Global carbon/nitrogen control by PII signal transduction in cyanobacteria: From signals to targets

FEMS Microbiology Reviews

Volumn 28, Issue 3, 2004, Pages 319-333

  Forchhammer, Karl ^a  

^a JUSTUS LIEBIG UNIVERSITY   (Germany)

Author keywords

2 Oxoglutarate; GlnB; Nitrate transport; Nitrogen regulation; NtcA; Protein phosphatase; Protein phosphorylation

Indexed keywords

2 OXOGLUTARIC ACID; ADENOSINE TRIPHOSPHATE; BACTERIAL PROTEIN; CARBON; CARBON DIOXIDE; METHYLAMMONIUM; NITRATE; NITRITE; NITROGEN; PHOSPHOPROTEIN PHOSPHATASE; PROTEIN P II; RECEPTOR PROTEIN; SERINE; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

BACTERIAL STRAIN; CATALYSIS; CRYSTAL STRUCTURE; CYANOBACTERIUM; ESCHERICHIA COLI; GENE EXPRESSION; GENE SEQUENCE; MOLECULAR WEIGHT; MUTANT; NOMENCLATURE; NONHUMAN; PLANT; PROCHLORALES; PROTEIN BINDING; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; SYNECHOCOCCUS; SYNECHOCYSTIS;

BACTERIAL PROTEINS; CARBON; CYANOBACTERIA; ESCHERICHIA COLI PROTEINS; KETOGLUTARIC ACIDS; MODELS, BIOLOGICAL; NITROGEN; OXIDATION-REDUCTION; PHOSPHOPROTEIN PHOSPHATASE; PHOTOSYSTEM II PROTEIN COMPLEX; PII NITROGEN REGULATORY PROTEINS; PROTEIN KINASES; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

BACTERIA (MICROORGANISMS); CYANOBACTERIA; SYNECHOCOCCUS; SYNECHOCYSTIS;

EID: 2642530192     PISSN: 01686445     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.femsre.2003.11.001     Document Type: Review

References (94)

1. Kaneko T., Nakamura Y., Wolk C.P., Kuritz T., Sasamoto S., Watanabe A., Iriguchi M., Ishikawa A., Kawashima K., Kimura T., Kishida Y., Kohara M., Matsumoto M., Matsuno A., Muraki A., Nakazaki N., Shimpo S., Sugimoto M., Takazawa M., Yamada M., Yasuda M., Tabata S. Complete genomic sequence of the filamentous nitrogen-fixing cyanobacterium Anabaena sp. strain PCC 7120. DNA Res. 8:2001;205-213
2. Meeks J.C., Elhai J., Thiel T., Potts M., Larimer F., Lamerdin J., Predki P., Atlas R. An overview of the genome of Nostoc punctiforme, a multicellular, symbiotic cyanobacterium. Photosynthesis Res. 70:2001;85-106
3. Wang L., Sun Y.-P., Chen W.-L., Li J.-H., Zhang C.-C. Genomic analysis of protein kinases, protein phosphatases and two-component regulatory systems of the cyanobacterium Anabaena sp. strain PCC 7120. FEMS Microbiol. Lett. 217:2002;155-165
4. II signal transduction proteins: pivotal players in microbial nitrogen control. Microbiol. Mol. Biol. Rev. 65:2001;80-105
5. II signal transduction proteins. Trends Microbiol. 8:2000;172-179
6. Shapiro B.M. The glutamine synthetase deadenylylating enzyme system from Escherichia coli: resolution into two components, specific nucleotide stimulation and cofactor requirements. Biochemistry. 8:1969;659-670
7. Stadtman E.R. Discovery of glutamine synthetase cascade. Methods Enzymol. 182:1990;793-809
8. Stadtman E.R. The story of glutamine synthetase regulation. J. Biol. Chem. 276:2001;44357-44364
9. II-homologue: structure reveals ATP binding site and indicates how the T-loop may be involved in molecular recognition. J. Mol. Biol. 282:1998;149-165
10. II-ATP complex. Eur. J. Biochem. 268:2001;2028-2037
11. Kamberov E.S., Atkinson M.A., Ninfa A.J. The Escherichia coli signal transduction protein is activated upon binding 2-ketoglutarate and ATP. J. Biol. Chem. 270:1995;17797-17807
12. II protein. Biochemistry. 37:1998;12782-12794
13. II is structurally similar to the enteric GlnK. Eur. J. Biochem. 269:2002;3296-3303
14. II protein and nucleotide sequence of its structural gene. J. Biol. Chem. 262:1987;8690-8695
15. Atkinson M., Ninfa A. Characterization of the GlnK protein of Escherichia coli. Mol. Microbiol. 32:1999;301-313
16. II from Escherichia coli. FEBS Lett. 391:1996;223-228
17. II regulatory protein and the uridylyltransferase-uridylylremoving enzyme. J. Biol. Chem. 250:1975;6264-6272
18. Liu J., Magasanik B. The glnB region of the Escherichia coli chromosome. J. Bacteriol. 175:1993;7441-7449
19. Atkinson M.A., Blauwkamp T.A., Bondarenko V., Studistky V., Ninfa A.J. Activation of the glnA, glnK and nac promoters as Escherichia coli undergoes the transition from nitrogen excess growth to nitrogen starvation. J. Bacteriol. 184:2002;5358-5363
20. Maheswaran M., Forchhammer K. Carbon-source-dependent nitrogen regulation in Escherichia coli is mediated through glutamine-dependent GlnB signalling. Microbiology. 149:2003;2163-2172
21. II, regulates transcription of the glnALG operon in Escherichia coli. Proc. Natl. Acad. Sci. USA. 83:1986;5909-5913
22. Jiang P., Peliska J.A., Ninfa A. Reconstitution of the signal-transduction bicyclic cascade responsible for the regulation of Ntr gene transcription in Escherichia coli. Biochemistry. 37:1998;12795-12801
23. II signal transduction protein. J. Bacteriol. 181:1999;1906-1911
24. Bueno R., Pahel G., Magasanik B. Role of glnB and glnD gene products in regulation of the glnALG operon of Escherichia coli. J. Bacteriol. 164:1985;816-822
25. Rhee S.G., Chock P.B., Stadtman E.R. Glutamine synthetase from Escherichia coli. Methods Enzymol. 113:1985;213-241
26. Jiang P., Peliska J.A., Ninfa A. The regulation of Escherichia coli glutamine synthetase revisited: role of 2-ketoglutarate in the regulation of glutamine synthetase adenylylation state. Biochemistry. 37:1998;12802-12810
27. Jaggi R., van Heeswijk W.C., Westerhoff H.V., Ollis D.L., Vasudevan S.G. The two opposing activities of adenylyltransferase reside in distinct homologous domains, with intramolecular signal transduction. EMBO J. 16:1997;5562-5571
28. Coutts G., Thomas G., Blakey D., Merrick M. Membrane sequestration of the signal transduction protein GlnK by the ammonium transporter AmtB. EMBO J. 21:2002;536-545
29. II signalling by the AmtB protein of Escherichia coli. Mol. Microbiol. 48:2003;1017-1028
30. Ninfa A.J., Jiang P., Atkinson M.R., Peliska J.A. Integration of antagonistic signals in the regulation of nitrogen assimilation in Escherichia coli. Curr. Top. Cell Regul. 36:2000;31-75
31. Hesketh A., Fink D., Gust B., Rexer H.-U., Scheel B., Chater K., Wohlleben W., Engels A. The GlnD and GlnK homologues of Streptomyces coelicolor A3(2) are functionally dissimilar to their nitrogen regulatory system counterparts from enteric bacteria. Mol. Microbiol. 46:2002;319-330
32. Detsch C., Stülke J. Ammonium utilization in Bacillus subtilis: transport and regulatory functions of NrgA and NrgB. Microbiology. 149:2003;3289-3297
33. Arcondeguy T., Lawson D., Merrick M. Two residues in the T-loop of GlnK determine NifL-dependent nitrogen control of nif-gene expression. J. Biol. Chem. 275:2000;38452-38456
34. II in Azospirillum brasiliense: evidence for a regulatory role of the NifA N-terminal domain. J. Bacteriol. 178:1996;4830-4838
35. Pawlowski A., Riedel K-U., Klipp W., Dreiskemper P., Groß S., Bierhoff H., Drepper T., Masepohl B. Yeast two-hybrid studies on interaction of proteins involved in regulation of nitrogen fixation in the phototrophic bacterium Rhodobacter capsulatus. J. Bacteriol. 185:2003;5240-5247
36. Little R., Colombo V., Leech A., Dixon R. 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. 277:2002;15472-15481
37. Hallenbeck P.C. Mutations affecting nitrogenase switch-off in Rhodobacter capsulatus. Biochem. Biophys. Acta. 1118:1992;161-168
38. Inoue K., Alsina J., Chen J., Inouye M. Suppression of defective ribosome assembly in a rbfA deletion mutant by overexpression of Era, an essential GTPase in Escherichia coli. Mol. Microbiol. 48:2003;1005-1016
39. Sanders C.E., Melis A., Allen J.F. In vivo phosphorylation of proteins in the cyanobacterium Synechococcus 6301 after chromatic acclimation to Photosystem I or Photosystem II light. Biochim. Biophys. Acta. 976:1989;168-172
40. Harrison M.A., Keen J.N., Findlay J.B., Allen J.F. Modification of a glnB-like gene product by photosynthetic electron transport in the cyanobacterium Synechococcus 6301. FEBS Lett. 264:1990;25-28
41. Tsinoremas N.F., Castets A.M., Harrison M.A., Allen J.F., Tandeau de Marsac N. Photosynthetic electron transport controls nitrogen assimilation in cyanobacteria by means of post-translational modification of the glnB gene product. Proc. Natl. Acad. Sci. USA. 88:1991;4565-4569
42. II protein in the cyanobacterium Synechococcus sp. strain PCC7942 is modified by serine phosphorylation and signals the cellular N-status. J. Bacteriol. 176:1994;84-91
43. II protein (glnB gene product) in the cyanobacterium Synechococcus sp. strain PCC 7942: analysis of in vitro kinase activity. J. Bacteriol. 177:1995;5812-5817
44. II protein) in the cyanobacterium Synechocystis PCC 6803. Plant Mol. Biol. 35:1997;723-734
45. II protein may be essential. Microbiology. 144:1998;1537-1547
46. II protein in response to nitrogen availability in filamentous heterocystous cyanobacteria Anabaena sp. PCC 7120. Pedrosa F.O., Hungria M., Yates G., Newton W.A. Nitrogen Fixation: From Molecules to Crop Productivity. 2000;107 Kluwer Academic, Dordrecht, NL
47. Partensky F., Hess W.R., Vaulot D. Prochlorococcus, a marine photosynthetic prokaryote of global significance. Microbiol. Mol. Biol. Rev. 63:1999;106-127
48. Dufresne A., Salanoubat M., Partensky F., Artiguenave F., Axmann I.M., Barbe V., Duprat S., Galperin M.Y., Koonin E.V., Le Gall F., Makarova K.S., Ostrowski M., Oztas S., Robert C., Rogozin I.B., Scanlan D.J., Tandeau de Marsac N., Weissenbach J., Wincker P., Wolf Y.I., Hess W.R. Genome sequence of the cyanobacterium Prochlorococcus marinus SS120, a nearly minimal oxyphototrophic genome. Proc. Natl. Acad. Sci. USA. 100:2003;10020-10025
49. II and bicarbonate aquisition in Prochlorococcus marinus PCC 9511, a marine cyanobacterium naturally deficient in nitrate and nitrite assimilation. Microbiology. 148:2002;2405-2412
50. II-like protein in Arabidopsis: putative role in nitrogen sensing. Proc. Natl. Acad. Sci. USA. 95:1998;13965-13970
51. Reith M.E., Munholland J. Complete sequence of the Porphyra purpurea chloroplast genome. Plant Mol. Biol. Rep. 13:1995;333-335
52. II? Plant Physiol. 133:2003;1-7
53. II from Arabidopsis thaliana. Plant J. 33:2003;353-360
54. II from the cyanobacterium Synechococcus sp. strain PCC 7942. J. Bacteriol. 177:1995;2033-2040
55. II in Synechococcus PCC 7942: identification of an ATP and 2-oxoglutarate-regulated phosphatase activity. Mol. Microbiol. 26:1997;81-90
56. II regulates both inorganic carbon and nitrate uptake and is modified by a redox signal in Synechocystis PCC 6803. FEBS Lett. 463:1999;216-220
57. II signal transduction protein from Escherichia coli. Eur. J. Biochem. 244:1997;869-875
58. II protein in Synechococcus PCC 7942 senses and signals 2-oxoglutarate under ATP-replete conditions. Peschek G., Löffelhardt W., Schmetterer G. The Phototrophic Prokaryotes. 1999;549-553 Kluwer Academic, New York, NY
59. Shi L., Potts M., Kenelly M. The serine, threonine, and/or tyrosine-specific protein kinases and protein phosphatases of prokaryotic organisms: a family portrait. FEMS Microbiol. Rev. 22:1998;229-253
60. Zhang C.C., Gonzalez L., Phalip V. Survey, analysis and genetic organization of genes encoding eukaryotic-like signaling proteins on a cyanobacterial genome. Nucleic Acids Res. 26:1998;3619-3625
61. II signalling protein in the cyanobacterium Synechocystis PCC 6803. Proc. Natl. Acad. Sci. USA. 98:2001;12978-12983
62. Kaneko T., Sato S., Kotani H., Tanaka A., Asamizu E., Nakamura Y., Miyajima N., Hirosawa M., Sugiura M., Sasamoto S., Kimura T., Hosouchi T., Matsuno A., Muraki A., Nakazaki N., Naruo K., Okumura S., Shimpo S., Takeuchi C., Wada T., Watanabe A., Yamada M., Yasuda M., Tabata S. Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC 6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res. 30:1996;109-136
63. Treuner-Lange A., Ward M.J., Zusman D.R. Pph1 from Myxococcus xanthus is a protein phosphatase involved in vegetative growth and development. Mol. Microbiol. 40:2001;126-140
64. II. Mol. Microbiol. 44:2002;855-864
65. II signalling in unicellular cyanobacteria: involvement of redox-signals, energy charge and metabolites. Physiol. Plantarm. 120:2004;51-56
66. II proteins from the cyanobacteria Synechococcus sp. PCC 7942 and Synechocystis sp. PCC 6803. Acta Cryst. D. 59:2003;2183-2190
67. II-mediated signal transduction systems. Mol. Microbiol. 33:1999;338-349
68. II in the control of nitrate/nitrite uptake in a cyanobacterium. FEBS Lett. 427:1998;291-295
69. II-mediated regulation of nitrate and nitrite uptake in the cyanobacterium Synechococcus sp. PCC 7942. Eur. J. Biochem. 267:2000;591-600
70. Kobayashi M., Rodriguez R., Lara C., Omata T. Involvement of th C-terminal domain of the ATP-binding subunit in the regulation of the ABC-type nitrate/nitrite transporter of the cyanobacterium Synechococcus sp. strain PCC 7942. J. Biol. Chem. 272:1997;21297-27201
71. Rodriguez R., Kobayashi M., Omata T., Lara C. Independence of carbon and nitrogen control in the posttranslational regulation of nitrate transport in the cyanobacterium Synechococcus sp. strain PCC 7942. FEBS Lett. 432:1998;207-212
72. Vazquez-Bermudez M.F., Paz-Yepes J., Herrero A., Flores E. The NtcA activated amt1 gene encodes a permease required for uptake of low concentrations of ammonium in the cyanobacterium Synechococcus sp. PCC 7942. Microbiology. 148:2002;861-869
73. II-like signal transmitter proteins and amtB in regulation of nif gene expression, nitrogenase activity, and posttranslational modification of NifH in Azoarcus sp. Strain BH 72. J. Bacteriol. 184:2002;2251-2259
74. 2 uptake systems in cyanobacteria: Genes involved and their phylogenetic relationship with homologous genes in other organisms. Proc. Natl. Acad. Sci. USA. 98:2001;11789-11794
75. Luque I., Flores E., Herrero A. Molecular mechanism for the operation of nitrogen control in cyanobacteria. EMBO J. 13:1994;2862-2869
76. Muro-Pastor A.M., Valladares A., Flores E., Herrero A. Mutual dependence of the expression of the cell differentiation regulatory protein HetR and the global nitrogen regulator NtcA during heterocyst development. Mol. Microbiol. 44:2002;1377-1385
77. Meeks J.C., Elhai J. Regulation of cellular differentiation in filamentous cyanobacteria in free-living and plant-associated symbiotic growth states. Microbiol. Mol. Biol. Rev. 66:2002;94-121
78. Wolk C.P. Heterocyst formation in Anabaena. Brun Y.V., Shimkets L.J. Prokaryotic Development. 2000;83-104 American Society for Microbiology, Washington, DC
79. Herrero A., Muro-Pastor A.M., Flores E. Nitrogen control in cyanobacteria. J. Bacteriol. 183:2001;411-425
80. II (GlnB) and influences its phosphorylation level in response to nitrogen and carbon supplies in the cyanobacterium Synechococcus sp. strain PCC 7942. J. Bacteriol. 181:1999;2697-2702
81. Sauer J., Görl M., Forchhammer K. Nitrogen starvation in Synechococcus PCC 7942: involvement of glutamine synthetase and NtcA in phycobiliprotein degradation and survival. Arch. Microbiol. 172:1999;247-255
82. Crespo J.L., Garcia-Dominguez M., Florencio F.J. Nitrogen control of the glnN gene that codes for GS type III, the only glutamine synthetase in the cyanobacterium Pseudoanabaena sp. PCC 6903. Mol. Microbiol. 30:1998;1101-1112
83. Sauer J., Dirmeier U., Forchhammer K. The Synechococcus strain PCC 7942 glnN product (glutamine synthetase III) helps recovery from prolonged nitrogen chlorosis. J. Bacteriol. 182:2000;5612-5619
84. Reyes J.C., Muro-Pastor M.I., Florencio F.J. Transcription of glutamine synthetase genes (glnA and glnN) from the cyanobacterium Synechocystis sp. strain PCC 6803 is differently regulated in response to nitrogen availability. J. Bacteriol. 179:1997;2678-2689
85. II is required for NtcA-regulated gene expression during nitrogen deprivation in the cyanobacterium Synechococcus elongatus strain PCC 7942. J. Bacteriol. 185:2002;2582-2591
86. II (glnB gene product) on NtcA-dependent genes in Synechococcus sp. PCC 7942. FEBS Lett. 543:2003;42-46
87. II protein in response to carbon and nitrogen availability in filamentous heterocystous cyanobacteria. FEMS Microbiol. Lett. 144:1996;185-190
88. Gonzalez L., Phalip V., Zhang C.-C. Characterization of PknC, a Ser/Thr kinase with broad substrate specificity from the cyanobacterium Anabaena sp. strain PCC 7120. Eur. J. Biochem. 268:2001;1869-1875
89. Tandeau de Marsac N., Lee H.M. Regulation of carbon and nitrogen metabolism in the unicellular cyanobacterium Synechococcus spp. Peschek G., Löffelhardt W., Schmetterer G. The Phototrophic Prokaryotes. 1999;539-548 Kluwer Academic, New York, NY
90. Muro-Pastor M.I., Reyes J.C., Florencio F.J. Cyanobacteria perceive nitrogen status by sensing intracellular 2-oxoglutarate levels. J. Biol. Chem. 276:2001;38320-38328
91. +- isocitrate dehydrogenase gene (icd) is nitrogen regulated in cyanobacteria. J. Bacteriol. 178:1996;4070-4076
92. Vazquez-Bermudez M.F., Herrero A., Flores E. 2-Oxoglutarate increases the binding affinity of the NtcA (nitrogen control) transcription factor for the Synechococcus glnA promotor. FEBS Lett. 512:2002;71-74
93. Tanigawa R., Shirokane M., Maeda S.-i., Omata T., Tanaka K., Takahashi H. Transcriptional activation of NtcA-dependent promotors of Synechococcus sp. PCC 7942 by 2-oxoglutarate in vitro. Proc. Natl. Acad. Sci. USA. 99:2002;4251-4255
94. Vazquez-Bermudez M.F., Herrero A., Flores E. Carbon supply and 2-oxoglutarate effects on expression of nitrate reductase and nitrogen-regulated genes in Synechococcus sp. strain PCC 7942. FEMS Microbiol. Lett. 221:2003;155-159