1887

Abstract

In the filamentous cyanobacterium sp. strain PCC 7120, a starvation of combined nitrogen induces differentiation of heterocysts, cells specialized in nitrogen fixation. How do filaments perceive the limitation of the source of combined nitrogen, and what determines the proportion of heterocysts? In cyanobacteria, 2-oxoglutarate provides a carbon skeleton for the incorporation of inorganic nitrogen. Recently, it has been proposed that the concentration of 2-oxoglutarate reflects the nitrogen status in cyanobacteria. To investigate the effect of 2-oxoglutarate on heterocyst development, a heterologous gene encoding a 2-oxoglutarate permease under the control of a regulated promoter was expressed in sp. PCC 7120. The increase of 2-oxoglutarate within cells can trigger heterocyst differentiation in a subpopulation of filaments even in the presence of nitrate. In the absence of a source of combined nitrogen, it can increase heterocyst frequency, advance the timing of commitment to heterocyst development and further increase the proportion of heterocysts in a mutant. Here, it is proposed that the intracellular concentration of 2-oxoglutarate is involved in the determination of the proportion of the two cell types according to the carbon/nitrogen status of the filament.

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2003-11-01
2019-11-17
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References

  1. Buikema, W. J. & Haselkorn, R. ( 2001; ). Expression of the Anabaena hetR gene from a copper-regulated promoter leads to heterocyst differentiation under repressing conditions. Proc Natl Acad Sci U S A 98, 2729–2734.[CrossRef]
    [Google Scholar]
  2. Cai, Y. & Wolk, C. P. ( 1997; ). Anabaena sp. strain PCC 7120 responds to nitrogen deprivation with a cascade-like sequence of transcriptional activations. J Bacteriol 179, 267–271.
    [Google Scholar]
  3. Elhai, J. & Wolk, C. P. ( 1988; ). Conjugal transfer of DNA to cyanobacteria. Methods Enzymol 167, 747–754.
    [Google Scholar]
  4. Fadi Aldehni, M., Sauer, J., Spielhaupter, C., Schmid, R. & Forchhammer, K. ( 2003; ). Signal transduction protein PII is required for NtcA-regulated gene expression during nitrogen deprivation in the cyanobacterium Synechococcus elongatus strain PCC 7942. J Bacteriol 185, 2582–2591.[CrossRef]
    [Google Scholar]
  5. Forchhammer, K. & Hedler, A. ( 1997; ). Phosphoprotein PII from cyanobacteria – analysis of functional conservation with the PII signal-transduction protein from Escherichia coli. Eur J Biochem 244, 869–875.[CrossRef]
    [Google Scholar]
  6. Forchhammer, K. & Tandeau de Marsac, N. ( 1995; ). Phosphorylation of the PII protein (glnB gene product) in the cyanobacterium Synechococcus sp. strain PCC 7942: analysis of the in vitro kinase activity. J Bacteriol 177, 5812–5817.
    [Google Scholar]
  7. Frias, J. E., Flores, E. & Herrero, A. ( 1994; ). Requirement of the regulatory protein NtcA for the expression of nitrogen assimilation and heterocyst development genes in the cyanobacterium Anabaena sp. PCC 7120. Mol Microbiol 14, 823–832.[CrossRef]
    [Google Scholar]
  8. Ghassemian, M., Wong, B., Ferreira, F., Markley, J. L. & Straus, N. A. ( 1994; ). Cloning, sequencing and transcriptional studies of the genes for cytochrome c-553 and plastocyanin from Anabaena sp. PCC 7120. Microbiology 140, 1151–1159.[CrossRef]
    [Google Scholar]
  9. Hanson, T. E., Forchhammer, K., Tandeau de Marsac, N. & Meeks, J. C. ( 1998; ). Characterization of the glnB gene product of Nostoc punctiforme strain ATCC 29133: glnB or the PII protein may be essential. Microbiology 144, 1537–1547.[CrossRef]
    [Google Scholar]
  10. Herrero, A., Muro-Pastor, A. M. & Flores, E. ( 2001; ). Nitrogen control in cyanobacteria. J Bacteriol 183, 411–425.[CrossRef]
    [Google Scholar]
  11. Irmler, A., Sanner, S., Dierks, H. & Forchhammer, K. ( 1997; ). Dephosphorylation of the phosphoprotein PII in Synechococcus PCC 7942: identification of an ATP and 2-oxoglutarate-regulated phosphatase activity. Mol Microbiol 26, 81–90.[CrossRef]
    [Google Scholar]
  12. Kaneko, T., Nakamura, Y., Wolk, C. P. & 19 other authors ( 2001; ). Complete genomic sequence of the filamentous nitrogen-fixing cyanobacterium Anabaena sp. strain PCC 7120. DNA Res 8, 205–213.[CrossRef]
    [Google Scholar]
  13. Lee, H.-M., Vazquez-Bermudez, M. F. & Tandeau de Marsac, N. ( 1999; ). The global nitrogen regulator NtcA regulates transcription of the signal transducer PII (GlnB) and influences its phosphorylation level in response to nitrogen and carbon supplies in the cyanobacterium Synechococcus sp. strain PCC 7942. J Bacteriol 181, 2697–2702.
    [Google Scholar]
  14. Lee, M. H., Scherer, M., Rigali, S. & Golden, J. W. ( 2003; ). PlmA, a new member of the GntR family, has plasmid maintenance functions in Anabaena sp. strain PCC 7120. J Bacteriol 185, 4315–4325.[CrossRef]
    [Google Scholar]
  15. Luque, I., Flores, E. & Herrero, A. ( 1994; ). Molecular mechanism for the operation of nitrogen control in cyanobacteria. EMBO J 13, 2862–2869.
    [Google Scholar]
  16. Martin-Figueroa, E., Navarro, F. & Florencio, F. J. ( 2000; ). The GS–GOGAT pathway is not operative in the heterocysts. Cloning and expression of the glsF gene from the cyanobacterium Anabaena sp. PCC 7120. FEBS Lett 476, 282–286.[CrossRef]
    [Google Scholar]
  17. Meeks, J. C. & Elhai, J. ( 2002; ). Regulation of cellular differentiation in filamentous cyanobacteria in free-living and plant-associated symbiotic growth states. Microbiol Mol Biol Rev 66, 94–121.[CrossRef]
    [Google Scholar]
  18. Merrick, M. J. & Edwards, R. A. ( 1995; ). Nitrogen control in bacteria. Microbiol Rev 59, 604–622.
    [Google Scholar]
  19. Muro-Pastor, M. I., Reyes, J. C. & Florencio, F. J. ( 2001; ). Cyanobacteria perceive nitrogen status by sensing intracellular 2-oxoglutarate levels. J Biol Chem 276, 38320–38328.
    [Google Scholar]
  20. Muro-Pastor, A. M., Valladares, A., Flores, E. & Herrero, A. ( 2002; ). Mutual dependence of the expression of the cell differentiation regulatory protein HetR and the global nitrogen regulator NtcA during heterocyst development. Mol Microbiol 44, 1377–1385.[CrossRef]
    [Google Scholar]
  21. Ninfa, A. J., Jiang, P., Atkinson, M. R. & Peliska, J. A. ( 2000; ). Integration of antagonistic signals in the regulation of nitrogen assimilation in Escherichia coli. Curr Top Cell Regul 36, 31–75.
    [Google Scholar]
  22. Paz-Yepes, J., Flores, E. & Herrero, A. ( 2003; ). Transcriptional effects of the signal transduction protein PII (glnB gene product) on NtcA-dependent genes in Synechococcus sp. PCC 7942. FEBS Lett 543, 42–46.[CrossRef]
    [Google Scholar]
  23. Ruppert, U., Irmler, A., Kloft, N. & Forchhammer, K. ( 2002; ). The novel protein phosphatase PphA from Synechocystis PCC 6803 controls dephosphorylation of the signaling protein PII. Mol Microbiol 44, 855–864.[CrossRef]
    [Google Scholar]
  24. Senior, P. J. ( 1975; ). Regulation of nitrogen metabolism in Escherichia coli and Klebsiella aerogenes: studies with the continuous-culture technique. J Bacteriol 123, 407–418.
    [Google Scholar]
  25. Seol, W. & Shatkin, A. J. ( 1991; ). Escherichia coli kgtP encodes an alpha-ketoglutarate transporter. Proc Natl Acad Sci U S A 88, 3802–3806.[CrossRef]
    [Google Scholar]
  26. Seol, W. & Shatkin, A. J. ( 1992; ). Escherichia coli alpha-ketoglutarate permease is a constitutively expressed proton symporter. J Biol Chem 267, 6409–6413.
    [Google Scholar]
  27. Stanier, R. Y. & Cohen-Bazire, G. ( 1977; ). Phototrophic prokaryotes: the cyanobacteria. Annu Rev Microbiol 31, 225–274.[CrossRef]
    [Google Scholar]
  28. 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]
  29. Vazquez-Bermudez, M. F., Herrero, A. & Flores, E. ( 2000; ). Uptake of 2-oxoglutarate in Synechococcus strains transformed with the Escherichia coli kgtP gene. J Bacteriol 182, 211–215.[CrossRef]
    [Google Scholar]
  30. 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]
  31. Vazquez-Bermudez, M. F., Herrero, A. & Flores, E. ( 2003; ). 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, 155–159.[CrossRef]
    [Google Scholar]
  32. Wilcox, M., Mitchison, G. J. & Smith, R. J. ( 1973; ). Pattern formation in the blue-green algae Anabaena. II. Controlled proheterocyst regression. J Cell Sci 13, 637–649.
    [Google Scholar]
  33. Wolk, C. P. ( 2000; ). Heterocyst formation in Anabaena. In Prokaryotic Development, pp. 83–104. Edited by Y. V. Brun & L. J. Shimkets. Washington, DC: American Society for Microbiology.
  34. Wolk, C. P., Ernst, A. & Elhai, J. ( 1994; ). Heterocyst metabolism and development. In The Molecular Biology of Cyanobacteria, pp. 769–823. Edited by D. A. Bryant. Dordrecht: Kluwer.
  35. Yoon, H. S. & Golden, J. W. ( 1998; ). Heterocyst pattern formation controlled by a diffusible peptide. Science 282, 935–938.[CrossRef]
    [Google Scholar]
  36. Yoon, H. S. & Golden, J. W. ( 2001; ). PatS and products of nitrogen fixation control heterocyst pattern. J Bacteriol 183, 2605–2613.[CrossRef]
    [Google Scholar]
  37. Zhang, C.-C. ( 1993; ). A gene encoding a protein related to eukaryotic protein kinases from the filamentous heterocystous cyanobacterium Anabaena PCC 7120. Proc Natl Acad Sci U S A 90, 11840–11844.[CrossRef]
    [Google Scholar]
  38. Zhang, C.-C., Durand, M.-C., Jeanjean, R. & Joset, F. ( 1989; ). Molecular and genetical analysis of the fructose-glucose transport system in the cyanobacterium Synechocystis PCC6803. Mol Microbiol 3, 1221–1229.[CrossRef]
    [Google Scholar]
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