1887

Abstract

The sp. PCC 7942 nitrogen regulator PipX interacts in a 2-oxoglutarate-dependent manner with the global nitrogen transcription factor NtcA and the signal transduction protein P. , PipX is involved in the NtcA-dependent induction of and genes. To further investigate the extent to which PipX is involved in global nitrogen control, the effect of inactivation on various nitrogen-regulated processes was determined. The PipX-deficient mutant was able to use nitrate as a nitrogen source and to efficiently inhibit the nitrate transport upon ammonium addition but showed decreased nitrate and nitrite reductase activities and a delay in the induction of nitrate utilization after transfer of cultures from ammonium- to nitrate-containing media. In contrast to the wild-type, glutamine synthetase activity was not upregulated upon depletion of combined nitrogen from cultures of the mutant strain. Inactivation of impaired induction of and delayed phycobilisome degradation, but did not affect recovery of nitrogen-deprived cultures. Taken together, the results indicate that PipX interacts with NtcA to facilitate efficient acclimation of cyanobacteria to conditions of nitrogen limitation.

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2007-03-01
2024-11-01
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References

  1. Aichi M., Maeda S., Ichikawa K., Omata T. 2004; Nitrite-responsive activation of the nitrate assimilation operon in cyanobacteria plays an essential role in up-regulation of nitrate assimilation activities under nitrate-limited growth conditions. J Bacteriol 186:3224–3229 [CrossRef]
    [Google Scholar]
  2. Andersson C. R., Tsinoremas N. F., Shelton J., Lebedeva N. V., Yarrow J., Min H., Golden S. S. 2000; Application of bioluminescence to the study of circadian rhythms in cyanobacteria. Methods Enzymol 305:527–542
    [Google Scholar]
  3. Arcondeguy T., Jack R., Merrick M. 2001; P(II) signal transduction proteins, pivotal players in microbial nitrogen control. Microbiol Mol Biol Rev 65:80–105 [CrossRef]
    [Google Scholar]
  4. Bender R. A., Janssen K. A., Resnick A. D., Blumenberg M., Foor F., Magasanik B. 1977; Biochemical parameters of glutamine synthetase from Klebsiella aerogenes . J Bacteriol 129:1001–1009
    [Google Scholar]
  5. Burillo S., Luque I., Fuentes I., Contreras A. 2004; Interactions between the nitrogen signal transduction protein PII and N -acetyl glutamate kinase in organisms that perform oxygenic photosynthesis. J Bacteriol 186:3346–3354 [CrossRef]
    [Google Scholar]
  6. Chen Y. M., Ferrar T. S., Lohmeir-Vogel E., Morrice N., Mizuno Y., Berenger B., Ng K. K., Muench D. G., Moorhead G. B. 2006; The PII signal transduction protein of Arabidopsis thaliana forms an arginine-regulated complex with plastid N -acetyl glutamate kinase. J Biol Chem 281:5726–5733
    [Google Scholar]
  7. Elhai J., Vepritskiy A., Muro-Pastor A. M., Flores E., Wolk C. P. 1997; Reduction of conjugal transfer efficiency by three restriction activities of Anabaena sp. strain PCC 7120. J Bacteriol 179:1998–2005
    [Google Scholar]
  8. Espinosa J., Forchhammer K., Burillo S., Contreras A. 2006; Interaction network in cyanobacterial nitrogen regulation: PipX, a protein that interacts in a 2-oxoglutarate dependent manner with PII and NtcA. Mol Microbiol 61:457–469 [CrossRef]
    [Google Scholar]
  9. Figurski D. H., Helinski D. R. 1979; Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans . Proc Natl Acad Sci U S A 76:1648–1652 [CrossRef]
    [Google Scholar]
  10. Forchhammer K. 2004; Global carbon/nitrogen control by PII signal transduction in cyanobacteria: from signals to targets. FEMS Microbiol Rev 28:319–333 [CrossRef]
    [Google Scholar]
  11. Hanahan D. 1985; Techniques for transformation of Escherichia coli . In DNA Cloning pp 109–135 Edited by Glover D. M. Oxford, UK: IRL Press;
    [Google Scholar]
  12. Heinrich A., Maheswaran M., Ruppert U., Forchhammer K. 2004; The Synechococcus elongatus PII signal transduction protein controls arginine synthesis by complex formation with N -acetyl-l-glutamate kinase. Mol Microbiol 52:1303–1314 [CrossRef]
    [Google Scholar]
  13. Herrero A., Guerrero M. G. 1986; Regulation of nitrite reductase in the cyanobacterium Anacystis nidulans . J Gen Microbiol 132:2463–2468
    [Google Scholar]
  14. Herrero A., Flores E., Guerrero M. G. 1985; Regulation of nitrate reductase cellular levels in the cyanobacteria Anabaena variabilis and Synechocystis sp. FEMS Microbiol Lett 26:21–25 [CrossRef]
    [Google Scholar]
  15. Herrero A., Muro-Pastor A. M., Flores E. 2001; Nitrogen control in cyanobacteria. J Bacteriol 183:411–425 [CrossRef]
    [Google Scholar]
  16. Kappell A. D., Bhaya D., van Waasbergen L. G. 2006; Negative control of the high light-inducible hliA gene and implications for the activities of the NblS sensor kinase in the cyanobacterium Synechococcus elongatus strain PCC 7942. Arch Microbiol 186:403–413 [CrossRef]
    [Google Scholar]
  17. Kloft N., Forchhammer K. 2005; Signal transduction protein PII phosphatase PphA is required for light-dependent control of nitrate utilization in Synechocystis sp. strain PCC 6803. J Bacteriol 187:6683–6690 [CrossRef]
    [Google Scholar]
  18. Lee H. M., Flores E., Herrero A., Houmard J., Tandeau de Marsac N. 1998; A role for the signal transduction protein PII in the control of nitrate/nitrite uptake in a cyanobacterium. FEBS Lett 427:291–295 [CrossRef]
    [Google Scholar]
  19. Lee H. M., Flores E., Forchhammer K., Herrero A., Tandeau De Marsac N. 2000; Phosphorylation of the signal transducer PII protein and an additional effector are required for the PII-mediated regulation of nitrate and nitrite uptake in the cyanobacterium Synechococcus sp. PCC 7942. Eur J Biochem 267:591–600 [CrossRef]
    [Google Scholar]
  20. Luque I., Zabulon G., Contreras A., Houmard J. 2001; Convergence of two global transcriptional regulators on nitrogen induction of the stress-acclimation gene nblA in the cyanobacterium Synechococcus sp. PCC 7942. Mol Microbiol 41:937–947
    [Google Scholar]
  21. Mackinney G. 1941; Absorption of light by chlorophyll solutions. J Biol Chem 140:315–322
    [Google Scholar]
  22. Maeda S., Kawaguchi Y., Ohe T. A., Omata T. 1998; cis -acting sequences required for NtcB-dependent, nitrite-responsive positive regulation of the nitrate assimilation operon in the cyanobacterium Synechococcus sp. strain PCC 7942. J Bacteriol 180:4080–4088
    [Google Scholar]
  23. Maheswaran M., Urbanke C., Forchhammer K. 2004; Complex formation and catalytic activation by the PII signaling protein of N -acetyl-l-glutamate kinase from Synechococcus elongatus strain PCC 7942. J Biol Chem 279:55202–55210 [CrossRef]
    [Google Scholar]
  24. Muro-Pastor M. I., Reyes J. C., Florencio F. J. 2005; Ammonium assimilation in cyanobacteria. Photosynth Res 83:135–150 [CrossRef]
    [Google Scholar]
  25. Ninfa A. J., Jiang P. 2005; PII signal transduction proteins: sensors of alpha-ketoglutarate that regulate nitrogen metabolism. Curr Opin Microbiol 8:168–173 [CrossRef]
    [Google Scholar]
  26. Osanai T., Sato S., Tabata S., Tanaka K. 2005; Identification of PamA as a PII-binding membrane protein important in nitrogen-related and sugar-catabolic gene expression in Synechocystis sp. PCC 6803. J Biol Chem 280:34684–34690 [CrossRef]
    [Google Scholar]
  27. Sauer J., Gorl M., Forchhammer K. 1999; Nitrogen starvation in Synechococcus PCC 7942: involvement of glutamine synthetase and NtcA in phycobiliprotein degradation and survival. Arch Microbiol 172:247–255 [CrossRef]
    [Google Scholar]
  28. Sauer J., Dirmeier U., Forchhammer K. 2000; The Synechococcus strain PCC 7942 glnN product (glutamine synthetase III) helps recovery from prolonged nitrogen chlorosis. J Bacteriol 182:5615–5619 [CrossRef]
    [Google Scholar]
  29. Schwarz R., Forchhammer K. 2005; Acclimation of unicellular cyanobacteria to macronutrient deficiency: emergence of a complex network of cellular responses. Microbiology 151:2503–2514 [CrossRef]
    [Google Scholar]
  30. Schwarz R., Grossman A. R. 1998; A response regulator of cyanobacteria integrates diverse environmental signals and is critical for survival under extreme conditions. Proc Natl Acad Sci U S A 95:11008–11013 [CrossRef]
    [Google Scholar]
  31. Snell F. D., Snell C. T. 1949 Colorimetric Methods of Analysis pp 804–805 New York: Van Nostrand;
    [Google Scholar]
  32. Sugiyama K., Hayakawa T., Kudo T., Ito T., Yamaya T. 2004; Interaction of N -acetylglutamate kinase with a PII-like protein in rice. Plant Cell Physiol 45:1768–1778 [CrossRef]
    [Google Scholar]
  33. Takatani N., Kobayashi M., Maeda S., Omata T. 2006; Regulation of nitrate reductase by non-modifiable derivatives of PII in the cells of Synechococcus elongatus strain PCC 7942. Plant Cell Physiol 47:1182–1186 [CrossRef]
    [Google Scholar]
  34. Tanigawa R., Shirokane M., Maeda Si S., Omata T., Tanaka K., Takahashi H. 2002; Transcriptional activation of NtcA-dependent promoters of Synechococcus sp. PCC 7942 by 2-oxoglutarate in vitro. Proc Natl Acad Sci U S A 99:4251–4255 [CrossRef]
    [Google Scholar]
  35. Vazquez-Bermudez M. F., Herrero A., Flores E. 2002; 2-Oxoglutarate increases the binding affinity of the NtcA (nitrogen control) transcription factor for the Synechococcus glnA promoter. FEBS Lett 512:71–74 [CrossRef]
    [Google Scholar]
  36. Vega-Palas M. A., Madueno F., Herrero A., Flores E. 1990; Identification and cloning of a regulatory gene for nitrogen assimilation in the cyanobacterium Synechococcus sp. strain PCC 7942. J Bacteriol 172:643–647
    [Google Scholar]
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