NasT-mediated antitermination plays an essential role in the regulation of the assimilatory nitrate reductase operon in azotobacter vinelandii

Applied and Environmental Microbiology

Volumn 78, Issue 18, 2012, Pages 6558-6567

  Wang, Baomin ^a,c   Pierson III, Leland S ^b   Rensing, Christopher ^a,d   Gunatilaka, Malkanthi K ^a   Kennedy, Christina ^a  

^a UNIVERSITY OF ARIZONA   (United States)

^b TEXAS A AND M UNIVERSITY   (United States)

^c UNIVERSITY OF VIRGINIA   (United States)

^d RTI INTERNATIONAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENTERIC BACTERIA; GENE MUTATIONS; HIGH ACTIVITY; MODEL SYSTEM; NITRATE REDUCTASE; NITRITE REDUCTASE; PROTEOBACTERIA; REGULATORY FUNCTIONS; REGULATORY MECHANISM; REGULATORY SYSTEMS; RNA-BINDING DOMAINS;

AMMONIUM COMPOUNDS; ENZYME ACTIVITY; GENES; NITROGEN FIXATION; RNA; TRANSCRIPTION;

NASA;

ANTITERMINATOR PROTEINS, BACTERIA; BACTERIAL PROTEIN; NAST PROTEIN, AZOTOBACTER VINELANDII; NITRATE REDUCTASE; RNA BINDING PROTEIN; TRANSACTIVATOR PROTEIN;

BACTERIUM; CHEMICAL BINDING; ENZYME ACTIVITY; HYPOTHESIS TESTING; MUTATION; NITRATE; NITROGEN FIXATION; PROTEIN;

ARTICLE; AZOTOBACTER VINELANDII; BINDING SITE; BIOSYNTHESIS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; OPERON; PROMOTER REGION;

AZOTOBACTER VINELANDII; BACTERIAL PROTEINS; BINDING SITES; GENE EXPRESSION REGULATION, BACTERIAL; NITRATE REDUCTASE; OPERON; PROMOTER REGIONS, GENETIC; RNA-BINDING PROTEINS; TRANS-ACTIVATORS;

AZOTOBACTER VINELANDII; ENTEROBACTERIACEAE; PROTEOBACTERIA;

EID: 84866175688     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01720-12     Document Type: Article

References (60)

1. Amann E, Brosius J, Ptashne M. 1983. Vectors bearing a hybrid trp-lac promoter useful for regulated expression of cloned genes in Escherichia coli. Gene. 25:167-178.
2. Baker KA, Perego M. 2011. Transcription antitermination by a phosphorylated response regulator and cobalamin-dependent termination at a B12 riboswitch contribute to ethanolamine utilization in Enterococcus faecalis. J. Bacteriol. 193:2575-2586.
3. Bali A, Blanco G, Hill S, Kennedy C. 1992. Excretion of ammonium by a nifL mutant of Azotobacter vinelandii fixing nitrogen. Appl. Environ. Microbiol. 58:1711-1718.
4. Barrios H, Valderrama B, Morett E. 1999. Compilation and analysis of sigma(54)-dependent promoter sequences. Nucleic Acids Res. 27:4305-4313.
5. Beynon J, Cannon M, Buchanan-Wollaston V, Cannon F. 1983. The nif promoters of Klebsiella pneumoniae have a characteristic primary structure. Cell. 34:665-671.
6. Bishop PE, Jarlenski DM, Hetherington DR. 1980. Evidence for an alternative nitrogen fixation system in Azotobacter vinelandii. Proc. Natl. Acad. Sci. U. S. A. 77:7342-7346.
7. Blanco G, Drummond M, Woodley P, Kennedy C. 1993. Sequence and molecular analysis of the nifL gene of Azotobacter vinelandii. Mol. Microbiol. 9:869-879.
8. Buchanan-Wollaston V, Cannon MC, Beynon JL, Cannon FC. 1981. Role of the nifA gene product in the regulation of nif expression in Klebsiella pneumoniae. Nature. 294:776-778.
9. Buck M, Miller S, Drummond M, Dixon R. 1986. Upstream activator sequences are present in the promoters of nitrogen fixation genes. Nature. 320:374-378.
10. Casadaban MJ, Cohen SN. 1980. Analysis of gene control signals by DNA fusion and cloning in Escherichia coli. J. Mol. Biol. 138:179-207.
11. Chai W, Stewart V. 1998. NasR, a novel RNA-binding protein, mediates nitrate-responsive transcription antitermination of the Klebsiella oxytoca M5al nasF operon leader in vitro. J. Mol. Biol. 283:339-351.
12. Chai W, Stewart V. 1999. RNA sequence requirements for NasRmediated, nitrate-responsive transcription antitermination of the Klebsiella oxytoca M5al nasF operon leader. J. Mol. Biol. 292:203-216.
13. Contreras A, et al. 1991. The product of the nitrogen fixation regulatory gene nfrX of Azotobacter vinelandii is functionally and structurally homologous to the uridylyltransferase encoded by glnD in enteric bacteria. J. Bacteriol. 173:7741-7749.
14. Del Papa MF, Perego M. 2008. Ethanolamine activates a sensor histidine kinase regulating its utilization in Enterococcus faecalis. J. Bacteriol. 190:7147-7156.
15. Dixon R, Kahn D. 2004. Genetic regulation of biological nitrogen fixation. Nat. Rev. Microbiol. 2:621-631.
16. Drummond M, Clements J, Merrick M, Dixon R. 1983. Positive control and autogenous regulation of the nifLA promoter in Klebsiella pneumoniae. Nature. 301:302-307.
17. Espin G, Alvarez-Morales A, Cannon F, Dixon R, Merrick M. 1982. Cloning of the glnA, ntrB and ntrC genes of Klebsiella pneumoniae and studies of their role in regulation of the nitrogen fixation (nif) gene cluster. Mol. Gen. Genet. 186:518-524.
18. Ferro-Luzzi Ames G, Nikaido K. 1985. Nitrogen regulation in Salmonella typhimurium. Identification of an ntrC protein-binding site and definition of a consensus binding sequence. EMBO J. 4:539-547.
19. Fox KA, et al. 2009. Multiple posttranscriptional regulatory mechanisms partner to control ethanolamine utilization in Enterococcus faecalis. Proc. Natl. Acad. Sci. U. S. A. 106:4435-4440.
20. Gollnick P, Babitzke P. 2002. Transcription attenuation. Biochim. Biophys. Acta. 1577:240-250.
21. Gutierrez JC, Ramos F, Ortner L, Tortolero M. 1995. nasST, two genes involved in the induction of the assimilatory nitrite-nitrate reductase operon (nasAB) of Azotobacter vinelandii. Mol. Microbiol. 18:579-591.
22. Gutierrez JC, Santero E, Tortolero M. 1997. Ammonium repression of the nitrite-nitrate (nasAB) assimilatory operon of Azotobacter vinelandii is enhanced in mutants expressing the nifO gene at high levels. Mol. Gen. Genet. 255:172-179.
23. Henkin TM, Yanofsky C. 2002. Regulation by transcription attenuation in bacteria: howRNAprovides instructions for transcription termination/antitermination decisions. Bioessays. 24:700-707.
24. Hill S, Austin S, Eydmann T, Jones T, Dixon R. 1996. Azotobacter vinelandii NIFL is a flavoprotein that modulates transcriptional activation of nitrogen-fixation genes via a redox-sensitive switch. Proc. Natl. Acad. Sci. U. S. A. 93:2143-2148.
25. Ho SN, Hunt HD, Horton RM, Pullen JK, Pease LR. 1989. Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene. 77:51-59.
26. 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.
27. Jiang P, Peliska JA, Ninfa AJ. 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.
28. Kamberov ES, Atkinson MR, Ninfa AJ. 1995. The Escherichia coli PII signal transduction protein is activated upon binding 2-ketoglutarate and ATP. J. Biol. Chem. 270:17797-17807.
29. Keener J, Kustu S. 1988. 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. Proc. Natl. Acad. Sci. U. S. A. 85:4976-4980.
30. Kennedy C, Drummond MH. 1985. The use of cloned nif regulatory elements from Klebsiella pneumoniae to examine nif regulation in Azotobacter vinelandii. J. Gen. Microbiol. 131:1787-1795.
31. Kennedy C, Robson RL. 1983. Activation of nif gene expression in Azotobacter by the nifA gene product of Klebsiella pneumoniae. Nature. 301:626-628.
32. Kustu S, North AK, Weiss DS. 1991. Prokaryotic transcriptional enhancers and enhancer-binding proteins. Trends Biochem. Sci. 16:397-402.
33. Leonardo JM, Goldberg RB. 1980. Regulation of nitrogen metabolism in glutamine auxotrophs of Klebsiella pneumoniae. J. Bacteriol. 142:99-110.
34. Lin JT, Stewart V. 1996. Nitrate and nitrite-mediated transcription antitermination control of nasF (nitrate assimilation) operon expression in Klebsiella pneumoniae M5al. J. Mol. Biol. 256:423-435.
35. Lin JT, Stewart V. 1998. Nitrate assimilation by bacteria. Adv. Microb. Physiol. 39:1-30, 379.
36. 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.
37. Little R, Reyes-Ramirez F, Zhang Y, van Heeswijk WC, Dixon R. 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.
38. Luque F, Santero E, Medina JR, Tortolero M. 1987. An effective mutagenic method in Azotobacter vinelandii. Microbiologia. 3:45-49.
39. 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.
40. Merrick MJ. 1983. Nitrogen control of the nif regulon in Klebsiella pneumoniae: involvement of the ntrA gene and analogies between ntrC and nifA. EMBO J. 2:39-44.
41. Merrick MJ, Edwards RA. 1995. Nitrogen control in bacteria. Microbiol. Rev. 59:604-622.
42. Miller WG, Leveau JHJ, Lindow SE. 2000. Improved gfp and inaZ broadhost-range promoter-probe vectors. Mol. Plant Microbe Interact. 13:1243-1250.
43. Morth JP, Feng V, Perry LJ, Svergun DI, Tucker PA. 2004. The crystal and solution structure of a putative transcriptional antiterminator from Mycobacterium tuberculosis. Structure. 12:1595-1605.
44. Newton JW, Wilson PW, Burris RH. 1953. Direct demonstration of ammonia as an intermediate in nitrogen fixation by Azotobacter. J. Biol. Chem. 204:445-451.
45. 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.
46. Norman RA, Poh CL, Pearl LH, O'Hara BP, Drew RE. 2000. Steric hindrance regulation of the Pseudomonas aeruginosa amidase operon. J. Biol. Chem. 275:30660-30667.
47. O'Hara BP, et al. 1999. Crystal structure and induction mechanism of AmiC-AmiR: a ligand-regulated transcription antitermination complex. EMBO J. 18:5175-5186.
48. Ramos F, Blanco G, Gutiérrez JC, Luque F, Tortolero M. 1993. Identification of an operon involved in the assimilatory nitrate-reducing system of Azotobacter vinelandii. Mol. Microbiol. 8:1145-1153.
49. Robson RL, et al. 1984. Genome size and complexity in Azotobacter chroococcum. J. Gen. Microbiol. 130:1603-1612.
50. Rudnick P, Kunz C, Gunatilaka MK, Hines ER, Kennedy C. 2002. Role of GlnK in NifL-mediated regulation of NifA activity in Azotobacter vinelandii. J. Bacteriol. 184:812-820.
51. Sambrook J, Russell DW. 2001. Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
52. Santero E, Luque F, Medina JR, Tortolero M. 1986. Isolation of ntrA-like mutants of Azotobacter vinelandii. J. Bacteriol. 166:541-544.
53. Santero E, Toukdarian A, Humphrey R, Kennedy C. 1988. Identification and characterization of two nitrogen fixation regulatory regions, nifA and nfrX, in Azotobacter vinelandii and Azotobacter chroococcum. Mol. Microbiol. 2:303-314.
54. Setubal JC, et al. 2009. Genome sequence of Azotobacter vinelandii, an obligate aerobe specialized to support diverse anaerobic metabolic processes. J. Bacteriol. 191:4534-4545.
55. Shu CJ, Ulrich LE, Zhulin IB. 2003. The NIT domain: a predicted nitrate-responsive module in bacterial sensory receptors. Trends Biochem. Sci. 28:121-124.
56. Shu CJ, Zhulin IB. 2002. ANTAR: an RNA-binding domain in transcription antitermination regulatory proteins. Trends Biochem. Sci. 27:3-5.
57. Soderback E, et al. 1998. The redox- and fixed nitrogen-responsive regulatory protein NIFL from Azotobacter vinelandii comprises discrete flavin and nucleotide-binding domains. Mol. Microbiol. 28:179-192.
58. Toukdarian A, Kennedy C. 1986. Regulation of nitrogen metabolism in Azotobacter vinelandii: isolation of ntr and glnA genes and construction of ntr mutants. EMBO J. 5:399-407.
59. Walmsley J, Kennedy C. 1991. Temperature-dependent regulation by molybdenum and vanadium of expression of the structural genes encoding three nitrogenases in Azotobacter vinelandii. Appl. Environ. Microbiol. 57:622-624.
60. Zuker M. 2003. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 31:3406-3415.