1887

Abstract

The inactivation of (), a gene encoding a protein Ser/Thr kinase in PCC 6803, led to a pleiotropic phenotype of the SpkD null mutant. This mutant is impaired in its growth ability under low concentration of inorganic carbon (C), though its C-uptake system is not affected. Addition of glucose, phosphoglyceraldehyde or pyruvate does not allow the mutant to grow under low-C conditions. In contrast, this growth defect can be restored when the low-C culture medium is supplemented with metabolites of the TCA cycle. Growth of the mutant is also inhibited when ammonium is provided as nitrogen source, whatever the carbon regime of the cells, due to the high demand for 2-oxoglutarate, which is the carbon skeleton for ammonium assimilation. When mutant cells are cultured under standard growth conditions, the intracellular concentration of 2-oxoglutarate is 20 % lower than is observed in the wild-type strain. However, this decrease of 2-oxoglutarate level only slightly affects the phosphorylation state of PII, a protein that regulates nitrogen and carbon metabolism according to the intracellular levels of 2-oxoglutarate. Properties of the SpkD mutant suggest that the Ser/Thr kinase SpkD could be involved in adjusting the pool of the TCA cycle metabolites according to C supply in the culture medium.

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2008-07-01
2019-10-13
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References

  1. Bédu, S., Pozuelos, P., Cami, B. & Joset, F. ( 1995; ). Uptake of inorganic carbon in the cyanobacterium Synechocystis PCC 6803: physiological and genetic evidence for a high-affinity uptake system. Mol Microbiol 18, 559–568.[CrossRef]
    [Google Scholar]
  2. Beuf, L., Bedu, S., Durand, M. C. & Joset, F. ( 1994; ). A protein involved in co-ordinated regulation of inorganic carbon and glucose metabolism in the facultative photoautotrophic cyanobacterium Synechocystis PCC 6803. Plant Mol Biol 25, 855–864.[CrossRef]
    [Google Scholar]
  3. Chollet, R. ( 1996; ). Phosphoenolpyruvate carboxylase: a ubiquitous, highly regulated enzyme in plants. Annu Rev Plant Physiol Plant Mol Biol 47, 273–298.[CrossRef]
    [Google Scholar]
  4. Collier, J. L. & Grossman, A. R. ( 1992; ). Chlorosis induced by nutrient deprivation in Synechococcus sp. strain PCC 7942: not all bleaching is the same. J Bacteriol 174, 4718–4726.
    [Google Scholar]
  5. Coleman, J. R. & Colman, B. ( 1981; ). Photosynthetic carbon assimilation in the blue green algae, Coccochloris peniocystis. Plant Cell Environ 4, 285–290.
    [Google Scholar]
  6. Colman, B., Cheng, K. H. & Ingle, R. K. ( 1976; ). The relative activities of PEP carboxylase and RuDP carboxylase in blue-green algae. Plant Sci Lett 6, 123–127.[CrossRef]
    [Google Scholar]
  7. Durocher, D., Taylor, I. A., Sarbossova, D., Haire, L. F., Westcott, S. L., Jackson, S. P., Smerdon, S. J. & Yaffe, M. B. ( 2000; ). The molecular basis of FHA domain: phosphopeptide binding specificity and implications for phospho-dependent signalling mechanisms. Mol Cell 6, 1169–1182.[CrossRef]
    [Google Scholar]
  8. Eisenhut, M., Aguirre von Wobeser, E., Jonas, J., Shubert, H., Ibelings, B. W., Bauwa, H., Mattijs, H. & Hagemann, M. ( 2007; ). Long-term response toward inorganic carbon limitation in the wild type and glycolate turnover mutants of the cyanobacterium Synechocystis sp. strain PCC 6803. Plant Physiol 144, 1946–1959.[CrossRef]
    [Google Scholar]
  9. 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]
  10. Forchhammer, K. & Tandeau de Marsac, N. ( 1994; ). The PII protein in the cyanobacterium Synechococcus sp. strain PCC 7942 is modified by serine phosphorylation and signals the cellular N-status. J Bacteriol 176, 84–91.
    [Google Scholar]
  11. Herrero, A., Muro-Pastor, A. M. & Flores, E. ( 2001; ). Nitrogen control in cyanobacteria. J Bacteriol 183, 411–425.[CrossRef]
    [Google Scholar]
  12. Hisbergues, M., Jeanjean, R., Joset, F., Tandeau de Marsac, N. & Bédu, S. ( 1999; ). Protein PII regulates both inorganic carbon and nitrate uptake and is modified by a redox signal in Synechocystis PCC 6803. FEBS Lett 463, 216–220.[CrossRef]
    [Google Scholar]
  13. 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]
  14. Kamei, A., Yuasa, T., Orikawa, K., Geng, X. & Ikeuchi, M. ( 2001; ). A eukaryotic-type protein kinase, SpkA, is required for normal motility of the unicellular cyanobacterium Synechocystis PCC 6803. J Bacteriol 183, 1505–1510.[CrossRef]
    [Google Scholar]
  15. Kamei, A., Yuasa, T., Orikawa, K., Geng, X. & Ikeuchi, M. ( 2002; ). Biochemical examination of the potential eukaryotic-type protein kinase genes in the complete genome of the unicellular cyanobacterium Synechocystis sp. PCC 6803. DNA Res 9, 71–78.[CrossRef]
    [Google Scholar]
  16. Kamei, A., Yoshihara, S., Yuasa, T., Orikawa, K., Geng, X. & Ikeuchi, M. ( 2003; ). Biochemical and functional characterization of a eukaryotic-type protein kinase, SpkB, in the cyanobacterium Synechocystis sp. PCC 6803. Curr Microbiol 46, 296–301.[CrossRef]
    [Google Scholar]
  17. Laurent, S., Chen, H., Bédu, S., Ziarelli, F., Peng, L. & Zhang, C.-C. ( 2005; ). Nonmetabolizable analogue of 2-oxoglutarate elicits heterocyst differentiation under repressive conditions in Anabaena sp. strain PCC 7120. Proc Natl Acad Sci U S A 102, 9907–9912.[CrossRef]
    [Google Scholar]
  18. Le Van Quy, Foyer, C. & Champigny, M. L. ( 1991; ). Effect of light and on wheat leaf phosphoenolpyruvate carboxylase activity Plant Physiol 97, 1476–1482.[CrossRef]
    [Google Scholar]
  19. Leonard, C. J., Aravind, L. & Koonin, E. V. ( 1998; ). Novel families of putative protein kinases in bacteria and archae: evolution of the “eukaryotic” protein kinase superfamily. Genome Res 8, 1038–1047.
    [Google Scholar]
  20. Mérida, A., Candau, P. & Florencio, F. J. ( 1991; ). Regulation of glutamine synthetase activity in the unicellular cyanobacterium Synechocystis sp. strain PCC 6803 by the nitrogen source: effect of ammonium. J Bacteriol 173, 4095–4100.
    [Google Scholar]
  21. 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]
  22. Ogawa, T. & Kaplan, A. ( 2003; ). Inorganic carbon acquisition systems in cyanobacteria. Photosynth Res 77, 105–115.[CrossRef]
    [Google Scholar]
  23. Owttrim, G. W. & Colman, B. ( 1988; ). Phosphoenolpyruvate carboxylase mediated carbon flow in a cyanobacterium. Biochem Cell Biol 66, 93–99.[CrossRef]
    [Google Scholar]
  24. Pauling, D. C., Lapointe, J. P., Paris, C. M. & Ludwig, R. A. ( 2001; ). Azorhizobium caulinodans pyruvate dehydrogenase activity is dispensable for aerobic but required for microaerobic growth. Microbiology 147, 2233–2245.
    [Google Scholar]
  25. Ponting, C. P., Aravind, L., Schultz, J., Bork, P. & Koonin, E. V. ( 1999; ). Eukaryotic signalling domain homologues in archaea and bacteria. Ancient ancestry and horizontal gene transfer. J Mol Biol 289, 729–745.[CrossRef]
    [Google Scholar]
  26. Rippka, R., Deruelles, J., Waterbury, J. B., Herdman, M. & Stanier, R. Y. ( 1979; ). Generic assignments, strain histories and properties of pure culture of cyanobacteria. J Gen Microbiol 111, 1–61.[CrossRef]
    [Google Scholar]
  27. Roskoski, R. ( 2004; ). Src protein-tyrosine kinase structure and regulation. Biochem Biophys Res Commun 324, 1155–1164.[CrossRef]
    [Google Scholar]
  28. Ruppert, U., Irmler, A., Kloft, N. & Forchhammer, K. ( 2002; ). The novel protein phosphatase PphA from Synechocystis PCC 6803 controls dephosphorylation of the signalling protein PII. Mol Microbiol 44, 855–864.[CrossRef]
    [Google Scholar]
  29. Schwarz, R. & Grossman, A. ( 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]
  30. Shi, L., Bishoff, K. M. & Kennelly, P. J. ( 1999; ). The icfG gene cluster of Synechocystis sp. strain PCC 6803 encodes an Rsb/Spo-like protein kinase, protein phosphatase, and two phosphoproteins. J Bacteriol 181, 4761–4767.
    [Google Scholar]
  31. Singh, A. K. & Sherman, L. A. ( 2005; ). Pleiotropic effect of a histidine kinase on carbohydrate metabolism in Synechocystis sp. strain PCC 6803 and its requirement for heterotrophic growth. J Bacteriol 187, 2368–2376.[CrossRef]
    [Google Scholar]
  32. Tabita, F. R. ( 1994; ). The biochemistry and molecular regulation of carbon dioxide metabolism in cyanobacteria. In The Molecular Biology of Cyanobacteria, pp. 487–467. Edited by D. Bryant. Dordrecht, The Netherlands: Kluwer Academic Publishers.
  33. Yang, C., Hua, Q. & Shimizu, K. ( 2002; ). Metabolic flux analysis in Synechocystis using isotope distribution from 13C-labeled glucose. Metab Eng 4, 202–216.[CrossRef]
    [Google Scholar]
  34. Yu, H., Chen, J. K., Feng, S., Dalgarno, D. C., Brauer, A. W. & Schreiber, S. L. ( 1994; ). Structural basis of the binding of proline-rich peptides to SH3 domains. Cell 266, 1241–1247.
    [Google Scholar]
  35. Zhang, C.-C., Durand, M.-C., Jeanjean, R. & Joset, F. ( 1989; ). Molecular and genetic analysis of the glucose-fructose transport system in the cyanobacterium Synechocystis PCC6803. Mol Microbiol 3, 1221–1229.[CrossRef]
    [Google Scholar]
  36. Zhang, C.-C., Gonzalez, L. & Phalip, V. ( 1998; ). Survey, analysis and genetic organisation of genes encoding eukaryotic-like proteins on a cyanobacterial genome. Nucleic Acids Res 26, 3619–3625.[CrossRef]
    [Google Scholar]
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