Common patterns - Unique features: Nitrogen metabolism and regulation in Gram-positive bacteria

FEMS Microbiology Reviews

Volumn 34, Issue 4, 2010, Pages 588-605

  Amon, Johannes ^a   Titgemeyer, Fritz ^b   Burkovski, Andreas ^a  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^b MÜNSTER UNIVERSITY OF APPLIED SCIENCES   (Germany)

Author keywords

AmtR; Bacillus; Corynebacterium; GlnR; Mycobacterium; Streptomyces

Indexed keywords

AMMONIA; NITROGEN; TRANSCRIPTION FACTOR; QUATERNARY AMMONIUM DERIVATIVE;

BACILLUS; BACTERIAL VIRULENCE; BIODIVERSITY; CLOSTRIDIUM; CONTROLLED STUDY; CORYNEBACTERIUM; GRAM POSITIVE BACTERIUM; METABOLIC REGULATION; MYCOBACTERIUM; NITROGEN METABOLISM; NONHUMAN; PHYLUM; REGULATORY MECHANISM; REVIEW; STREPTOMYCES; GENE EXPRESSION REGULATION; METABOLISM; PATHOGENICITY; PHYSIOLOGY; VIRULENCE;

GENE EXPRESSION REGULATION, BACTERIAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GRAM-POSITIVE BACTERIA; NITROGEN; QUATERNARY AMMONIUM COMPOUNDS; VIRULENCE;

EID: 77953194775     PISSN: 01686445     EISSN: 15746976     Source Type: Journal    
DOI: 10.1111/j.1574-6976.2010.00216.x     Document Type: Review

References (156)

1. Amon J, Bräu T, Grimrath A et al 2008) Nitrogen control in Mycobacterium smegmatis: nitrogen-dependent expression of ammonium transport and assimilation proteins depends on the OmpR-type regulator GlnR. J Bacteriol 190 : 7108 7116.
2. Amon J, Titgemeyer F Burkovski A (2009) A genomic view on nitrogen metabolism and nitrogen control in mycobacteria. J Mol Microb Biotech 17 : 20 29.
3. Arcondeguy T, Jack R Merrick M (2001) PII signal transduction proteins, pivotal players in microbial nitrogen control. Microbiol Mol Biol R 65 : 80 105.
4. Ascenzi P, Bolognesi M, Milani M, Guertin M visca P (2007) Mycobacterial truncated hemoglobins: from genes to functions. Gene 398 : 42 51.
5. Atkinson MR, Blauwkamp TA, Bondarenko V, Studitsky V Ninfa A (2002) Activation of the glnA, glnK, and nac promoters as Escherichia coli undergoes the transition from nitrogen excess growth to nitrogen starvation. J Bacteriol 184 : 5358 5363.
6. Balleza E, López-Bojorquez LN, Martínez-Antonio A, Resendis-Antonio O, Lozada-Chávez I, Balderas-Martínez YI, Encarnación S Collado-vides J (2009) Regulation by transcription factors in bacteria: beyond description. FEMS Microbiol Rev 33 : 133 151.
7. Bandyopadhyay A, Arora A, Jain S et al 2009) Expression and molecular characterization of the Mycobacterium tuberculosis PII protein. J Biochem 147 : 279 289.
8. Beckers G, Strösser J, Hildebrandt U, Kalinowski J, Farwick M, Krämer R Burkovski A (2005) Regulation of AmtR-controlled gene expression in Corynebacterium glutamicum: mechanism and characterization of the AmtR regulon. Mol Microbiol 58 : 580 595.
9. Beckman JS, Beckman TW, Chen J, Marshall PA Freeman BA (1990) Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide. P Natl Acad Sci USA 87 : 1620 1624.
10. Behrmann I, Hillemann D, Pühler A, Strauch E Wohlleben W (1990) Overexpression of a Streptomyces viridochromogenes gene (glnII) encoding a glutamine synthetase similar to those of eucaryotes confers resistance against the antibiotic phosphinothricyl-alanyl-alanine. J Bacteriol 172 : 5326 5334.
11. Belitsky BR Sonenshein AL (2004) Modulation of activity of Bacillus subtilis regulatory proteins GltC and TnrA by glutamate dehydrogenase. J Bacteriol 186 : 3399 3407.
12. Belitsky BR, Wray LV Jr., Fisher SH, Bohannon DE Sonenshein AL (2000) Role of TnrA in nitrogen source-dependent repression of Bacillus subtilis glutamate synthase gene expression. J Bacteriol 182 : 5939 5947.
13. Brandenburg JL, Wray LV Jr., Beier L, Jarmer H, Saxild HH Fisher SH (2002) Roles of PucR, GlnR, and TnrA in regulating expression of the Bacillus subtilis ure P3 promoter. J Bacteriol 184 : 6060 6064.
14. Brown JR, Masuchi Y, Robb FT Doolittle WF (1994) Evolutionary relationships of bacterial and archaeal glutamine synthetase genes. J Mol Evol 38 : 566 576.
15. Brown SW Sonenshein AL (1996) Autogenous regulation of the Bacillus subtilis glnRA operon. J Bacteriol 178 : 2450 2454.
16. Bryk R, Griffin P Nathan C (2000) Peroxynitrite reductase activity of bacterial peroxiredoxins. Nature 407 : 211 215.
17. Bryk R, Lima CD, Erdjument-Bromage H, Tempst P Nathan C (2002) Metabolic enzymes of mycobacteria linked to antioxidant defense by a thioredoxin-like protein. Science 295 : 1073 1077.
18. Bryk R, Gold B, venugopal A et al 2008) Selective killing of nonreplicating mycobacteria. Host Cell Microbe 3 : 137 145.
19. Buchinger S, Strösser J, Rehm N, Hänßler E, Hans S, Bathe B, Schomburg D, Krämer R Burkovski A (2009) A combination of transcriptome and metabolome analyses reveals new targets of the Corynebacterium glutamicum nitrogen regulator AmtR. J Biotechnol 140 : 68 74.
20. Bueno R, Pahel G Magasanik B (1985) Role of glnB and glnD gene products in regulation of the glnALG operon of Escherichia coli. J Bacteriol 164 : 816 822.
21. Burkovski A (2005) Nitrogen metabolism and its regulation. Handbook of Corynebacterium glutamicum (Bott M Eggeling L, eds), pp. 333 349. CRC Press LLC
22. Burkovski A (2007) Nitrogen control in Corynebacterium glutamicum: proteins, mechanisms, signals. J Microbiol Biotechn 17 : 187 194.
23. Carroll P, Pashley CA Parish T (2008) Functional analysis of GlnE, an essential adenylyl transferase in Mycobacterium tuberculosis. J Bacteriol 190 : 4894 4902.
24. Clemens DL, Lee B-Y Horwitz MA (1995) Purification, characterization, and genetic analysis of Mycobacterium tuberculosis urease, a potentially critical determinant of host-pathogen interaction. J Bacteriol 177 : 5644 5652.
25. Crawford MJ Goldberg DE (1998) Role for the Salmonella flavohemoglobin in protection from nitric oxide. J Biol Chem 273 : 34028 34032.
26. Detsch C Stülke J (2003) Ammonium utilization in Bacillus subtilis: transport and regulatory functions of NrgA and NrgB. Microbiology 149 : 3289 3297.
27. Dineen SS, villapakkam AC, Nordman JT Sonenshein AL (2007) Repression of Clostridium difficile toxin gene expression by CodY. Mol Microbiol 66 : 206 219.
28. Doroshchuk NA, Gelfand MS Rodionov DA (2006) Regulation of nitrogen metabolism in Gram-positive bacteria. Mol Biol 40 : 919 926.
29. Dupuy B, Govind R, Antunes A Matamouros S (2008) Clostridium difficile toxin synthesis is negatively regulated by TcdC. J Med Microbiol 57 : 685 689.
30. Ehrt S Schnappinger D (2009) Mycobacterial survival strategies in the phagosome: defense against host stresses. Cell Microbiol 11 : 1170 1178.
31. Eisenberg D, Gill HS, Pfluegl GM Rotstein SH (2000) Structure-function relationships of glutamine synthetases. Biochim Biophys Acta 1477 : 122 145.
32. Fabrino DL, Bleck CKE, Anes E, Hasilik A, Melo RCN, Niederweis M, Griffiths G Gutierrez MG (2009) Porins facilitate nitric oxide-mediated killing of mycobacteria. Microbes Infect 11 : 868 875.
33. Fadiel A, Eichenbaum KD, El Semary N Epperson B (2007) Mycoplasma genomics: tailoring the genome for minimal life requirements through reductive evolution. Front Biosci 12 : 2020 2028.
34. Fink D, Weisschuh N, Reuther J, Wohlleben W Engels A (2002) Two transcriptional regulators GlnR and GlnRII are involved in regulation of nitrogen metabolism in Streptomyces coelicolor A3(2). Mol Microbiol 46 : 331 347.
35. Fisher SH (1999) Regulation of nitrogen metabolism in Bacillus subtilis: vive la différence! Mol Microbiol 32 : 223 232.
36. Fisher SH Wray LV Jr. (2008) Bacillus subtilis glutamine synthetase regulates its own synthesis by acting as a chaperone to stabilize GlnR-DNA complexes. P Natl Acad Sci USA 105 : 1014 1019.
37. Fisher SH Wray LV Jr. (2009) Novel trans-acting Bacillus subtilis glnA mutations that derepress glnRA expression. J Bacteriol 191 : 2485 2492.
38. Forchhammer K (2004) Global carbon/nitrogen control by PII signal transduction in cyanobacteria: from signals to targets. FEMS Microbiol Rev 28 : 319 333.
39. Forchhammer K (2007) Glutamine signalling in bacteria. Front Biosci 12 : 358 370.
40. Forchhammer K (2008) P(II) signal transducers: novel functional and structural insights. Trends Microbiol 16 : 65 72.
41. Fuerst JA (1995) The planctomycetes: emerging models for microbial ecology, evolution and cell biology. Microbiology 141 : 1493 1506.
42. Gardner PR, Gardner AM, Martin LA Salzman AL (1998) Nitric oxide deoxygenase: an enzymatic function for flavohemoglobin. P Natl Acad Sci USA 95 : 10378 10383.
43. Gómez-Valero L, Rocha EP, Latorre A Silva FJ (2007) Reconstructing the ancestor of Mycobacterium leprae: the dynamics of gene loss and genome reduction. Genome Res 17 : 1178 1185.
44. Gustafson J, Strassle A, Hachler H, Kayser FH Berger-Bächi B (1994) The femC locus of Staphylococcus aureus required for methicillin resistance includes the glutamine synthetase operon. J Bacteriol 176 : 1460 1467.
45. Hänßler E Burkovski A (2008) Molecular mechanisms of nitrogen control in corynebacteria. Corynebacteria: Genomics and Molecular Biology (Burkovski A, ed), pp. 183 201. Caister Academic Press
46. Harth G Horwitz MA (1997) Expression and efficient export of enzymatically active Mycobacterium tuberculosis glutamine synthetase in Mycobacterium smegmatis and evidence that the information for export is contained within the protein. J Biol Chem 272 : 22728 22735.
47. Harth G Horwitz MA (1999) An inhibitor of exported Mycobacterium tuberculosis glutamine synthetase selectively blocks the growth of pathogenic mycobacteria in axenic culture and in human monocytes: extracellular proteins as potential novel drug targets. J Exp Med 189 : 1425 1436.
48. Harth G Horwitz MA (2003) Inhibition of Mycobacterium tuberculosis glutamine synthetase as a novel antibiotic strategy against tuberculosis: demonstration of efficacy in vivo. Infect Immun 71 : 456 464.
49. Harth G, Clemens DL Horwitz MA (1994) Glutamine synthetase of Mycobacterium tuberculosis: extracellular release and characterization of its enzymatic activity. P Natl Acad Sci USA 91 : 9342 9346.
50. Harth G, Zamecnik PC, Tang JY, Tabatadze D Horwitz MA (2000) Treatment of Mycobacterium tuberculosis with antisense oligonucleotides to glutamine synthetase mRNA inhibits glutamine synthetase activity, formation of the poly-l-glutamate/glutamine cell wall structure, and bacterial replication. P Natl Acad Sci USA 97 : 418 423.
51. Harth G, Maslesa-Galić S, Tullius MV Horwitz MA (2005) All four Mycobacterium tuberculosis glnA genes encode glutamine synthetase activities but only GlnA1 is abundantly expressed and essential for bacterial homeostasis. Mol Microbiol 58 : 1157 1172.
52. Hasselt K, Sevvana M, Burkovski A Muller YA (2009) Crystallization and preliminary analysis of selenomethionine-labelled AmtR from Corynebacterium glutamicum. Acta Crystallogr F 65 : 1123 1127.
53. Heinrich A, Woyda K, Brauburger K, Meiss G, Detsch C, Stülke J Forchhammer K (2006) Interaction of the membrane-bound GlnK-AmtB complex with the master regulator of nitrogen metabolism TnrA in Bacillus subtilis. J Biol Chem 281 : 34909 34917.
54. Hendriksen WT, Bootsma HJ, Estevão S, Hoogenboezem T, de Jong A, de Groot R, Kuipers OP Hermans PW (2008a) CodY of Streptococcus pneumoniae: link between nutritional gene regulation and colonization. J Bacteriol 190 : 590 601.
55. Hendriksen WT, Kloosterman TG, Bootsma HJ, Estevão S, de Groot R, Kuipers OP Hermans PW (2008b) Site-specific contributions of glutamine-dependent regulator GlnR and GlnR-regulated genes to virulence of Streptococcus pneumoniae. Infect Immun 76 : 1230 1238.
56. Herrero A, Muro-Pastor AM Flores E (2001) Nitrogen control in cyanobacteria. J Bacteriol 183 : 411 425.
57. Hesketh A, Fink D, Gust B, Rexer H-U, Scheel B, Chater K, Wohlleben W Engels A (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.
58. Hotter GS, Mouat P Collins DM (2008) Independent transcription of glutamine synthetase (glnA2) and glutamine synthetase adenylyltransferase (glnE) in Mycobacterium bovis and Mycobacterium tuberculosis. Tuberculosis 88 : 382 389.
59. Hu P, Leighton T, Ishkhanova G Kustu S (1999a) Sensing of nitrogen limitation by Bacillus subtilis: Comparison to enteric bacteria. J Bacteriol 181 : 5042 5050.
60. Hu Y, Butcher PD, Mangan JA, Rajandream MA Coates AR (1999b) Regulation of hmp gene transcription in Mycobacterium tuberculosis: effects of oxygen limitation and nitrosative and oxidative stress. J Bacteriol 181 : 3486 3493.
61. Ikeda TP, Shauger AE Kustu S (1996) Salmonella typhimurium apparently perceives external nitrogen limitation as internal glutamine limitation. J Mol Biol 259 : 589 607.
62. Jakoby M, Tesch M, Sahm H, Krämer R Burkovski A (1997) Isolation of the Corynebacterium glutamicum glnA gene encoding glutamine synthetase I. FEMS Microbiol Lett 154 : 81 88.
63. Jakoby M, Krämer R Burkovski A (1999) Nitrogen regulation in Corynebacterium glutamicum: isolation of genes involved and biochemical characterization of corresponding proteins. FEMS Microbiol Lett 173 : 303 310.
64. Jakoby M, Nolden L, Meier-Wagner J, Krämer R Burkovski A (2000) AmtR, a global repressor in the nitrogen regulation system of Corynebacterium glutamicum. Mol Microbiol 37 : 964 977.
65. Jiang P Ninfa AJ (2009a) Reconstitution of Escherichia coli glutamine synthetase adenylyltransferase from N-terminal and C-terminal fragments of the enzyme. Biochemistry 48 : 415 423.
66. Jiang P Ninfa AJ (2009b) α-ketoglutarate controls the ability of the Escherichia coli PII signal transduction protein to regulate the activities of NRII (NtrB) but does not control the binding of PII to NRII. Biochemistry 48 : 11514 11521.
67. Jiang P Ninfa AJ (2009c) 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.
68. Jiang P, Peliska JA Ninfa AJ (1998a) 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.
69. Jiang P, Peliska JA Ninfa AJ (1998b) Reconstitution of the signal-transduction bicyclic cascade responsible for the regulation of Ntr gene transcription in Escherichia coli. Biochemistry 37 : 12795 12801.
70. Jiang P, Peliska JA Ninfa AJ (1998c) The regulation of Escherichia coli glutamine synthetase revisited: role of 2-ketoglutarate in the regulation of glutamine synthetase adenylylation state. Biochemistry 37 : 12802 12810.
71. Karlsson S, Burman LG Akerlund T (2008) Induction of toxins in Clostridium difficile is associated with dramatic changes of its metabolism. Microbiology 154 : 3430 3436.
72. Kayumov A, Heinrich A, Sharipova M, Iljinskaya O Forchhammer K (2008) Inactivation of the general transcription factor TnrA in Bacillus subtilis by proteolysis. Microbiology 154 : 2348 2355.
73. Kenney LJ (2002) Structure/function relationships in OmpR and other winged-helix transcription factors. Curr Opin Microbiol 5 : 135 141.
74. Kloosterman TG, Hendriksen WT, Bijlsma JJ, Bootsma HJ, van Hijum S, Kok J, Hermans PW Kuipers OP (2006) Regulation of glutamine and glutamate metabolism by GlnR and GlnA in Streptococcus pneumonia. J Biol Chem 281 : 25097 25109.
75. Lama A, Pawaria S, Bidon-Chanal A, Anand A, Gelpi JL, Arya S, Marti M, Estrin DA, Luque FJ Dikshit KL (2009) Role of Pre-A motif in nitric oxide scavenging by truncated hemoglobin, HbN, of Mycobacterium tuberculosis. J Biol Chem 284 : 14457 14468.
76. Larsen R, Kloosterman TG, Kok J Kuipers OP (2006) GlnR-mediated regulation of nitrogen metabolism in Lactococcus lactis. J Bacteriol 188 : 4978 4982.
77. Leigh JA Dodsworth JA (2007) Nitrogen regulation in bacteria and archaea. Annu Rev Microbiol 61 : 349 377.
78. Malm S, Tiffert Y, Micklinghoff J et al 2009) The roles of the nitrate reductase NarGHJI, the nitrite reductase NirBD and the response regulator GlnR in nitrate assimilation of Mycobacterium tuberculosis. Microbiology 155 : 1332 1339.
79. Mendez M, Huang IH, Ohtani K, Grau R, Shimizu T Sarker MR (2008) Carbon catabolite repression of type IV pilus-dependent gliding motility in the anaerobic pathogen Clostridium perfringens. J Bacteriol 190 : 48 60.
80. Merrick MJ Edwards RA (1995) Nitrogen control in bacteria. Microbiol Rev 59 : 604 622.
81. Muhl D, Jeßberger N, Hasselt K, Jardin C, Sticht H Burkovski A (2009) DNA binding by Corynebacterium glutamicum TetR-type transcription regulator AmtR. BMC Mol Biol 10 : 73.
82. Müller T, Strösser J, Buchinger S, Nolden L, Wirtz A, Krämer R Burkovski A (2006) Mutation-induced metabolite pool alterations in Corynebacterium glutamicum: towards the identification of nitrogen control signals. J Biotechnol 126 : 440 453.
83. Muro-Pastor MI, Reyes JC Florencio FJ (2005) Ammonium assimilation in cyanobacteria. Photosynth Res 83 : 135 150.
84. Nakano MM, Hoffmann T, Zhu Y Jahn D (1998) Nitrogen and oxygen regulation of Bacillus subtilis nasDEF encoding NADH-dependent nitrite reductase by TnrA and ResDE. J Bacteriol 180 : 5344 5350.
85. Nathan CF Ehrt S (2004) Nitric oxide in tuberculosis. Tuberculosis, 2nd edn (Rom W Garay S, eds), pp. 215 236. Lippincott Williams and Wilkins
86. Nathan CF Shiloh MU (2000) Reactive oxygen and nitrogen intermediates in the relationship between mammalian hosts and microbial pathogens. P Natl Acad Sci USA 97 : 8841 8848.
87. Niebisch A, Kabus A, Schultz C, Weil B Bott A (2006) Corynebacterial protein kinase G controls 2-oxoglutarate dehydrogenase activity via the phosphorylation status of the OdhI protein. J Biol Chem 281 : 12300 12307.
88. Nolden L, Farwick M, Krämer R Burkovski A (2001a) Glutamine synthetases of Corynebacterium glutamicum: transcriptional control and regulation of activity. FEMS Microbiol Lett 201 : 91 98.
89. Nolden L, Ngouoto-Nkili C-E, Bendt AK, Krämer R Burkovski A (2001b) Sensing nitrogen limitation in Corynebacterium glutamicum: The role of glnK and glnD. Mol Microbiol 42 : 1281 1295.
90. Nolden L, Beckers G Burkovski A (2002) Nitrogen assimilation in Corynebacterium diphtheriae: pathways and regulatory cascades. FEMS Microbiol Lett 208 : 287 293.
91. Nordqvist A, Nilsson MT, Röttger S, Odell LR, Krajewski WW, Evalena Andersson C, Larhed M, Mowbray SL Karlén A (2008) Evaluation of the amino acid binding site of Mycobacterium tuberculosis glutamine synthetase for drug discovery. Bioorg Med Chem 16 : 5501 5513.
92. Osanai T Tanaka K (2007) Keeping in touch with PII: PII-interacting proteins in unicellular cyanobacteria. Plant Cell Physiol 48 : 908 914.
93. Parish T Stoker NG (2000) glnE is an essential gene in Mycobacterium tuberculosis. J Bacteriol 182 : 5715 5720.
94. Pashley CA, Brown AC, Robertson D Parish T (2006) Identification of the Mycobacterium tuberculosis GlnE promoter and its response to nitrogen availability. Microbiology 152 : 2727 2734.
95. Perez JC Groisman EA (2009) Evolution of transcriptional regulatory circuits in bacteria. Cell 138 : 233 244.
96. Picossi S, Belitsky BR Sonenshein AL (2007) Molecular mechanism of the regulation of Bacillus subtilis gltAB expression by GltC. J Mol Biol 365 : 1298 1313.
97. 2 and NO by reduced coenzyme F420 protects mycobacteria from nitrosative damage. P Natl Acad Sci USA 106 : 6333 6338.
98. Quaiser A, Ochsenreiter T, Lanz C, Schuster SC, Treusch AH, Eck J Schleper C (2003) Acidobacteria form a coherent but highly diverse group within the bacterial domain: evidence from environmental genomics. Mol Microbiol 50 : 563 575.
99. Ramos JL, Martinez-Bueno M, Molina-Henares AJ, Teran W, Watanabe K, Zhang X, Gallegos MT, Brennan R Tobes R (2005) The TetR family of transcriptional repressors. Microbiol Mol Biol R 69 : 326 356.
100. Read R, Pashley CA, Smith D Parish T (2007) The role of GlnD in ammonia assimilation in Mycobacterium tuberculosis. Tuberculosis 87 : 384 390.
101. Rehm N, Buchinger S, Strösser J, Dotzauer A, Walter B, Hans S, Bathe B, Schomburg D, Krämer R Burkovski A (2010) Impact of adenylyltransferase GlnE on nitrogen starvation response in Corynebacterium glutamicum. J Biotechnol 145 : 244 252.
102. Reid SJ Stutz HE (2005) Nitrogen assimilation in clostridia. Handbook on Clostridia (Dürre P, ed), pp. 239 256. CRC Press LLC
103. Reuther J Wohlleben W (2007) Nitrogen metabolism in Streptomyces coelicolor: transcriptional and post-translational regulation. J Mol Microb Biotech 12 : 139 146.
104. Rexer HU, Schäberle T, Wohlleben W Engels A (2006) Investigation of the functional properties and regulation of three glutamine synthetase-like genes in Streptomyces coelicolor A3(2). Arch Microbiol 186 : 447 458.
105. Reyrat J-M, Lopez-Ramirez G, Ofredo C, Gicquel B Winter N (1996) Urease activity does not contribute dramatically to persistence of Mycobacterium bovis Bacillus Calmette-Guérin. Infect Immun 64 : 3934 3936.
106. Rodríguez-García A, Barreiro C, Santos-Beneit F, Sola-Landa A Martín JF (2007) Genome-wide transcriptomic and proteomic analysis of the primary response to phosphate limitation in Streptomyces coelicolor M145 and in a ΔphoP mutant. Proteomics 7 : 2410 2429.
107. Rodríguez-García A, Sola-Landa A, Apel K, Santos-Beneit F Martín JF (2009) Phosphate control over nitrogen metabolism in Streptomyces coelicolor: direct and indirect negative control of glnR, glnA, glnII and amtB expression by the response regulator PhoP. Nucleic Acids Res 37 : 3230 3242.
108. Schmitz RA (2000) Internal glutamine and glutamate pools in Klebsiella pneumoniae grown under different conditions of nitrogen availability. Curr Microbiol 41 : 357 362.
109. Schreier HJ, Brown SW, Hirschi KD, Nomellini JF Sonenshein AL (1989) Regulation of Bacillus subtilis glutamine synthetase gene expression by the product of the glnR gene. J Mol Biol 210 : 51 63.
110. Schreier HJ, Caruso SM Maier KC (2000) Control of Bacillus subtilis glutamine synthetase expression by glnR from Staphylococcus aureus. Curr Microbiol 41 : 425 429.
111. Sendide K, Deghmane A-E, Reyrat J-M, Talal A Hmama Z (2004) Mycobacterium bovis BCG urease attenuates major histocompatibility complex class II trafficking to the macrophage cell surface. Infect Immun 72 : 4200 4209.
112. Shatalin K, Gusarov I, Avetissova E, Shatalina Y, McQuade LE, Lippard SJ Nudler E (2008) Bacillus anthracis-derived nitric oxide is essential for pathogen virulence and survival in macrophages. P Natl Acad Sci USA 105 : 1009 1013.
113. Shi S Ehrt S (2006) Dihydrolipoamide acyltransferase is critical for Mycobacterium tuberculosis pathogenesis. Infect Immun 74 : 56 63.
114. Shiloh MU Nathan CF (2000) Reactive nitrogen intermediates and the pathogenesis of Salmonella and mycobacteria. Curr Opin Microbiol 3 : 35 42.
115. Shu CJ Zhulin IB (2002) ANTAR: an RNA-binding domain in transcription antitermination regulatory proteins. Trends Biochem Sci 27 : 3 5.
116. Slack FJ, Serror P, Joyce E Sonenshein AL (1995) A gene required for nutritional repression of the Bacillus subtilis dipeptide permease operon. Mol Microbiol 15 : 689 702.
117. Somerville GA Proctor RA (2009) At the crossroads of bacterial metabolism and virulence factor synthesis in staphylococci. Microbiol Mol Biol R 73 : 233 248.
118. Sonenshein AL (2007) Control of key metabolic intersections in Bacillus subtilis. Nat Rev Microbiol 5 : 917 927.
119. Strandén AM, Roos M Berger-Bächi B (1996) Glutamine synthetase and heteroresistance in methicillin-resistant Staphylococcus aureus. Microb Drug Resist 2 : 201 207.
120. Strösser J, Lüdke A, Schaffer S, Krämer R Burkovski A (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.
121. Stutz HE, Quixley KW, McMaster LD Reid SJ (2007) Co-regulation of the nitrogen-assimilatory gene cluster in Clostridium saccharobutylicum. Microbiology 153 : 3081 3090.
122. Tamura GS, Nittayajarn A Schoentag DL (2002) A glutamine transport gene, glnQ, is required for fibronectin adherence and virulence of group B streptococci. Infect Immun 70 : 2877 2885.
123. Tangney M, Galinier A, Deutscher J Mitchell WJ (2003) Analysis of the elements of catabolite repression in Clostridium acetobutylicum ATCC 824. J Mol Microb Biotech 6 : 6 11.
124. Tauch A, Kaiser O, Hain T et al 2005) Complete genome sequence and analysis of the multiresistant nosocomial pathogen Corynebacterium jeikeium K411, a lipid-requiring bacterium of the human skin flora. J Bacteriol 187 : 4671 4682.
125. Tauch A, Schneider J, Szczepanowski R et al 2008a) Ultrafast pyrosequencing of Corynebacterium kroppenstedtii DSM44385 revealed insights into the physiology of a lipophilic corynebacterium that lacks mycolic acids. J Biotechnol 136 : 22 30.
126. Tauch A, Trost E, Tilker A et al 2008b) The lifestyle of Corynebacterium urealyticum derived from its complete genome sequence established by pyrosequencing. J Biotechnol 136 : 11 21.
127. Tiffert Y, Supra P, Wurm R, Wohlleben W, Wagner R Reuther J (2008) The Streptomyces coelicolor GlnR regulon: identification of new GlnR targets and evidence for a central role of GlnR in nitrogen metabolism in actinomycetes. Mol Microbiol 67 : 861 880.
128. Titgemeyer F, Amon J, Parche S et al 2007) A genomic view of sugar transport in Mycobacterium smegmatis and Mycobacterium tuberculosis. J Bacteriol 189 : 5903 5915.
129. Tøndervik A, Torgersen HR, Botnmark HK Strøm AR (2006) Transposon mutations in the 5′ end of glnD, the gene for a nitrogen regulatory sensor, that suppress the osmosensitive phenotype caused by otsBA lesions in Escherichia coli. J Bacteriol 188 : 4218 4226.
130. Tremblay PL Hallenbeck PC (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.
131. Tullius MV, Harth G Horwitz MA (2001) High extracellular levels of Mycobacterium tuberculosis glutamine synthetase and superoxide dismutase in actively growing cultures are due to high expression and extracellular stability rather than to a protein-specific export mechanism. Infect Immun 69 : 6348 6363.
132. Tullius MV, Harth G Horwitz MA (2003) Glutamine synthetase GlnA1 is essential for growth of Mycobacterium tuberculosis in human THP-1 macrophages and guinea pigs. Infect Immun 71 : 3927 3936.
133. van Heeswijk WC, Stegeman B, Hoving S, Molenaar D, Kahn D Westerhoff HV (1995) An additional PII in Escherichia coli: a new regulatory protein in the glutamine synthetase cascade. FEMS Microbiol Lett 132 : 153 157.
134. van Heeswijk WC, Hoving S, Molenaar D, Stegeman B, Kahn D Westerhoff HV (1996) An alternative PII protein in the regulation of glutamine synthetase in Escherichia coli. Mol Microbiol 21 : 133 146.
135. van Heeswijk WC, Wen D, Clancy P, Jaggi R, Ollis DL, Westerhoff HV Vasudevan SG (2000) The Escherichia coli signal transducers PII (GlnB) and GlnK form heterotrimers in vivo: fine tuning the nitrogen signal cascade. P Natl Acad Sci USA 97 : 3942 3947.
136. van Heeswijk WC, Molenaar D, Hoving S Westerhoff HV (2009) The pivotal regulator GlnB of Escherichia coli is engaged in subtle and context-dependent control. FEBS J 276 : 3324 3340.
137. van Schaik W, Château A, Dillies MA, Coppée JY, Sonenshein AL Fouet A (2009) The global regulator CodY regulates toxin gene expression in Bacillus anthracis and is required for full virulence. Infect Immun 77 : 4437 4445.
138. Varga JJ, Stirewalt VL Melville SB (2004) The CcpA protein is necessary for efficient sporulation and enterotoxin gene (cpe) regulation in Clostridium perfringens. J Bacteriol 186 : 5221 5229.
139. Varga JJ, Therit B Melville SB (2008) Type IV pili and the CcpA protein are needed for maximal biofilm formation by the Gram-positive anaerobic pathogen Clostridium perfringens. Infect Immun 76 : 4944 4951.
140. Varmanen P, Savijoki K, Avall S, Palva A Tynkkynen S (2000) X-prolyl dipeptidyl aminopeptidase gene (pepX) is part of the glnRA operon in Lactobacillus rhamnosus. J Bacteriol 182 : 146 154.
141. Wagner M Horn M (2006) The Planctomycetes, verrucomicrobia, Chlamydiae and sister phyla comprise a superphylum with biotechnological and medical relevance. Curr Opin Biotech 17 : 241 249.
142. Walter B, Hänßler E, Kalinowski J Burkovski A (2007) Nitrogen metabolism and nitrogen control in corynebacteria: variations of a common theme. J Mol Microb Biotech 12 : 131 138.
143. Wang J Zhao GP (2009) GlnR positively regulates nasA transcription in Streptomyces coelicolor. Biochem Bioph Res Co 386 : 77 81.
144. Weiss V, Kramer G, Dünnebier T Flotho A (2002) Mechanism of regulation of the bifunctional histidine kinase NtrB in Escherichia coli. J Mol Microb Biotech 4 : 229 233.
145. Weisschuh N, Fink D, vierling S, Bibb MJ, Wohlleben W Engels A (2000) Transcriptional analysis of the gene for glutamine synthetase II and two upstream genes in Streptomyces coelicolor A3(2). Mol Gen Genet 264 : 461 469.
146. Wray LV Jr. Fisher SH (1993) The Streptomyces coelicolor glnR gene encodes a protein similar to other bacterial response regulators. Gene 130 : 145 150.
147. Wray LV Jr. Fisher SH (2008) Bacillus subtilis GlnR contains an autoinhibitory C-terminal domain required for the interaction with glutamine synthetase. Mol Microbiol 68 : 277 285.
148. Wray LV Jr., Atkinson MR Fisher SH (1991) Identification and cloning of the glnR locus, which is required for transcription of the glnA gene in Streptomyces coelicolor A3(2). J Bacteriol 173 : 7351 7360.
149. Wray LV Jr., Ferson AE, Rohrer K Fisher SH (1996) TnrA, a transcription factor required for global nitrogen regulation in Bacillus subtilis. P Natl Acad Sci USA 93 : 8841 8845.
150. Wray LV Jr., Ferson AE Fisher SH (1997) Expression of the Bacillus subtilis ureABC operon is controlled by multiple regulatory factors including CodY, GlnR, TnrA, and Spo0H. J Bacteriol 179 : 5494 5501.
151. Wray LV Jr., Zalieckas JM, Ferson AE Fisher SH (1998) Mutational analysis of the TnrA-binding sites in the Bacillus subtilis nrgAB and gabP promoter regions. J Bacteriol 180 : 2943 2949.
152. Yoshida K, Yamaguchi H, Kinehara M, Ohki YH, Nakaura Y Fujita Y (2003) Identification of additional TnrA-regulated genes of Bacillus subtilis associated with a TnrA box. Mol Microbiol 49 : 157 165.
153. Yoshida T, Qin L, Egger LA Inouye M (2006) Transcription regulation of ompF and ompC by a single transcription factor, OmpR. J Biol Chem 281 : 17114 17123.
154. Yu H, Peng WT, Liu Y, Wu T, Yao YF, Cui MX, Jiang WH Zhao GP (2006) Identification and characterization of glnA promoter and its corresponding trans-regulatory protein GlnR in the rifamycin SV producing actinomycete, Amycolatopsis mediterranei U32. Acta Bioch Bioph Sin 38 : 831 843.
155. Yu H, Yao Y, Liu Y, Jiao R, Jiang W Zhao GP (2007) A complex role of Amycolatopsis mediterranei GlnR in nitrogen metabolism and related antibiotics production. Arch Microbiol 188 : 89 96.
156. Zalieckas JM, Wray LV Jr. Fisher SH (2006) Cross-regulation of the Bacillus subtilis glnRA and tnrA genes provides evidence for DNA binding site discrimination by GlnR and TnrA. J Bacteriol 188 : 2578 2585.