP-ribosylation system of dinitrogenase reductase from Rhodospirillum rubrum. Mol. Gen. Genet. 218:340-347.
14. Foor, F., R. J. Cedergren, S. L. Streicher, S. G. Rhee, and B. Magasanik. 1978. Glutamine synthetase of Klebsiella aerogenes: properties of glnD mutants lacking uridylyltransferase. J. Bacteriol. 134:562-568.
15. Graf, J., and E. G. Ruby. 2000. Novel effects of a transposon insertion in the Vibrio fischeri glnD gene: defects in iron uptake and symbiotic persistence in addition to nitrogen utilization. Mol. Microbiol. 37:168-179.
16. Grunwald, S. K., D. P. Lies, G. P. Roberts, and P. W. Ludden. 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.
17. He, L., E. Soupene, A. Ninfa, and S. Kustu. 1998. Physiological role for the GlnK protein of enteric bacteria: relief of NifL inhibition under nitrogen-limiting conditions. J. Bacteriol. 180:6661-6667.
18. Henderson, N., S. Austin, and R. Dixon. 1989. Role of metal ions in negative regulation of nitrogen fixation by the nifL gene product from Klebsiella pneumoniae. Mol. Gen. Genet. 216:484-491.
19. Hesketh, A., D. Fink, B. Gust, H. U. Rexer, B. Scheel, K. Chater, W. Wohlleben, and A. Engels. 2002. The GlnD and GlnK homologues of Streptomyces coelicolor A3(2) are functionally dissimilar to their nitrogen regulatory system counterparts from enteric bacteria. Mol. Microbiol. 46:319-330.
20. Holm, L., and C. Sander. 1995. DNA polymerase beta belongs to an ancient nucleotidyltransferase superfamily. Trends Biochem. Sci. 20:345-347.
21. Hsieh, M. H., and H. M. Goodman. 2002. Molecular characterization of a novel gene family encoding ACT domain repeat proteins in Arabidopsis. Plant Physiol. 130:1797-1806.
22. Ikeda, T. P., A. E. Shauger, and S. Kustu. 1996. Salmonella typhimurium apparently perceives external nitrogen limitation as internal glutamine limitation. J. Mol. Biol. 259:589-607.
23. Jack, R., M. De Zamaroczy, and M. Merrick. 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.
24. Jiang, P., and A. J. Ninfa. 1999. Regulation of autophosphorylation of Escherichia coli nitrogen regulator II by the PII signal transduction protein. J. Bacteriol. 181:1906-1911.
25. Jiang, P., J. A. Peliska, and A. J. Ninfa. 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.
26. Jiang, P., J. A. Peliska, and A. J. Ninfa. 1998. The regulation of Escherichia coli glutamine synthetase revisited: role of 2-ketoglutarate in the regulation of glutamine synthetase adenylylation state. Biochemistry 37:12802-12810.
27. II-UMP and in vitro studies of regulation of glutamine synthetase in Rhodospirillum rubrum. J. Bacteriol. 181:6524-6529.
28. Johansson, M., and S. Nordlund. 1996. Transcription of the glnB and glnA genes in the photosynthetic bacterium Rhodospirillum rubrum. Microbiology 142:1265-1272.
29. II protein in the photosynthetic bacterium Rhodospirillum rubrum. J. Bacteriol. 179:4190-4194.
30. Kamberov, E. S., M. R. Atkinson, and A. J. Ninfa. 1995. The Escherichia coli PII signal transduction protein is activated upon binding 2-ketoglutarate and ATP. J. Biol. Chem. 270:17797-17807.
31. Kanemoto, R. H., and P. W. Ludden. 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.
32. Kennedy, C., and M. H. Drummond. 1985. The use of cloned nif regulatory elements from Klebsiella pneumoniae to examine nif regulation in Azotobacter vinelandii. J. Gen. Microbiol. 131:1787-1795.
33. Lehman, L. J., and G. P. Roberts. 1991. Identification of an alternative nitrogenase system in Rhodospirillum rubrum. J. Bacteriol. 173:5705-5711.
34. Liang, J. H., G. M. Nielsen, D. P. Lies, R. H. Burris, G. P. Roberts, and P. W. Ludden. 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.
35. Little, R., F. Reyes-Ramirez, Y. Zhang, W. C. van Heeswijk, and R. Dixon. 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.
36. Ludden, P. W. 1994. Reversible ADP-ribosylation as a mechanism of enzyme regulation in procaryotes. Mol. Cell. Biochem. 138:123-129.
37. Martinez-Argudo, I., R. Little, N. Shearer, P. Johnson, and R. Dixon. 2004. The NifL-NifA system: a multidomain transcriptional regulatory complex that integrates environmental signals. J. Bacteriol. 186:601-610.
38. Money, T., J. Barrett, R. Dixon, and S. Austin. 2001. Protein-protein interactions in the complex between the enhancer binding protein NIFA and the sensor NIFL from Azotobacter vinelandii. J. Bacteriol. 183:1359-1368.
39. Money, T., T. Jones, R. Dixon, and S. Austin. 1999. Isolation and properties of the complex between the enhancer binding protein NIFA and the sensor NIFL. J. Bacteriol. 181:4461-4468.
40. Ninfa, A. J., and M. R. Atkinson. 2000. PII signal transduction proteins. Trends Microbiol. 8:172-179.
41. II two-component system of enteric bacteria, p. 67-88. In J. A. Hoch and T. J. Silhavy (ed.), Two-component signal transduction. American Society for Microbiology, Washington, D.C.
42. O'Connell, K. P., S. J. Raffel, B. J. Saville, and J. Handelsman. 1998. Mutants of Rhizobium tropici strain CIAT899 that do not induce chlorosis in plants. Microbiology 144:2607-2617.
43. Pawlowski, A., K. U. Riedel, W. Klipp, P. Dreiskemper, S. Groß, H. Bierhoff, T. Drepper, and B. Masepohl. 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.
44. Perlova, O., R. Nawroth, E. M. Zellermann, and D. Meletzus. 2002. Isolation and characterization of the glnD gene of Gluconacetobacter diazotrophicus, encoding a putative uridylyltransferase/uridylyl-removing enzyme. Gene 297:159-168.
45. Porter, S. C., A. K. North, and S. Kustu. 1995. Mechanism of transcriptional activation by NtrC, p. 147-158. In J. A. Hoch and T. J. Silhavy (ed.), Two-component signal transduction. American Society for Microbiology, Washington, D.C.
46. Reitzer, L. 2003. Nitrogen assimilation and global regulation in Escherichia coli. Annu. Rev. Microbiol. 57:155-176.
47. Rudnick, P. A., T. Arcondeguy, C. K. Kennedy, and D. Kahn. 2001. glnD and mviN are genes of an essential operon in Sinorhizobium meliloti. J. Bacteriol. 183:2682-2685.
48. Schägger, H., and G. von Jagow. 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.
49. Schlüter, A., M. Nöhlen, M. Krämer, R. Defez, and U. B. Priefer. 2000. The Rhizobium leguminosatum bv. viciae glnD gene, encoding a uridylyltransferase/uridylyl-removing enzyme, is expressed in the root nodule but is not essential for nitrogen fixation. Microbiology 146:2987-2996.
50. Schweizer, H. P. 1993. Small broad-host-range gentamycin resistance gene cassetts for site-specific inserrtion and deletion mutagenesis. BioTechniques 15:831-834.
51. Shapiro, B. M., H. S. Kingdon, and E. R. Stadtman. 1967. Regulation of glutamine synthetase. VII. Adenylyl glutamine synthetase: a new form of the enzyme with altered regulatory and kinetic properties. Proc. Natl. Acad. Sci. USA 58:642-649.
52. Simon, R., U. B. Priefer, and A. Pühler. 1983. A broad host range mobilization system for in vivo genetic engineering: tranposon mutagenesis in Gram negative bacteria. Bio/Technology 1:784-791.
53. Stadtman, E. R. 2001. The story of glutamine synthetase regulation. J. Biol. Chem. 276:44357-44364.
54. Strösser, J., A. Lüdke, S. Schaffer, R. Krämer, and A. Burkovski. 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.
55. Van Dommelen, A., V. Keijers, E. Somers, and J. Vanderleyden. 2002. Cloning and characterisation of the Azospirillum brasilense glnD gene and analysis of a glnD mutant. Mol. Genet. Genomics 266:813-820.
56. II protein in the regulation of glutamine synthetase in Escherichia coli. Mol. Microbiol. 21:133-146.
57. Vieira, J., and J. Messing. 1991. New pUC-derived cloning vectors with different selectable markers and DNA replication origins. Gene 100:189-194.
58. Zhang, Y., R. H. Burris, P. W. Ludden, and G. P. Roberts. 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.
59. Zhang, Y., A. D. Cummings, R. H. Burris, P. W. Ludden, and G. P. Roberts. 1995. Effect of an ntrBC mutation on the posttranslational regulation of nitrogenase activity in Rhodospirillum rubrum. J. Bacteriol. 177:5322-5326.
60. Zhang, Y., K. Kim, P. Ludden, and G. Roberts. 2001. Isolation and characterization of draT mutants that have altered regulatory properties of dinitrogenase reductase ADP-ribosyltransferase in Rhodospirillum rubrum. Microbiology 147:193-202.
61. Zhang, Y., E. L. Pohlmann, P. W. Ludden, and G. P. Roberts. 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.
62. Zhang, Y., E. L. Pohlmann, P. W. Ludden, and G. P. Roberts. 2000. Mutagenesis and functional characterization of the glnB, glnA, and nifA genes from the photosynthetic bacterium Rhodospirillum rubrum. J. Bacteriol. 182:983-992.
63. II homologs in the photosynthetic bacterium Rhodospirillum rubrum. Symbiosis 35:85-100.
64. Zhang, Y., E. L. Pohlmann, and G. P. Roberts. 2004. Identification of critical residues in GlnB for its activation of NifA activity in the photosynthetic bacterium Rhodospirillum rubrum. Proc. Natl. Acad. Sci. USA 101:2782-2787.