Role of calcium in acclimation of the cyanobacterium PCC 7942 to nitrogen starvation Free

Abstract

A Ca signal is required for the process of heterocyst differentiation in the filamentous diazotrophic cyanobacterium sp. PCC 7120. This paper presents evidence that a transient increase in intracellular free Ca is also involved in acclimation to nitrogen starvation in the unicellular non-diazotrophic cyanobacterium PCC 7942. The Ca transient was triggered in response to nitrogen step-down or the addition of 2-oxoglutarate (2-OG), or its analogues 2,2-difluoropentanedioic acid (DFPA) and 2-methylenepentanedioic acid (2-MPA), to cells growing with combined nitrogen, suggesting that an increase in intracellular 2-OG levels precedes the Ca transient. The signalling protein P and the transcriptional regulator NtcA appear to be needed to trigger the signal. Suppression of the Ca transient by the intracellular Ca chelator ,-[1,2-ethanediylbis(oxy-2,1-phenylene)]bis[-[2-[(acetyloxy)methoxy]-2-oxoethyl]]-,bis[(acetyloxy)methyl] ester (BAPTA-AM) inhibited expression of the and genes, which are involved in acclimation to nitrogen starvation and transcriptionally activated by NtcA. BAPTA-AM treatment partially inhibited expression of the gene, which is involved in phycobiliprotein degradation following nutrient starvation and is regulated by NtcA and NblR; in close agreement, BAPTA-AM treatment partially inhibited bleaching following nitrogen starvation. Taken together, the results presented here strongly suggest an involvement of a defined Ca transient in acclimation of to nitrogen starvation through NtcA-dependent regulation.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.022251-0
2009-01-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/micro/155/1/25.html?itemId=/content/journal/micro/10.1099/mic.0.022251-0&mimeType=html&fmt=ahah

References

  1. Aldehni M. F., Forchhammer K. 2006; Analysis of a non-canonical NtcA-dependent promoter in Synechococcus elongatus and its regulation by NtcA and PII. Arch Microbiol 184:378–386
    [Google Scholar]
  2. Aldehni M. F., 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
    [Google Scholar]
  3. Allen M. M., Smith A. J. 1969; Nitrogen chlorosis in blue-green algae. Arch Mikrobiol 69:114–120
    [Google Scholar]
  4. Bennet A., Bogorad L. 1973; Complementary chromatic adaptation in cyanobacteria. J Bacteriol 130:82–91
    [Google Scholar]
  5. Bhaya D., Schwarz R., Grossman A. R. 2000; Molecular responses to environmental stress. In The Ecology of Cyanobacteria pp 397–442 Edited by Whitton B. A., Potts M. Dordrecht, The Netherlands: Kluwer Academic Publishers;
    [Google Scholar]
  6. Bienert R., Baier K., Volkmer R., Lockau W., Heinemann U. 2006; Crystal structure of NblA from Anabaena sp. PCC 7120, a small protein playing a key role in phycobilisome degradation. J Biol Chem 281:5216–5223
    [Google Scholar]
  7. Chen H., Laurent S., Bedu S., Ziarelli F., Chen H. L., Cheng Y., Zhang C. C., Peng L. 2006; Studying the signaling role of 2-oxoglutaric acid using analogs that mimic the ketone and ketal forms of 2-oxoglutaric acid. Chem Biol 13:849–856
    [Google Scholar]
  8. Collier J. L., Grossman A. R. 1994; A small polypeptide triggers complete degradation of light-harvesting phycobiliproteins in nutrient-deprived cyanobacteria. EMBO J 13:1039–1047
    [Google Scholar]
  9. Elhai J., Wolk C. P. 1988; Conjugal transfer of DNA to cyanobacteria. Methods Enzymol 167:747–754
    [Google Scholar]
  10. 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
    [Google Scholar]
  11. Espinosa J., Forchhammer K., Contreras A. 2007; Role of the Synechococcus PCC 7942 nitrogen regulator protein PipX in NtcA-controlled processes. Microbiology 153:711–718
    [Google Scholar]
  12. Forchhammer K. 2004; Global carbon/nitrogen control by PII signal transduction in cyanobacteria: from signals to targets. FEMS Microbiol Rev 28:319–333
    [Google Scholar]
  13. Forchhammer K., Tandeau de Marsac N. 1995; Functional analysis of the phosphoprotein PII ( glnB gene product) in the cyanobacterium Synechococcus sp. strain PCC 7942. J Bacteriol 177:2033–2040
    [Google Scholar]
  14. Gendel S., Straus N., Pulleyblank D., Williams J. 1983; Shuttle cloning vectors for the cyanobacterium Anacystis nidulans . J Bacteriol 156:148–154
    [Google Scholar]
  15. Golden S. S., Brusslan J., Haselkorn R. 1987; Genetic engineering of the cyanobacterial chromosome. Methods Enzymol 153:215–231
    [Google Scholar]
  16. Görl M., Sauer J., Baier T., Forchhammer K. 1998; Nitrogen-starvation-induced chlorosis in Synechococcus PCC 7942: adaptation to long-term survival. Microbiology 144:2449–2458
    [Google Scholar]
  17. Grossman A. R., Bhaya D., He Q. 2001; Tracking the light environment by cyanobacteria and the dynamic nature of light harvesting. J Biol Chem 276:11449–11452
    [Google Scholar]
  18. Hastings J. W., Weber G. 1963; Total quantum flux of isotropic sources. J Opt Soc Am 53:1410–1415
    [Google Scholar]
  19. Herrero A., Muro-Pastor A. M., Flores E. 2001; Nitrogen control in cyanobacteria. J Bacteriol 183:411–425
    [Google Scholar]
  20. Herrero A., Muro-Pastor A. M., Valladares A., Flores E. 2004; Cellular differentiation and the NtcA transcription factor in filamentous cyanobacteria. FEMS Microbiol Rev 28:469–487
    [Google Scholar]
  21. Laurent S., Chen H., Bedu S., Ziarelli F., Peng L., Zhang C. C. 2005; Nonmetabolizable analogue of 2-oxoglutarate elicits heterocyst differentiation under repressive conditions in Anabaena sp. PCC 7120. Proc Natl Acad Sci U S A 102:9907–9912
    [Google Scholar]
  22. Li H., Sherman L. A. 2002; Characterization of Synechocystis sp. strain PCC 6803 and Δ nbl mutants under nitrogen-deficient conditions. Arch Microbiol 178:256–266
    [Google Scholar]
  23. Li J. H., Laurent S., Konde V., Bedu S., Zhang C. C. 2003; An increase in the level of 2-oxoglutarate promotes heterocyst development in the cyanobacterium Anabaena sp. strain PCC 7120. Microbiology 149:3257–3263
    [Google Scholar]
  24. 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]
  25. Luque I., Ochoa De Alda J. A., Richaud C., Zabulon G., Thomas J. C., Houmard J. 2003; The NblAI protein from the filamentous cyanobacterium Tolypothrix PCC 7601: regulation of its expression and interactions with phycobilisome components. Mol Microbiol 50:1043–1054
    [Google Scholar]
  26. 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
    [Google Scholar]
  27. Marker A. F. H. 1972; The use of acetone and methanol in the estimation of chlorophyll in the presence of phaeophytin. Freshw Biol 2:361–385
    [Google Scholar]
  28. Rippka R. 1988; Isolation and purification of cyanobacteria. Methods Enzymol 167:3–27
    [Google Scholar]
  29. Sauer J., Görl 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
    [Google Scholar]
  30. Schwarz R., Forchhammer K. 2005; Acclimation of unicellular cyanobacteria to macronutrient deficiency: emergence of a complex network of cellular responses. Microbiology 151:2503–2514
    [Google Scholar]
  31. 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
    [Google Scholar]
  32. Shi Y., Zhao W., Zhang W., Ye Z., Zhao J. 2006; Regulation of intracellular free calcium concentration during heterocyst differentiation by HetR and NtcA in Anabaena sp. PCC 7120. Proc Natl Acad Sci U S A 103:11334–11339
    [Google Scholar]
  33. Tandeau-de-Marsac N., Houmard J. 1993; Adaptation of cyanobacteria to environmental stimuli, new steps towards molecular mechanisms. FEMS Microbiol Rev 104:119–189
    [Google Scholar]
  34. Torrecilla I., Leganes F., Bonilla I., Fernandez-Pinas F. 2000; Use of recombinant aequorin to study calcium homeostasis and monitor calcium transients in response to heat and cold shock in cyanobacteria. Plant Physiol 123:161–176
    [Google Scholar]
  35. Torrecilla I., Leganes F., Bonilla I., Fernandez-Pinas F. 2004; A calcium signal is involved in heterocyst differentiation in the cyanobacterium Anabaena sp. PCC7120. Microbiology 150:3731–3739
    [Google Scholar]
  36. Tous C., Vega-Palas M. A., Vioque A. 2001; Conditional expression of RNase P in the cyanobacterium Synechocystis sp. PCC6803 allows detection of precursor RNAs. Insight in the in vivo maturation pathway of transfer and other stable RNAs. J Biol Chem 276:29059–29066
    [Google Scholar]
  37. Vázquez-Bermúdez 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
    [Google Scholar]
  38. Vega-Palas M. A., Flores E., Herrero A. 1992; NtcA, a global nitrogen regulator from the cyanobacterium Synechococcus that belongs to the Crp family of bacterial regulators. Mol Microbiol 6:1853–1859
    [Google Scholar]
  39. Wolk C. P., Vonshak A., Kehoe P., Elhai J. 1984; Construction of shuttle vectors capable of conjugative transfer from Escherichia coli to nitrogen-fixing filamentous cyanobacteria. Proc Natl Acad Sci U S A 81:1561–1565
    [Google Scholar]
  40. Wyman M., Fay P. 1986; Underwater light climate and the growth and pigmentation of planktonic blue-green algae (cyanobacteria) I. The influence of light quantity. Proc R Soc Lond B Biol Sci 227:367–380
    [Google Scholar]
  41. Zhao Y., Shi Y., Zhao W., Huang X., Wang D., Brown N., Brand J., Zhao J. 2005; CcbP, a calcium-binding protein from Anabaena sp. PCC 7120, provides evidence that calcium ions regulate heterocyst differentiation. Proc Natl Acad Sci U S A 102:5744–5748
    [Google Scholar]
  42. Zinchenko V. V., Piven I. V., Melnik V. A., Shestakov S. V. 1999; Vectors for the complementation analysis of cyanobacterial mutants. Mol Genet 35:228–232
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.022251-0
Loading
/content/journal/micro/10.1099/mic.0.022251-0
Loading

Data & Media loading...

Most cited Most Cited RSS feed