1887

Abstract

The impact of calcium signals in virtually all cells has led to the study of their role in prokaryotic organisms as stress response modulators. Cell differentiation in adverse conditions is a common Ca-requiring response. Nitrogen starvation induces the differentiation of N-fixing heterocysts in the filamentous cyanobacterium sp. PCC7120. This paper reports the use of a recombinant strain of this organism expressing the photoprotein aequorin to monitor the intracellular free-calcium concentration during the course of heterocyst differentiation. A specific calcium signature that is triggered exclusively when cells are deprived of combined nitrogen and generated by intracellular calcium stores was identified. The intracellular calcium signal was manipulated by treatment with specific calcium drugs, and the effect of such manipulation on the process of heterocyst differentiation was subsequently assessed. Suppression, magnification or poor regulation of this signal prevented the process of heterocyst differentiation, thereby suggesting that a calcium signal with a defined set of kinetic parameters may be required for differentiation. A mutant of sp. PCC7120 that cannot differentiate into heterocysts retains, however, the capacity to generate the calcium transient in response to nitrogen deprivation, strongly suggesting that Ca may be involved in a very early step of the differentiation process.

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2004-11-01
2020-08-08
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References

  1. Allen G. J., Schroeder J. I. 2001; Combining genetics and cell biology to crack the code of plant cell calcium signalling. Sci STKE102:RE13
    [Google Scholar]
  2. Allen G. J., Kwak J. M., Chu S. P., Llopis J., Tsien R. Y., Harper J. F., Schroeder J. I. 1999; Cameleon calcium indicator reports cytoplasmic calcium dynamics in Arabidopsis guard cells. Plant J19:735–747[CrossRef]
    [Google Scholar]
  3. Allen G. J., Chu S. P., Schumacher K.. 9 other authors 2000; Alteration of stimulus-specific guard cell calcium oscillations and stomatal closing in Arabidopsis det3 mutant. Science289:2338–2342[CrossRef]
    [Google Scholar]
  4. Allen G. J., Chu S. P., Harrington C. L., Schumacher K., Hoffman T., Tang Y. Y., Grill E., Schroeder J. 2001; A defined range of guard cell calcium oscillation parameters encodes stomatal movements. Nature411:1053–1057[CrossRef]
    [Google Scholar]
  5. Black T. A., Cai Y., Wolk C. P. 1993; Spatial expression and autoregulation of hetR, a gene involved in the control of heterocyst development in Anabaena. Mol Microbiol9:77–84[CrossRef]
    [Google Scholar]
  6. Cann M. J. 2003; Signalling through cyclic nucleotide monophosphates in cyanobacteria. New Phytol161:23–34[CrossRef]
    [Google Scholar]
  7. Dolmetsch R. E., Lewis R. S., Goodnow C. C., Healy J. I. 1997; Differential activation of transcription factors induced by Ca2+ response amplitude and duration. Nature386:855–858[CrossRef]
    [Google Scholar]
  8. Dolmetsch R. E., Xu K., Lewis R. S. 1998; Calcium oscillations increase the efficiency and specificity of gene expression. Nature392:933–936[CrossRef]
    [Google Scholar]
  9. Dominguez D. C., Adams H., Hageman J. H. 1999; Immunocytochemical localization of a calmodulin-like protein in Bacillus subtilis cells. J Bacteriol181:4605–4610
    [Google Scholar]
  10. Dong Y., Huang X., Wu X. Y., Zhao J. 2000; Identification of the active site of HetR protease and its requirement for heterocyst differentiation in the cyanobacterium Anabaena sp. strain PCC 7120. J Bacteriol182:1575–1579[CrossRef]
    [Google Scholar]
  11. Golden J. W., Yoon H. S. 1998; Heterocyst formation in Anabaena. Curr Opin Microbiol1:623–629[CrossRef]
    [Google Scholar]
  12. Golden J. W., Yoon H. S. 2003; Heterocyst development in Anabaena. Curr Opin Microbiol6:557–563[CrossRef]
    [Google Scholar]
  13. Gu X., Spitzer N. C. 1995; Distinct aspects of neuronal differentiation encoded by frequency of spontaneous Ca2+ transients. Nature375:784–787[CrossRef]
    [Google Scholar]
  14. Hood E. E., Armour S., Ownby J. D., Handa A. K., Bressan R. A. 1979; Effect of nitrogen starvation on the level of adenosine 3′,5′-monophosphate in Anabaena variabilis. Biochim Biophys Acta588:193–200[CrossRef]
    [Google Scholar]
  15. Inouye S., Franceschini T., Inouye M. 1983; Structural similarities between the development-specific protein S from a gram-negative bacterium, Myxococcus xantus, and calmodulin. Proc Natl Acad Sci U S A80:6829–6833[CrossRef]
    [Google Scholar]
  16. Jiménez-Sanchez A., Guzmán E. C., Botello E. 1993; An approach to the control of the initiation of chromosome replication in Escherichia coli. Curr Top Mol Genet1:33–48
    [Google Scholar]
  17. Kerson G. W., Miermyk J. A., Budd K. 1984; Evidence for the occurrence and possible physiological role for cyanobacterial calmodulin. Plant Physiol75:222–224[CrossRef]
    [Google Scholar]
  18. Knight M. R., Campbell A. K., Smith S. M., Trewavas A. J. 1991; Recombinant aequorin as a probe for cytosolic free Ca2+ inEscherichia coli. FEBS Lett282:405–408[CrossRef]
    [Google Scholar]
  19. Lockau W., Massalsky B., Dirmeier A. 1988; Purification and partial characterization of a calcium-stimulated protease from the cyanobacterium, Anabaena variabilis. Eur J Biochem172:433–438[CrossRef]
    [Google Scholar]
  20. Maldener I., Lockau W., Cai Y., Wolk C. P. 1991; The calcium-dependent protease of the cyanobacterium Anabaena: molecular cloning and expression of the gene in Escherichia coli, sequencing and site-directed mutagenesis. Mol Gen Genet225:113–120
    [Google Scholar]
  21. Michiels J., Xi C., Verhaert J., Vanderleyden J. 2002; The functions of Ca2+ in bacteria: a role for EF-hand proteins?. Trends Microbiol10:87–93[CrossRef]
    [Google Scholar]
  22. Ng C. K. Y., McAinsh M. R. 2003; Encoding specificity in plant calcium signalling: hot-spotting the ups and downs and waves. Ann Bot92:477–495[CrossRef]
    [Google Scholar]
  23. Norris J. R., Jensen H. L. 1957; Calcium requirements of Azotobacter. Nature180:1493–1494[CrossRef]
    [Google Scholar]
  24. Norris V., Grant S., Freestone P., Canvin J., Sheikh F. N., Toth I., Trinei M., Modha K., Norman R. I. 1996; Calcium signalling in Bacteria. J Bacteriol178:3677–3682
    [Google Scholar]
  25. O'Hara M. B., Hageman J. H. 1990; Energy and calcium ion dependence of proteolysis during sporulation of Bacillus subtilis cells. J Bacteriol172:4161–4170
    [Google Scholar]
  26. Onek L. A., Smith R. J. 1992; Calmodulin and calcium mediated regulation in prokaryotes. J Gen Microbiol138:1039–1049[CrossRef]
    [Google Scholar]
  27. Pettersson A., Bergman B. 1989; Calmodulin in heterocystous cyanobacteria: biochemical and immunological evidence. FEMS Microbiol lett60:95–99[CrossRef]
    [Google Scholar]
  28. Pitta T. P., Sherwood E. E., Kobel A. M., Berg H. C. 1997; Calcium is required for swimming by the nonflagellated cyanobacterium Synechococcus strain WH8113. J Bacteriol179:2524–2528
    [Google Scholar]
  29. Renzel S., Esselborn S., Sauer H. W., Hildebrant A. 2000; Calcium and malate are sporulation-promoting factors of. Physarum polycephalum. J Bacteriol182:6900–6905[CrossRef]
    [Google Scholar]
  30. Rose R. K., Dibdin G. H., Shellis R. P. 1993; A quantitative study of calcium binding and aggregation in selected oral bacteria. J Dent Res72:78–84[CrossRef]
    [Google Scholar]
  31. Scrase-Field S., Knight M. R. 2003; Calcium: just a chemical switch?. Curr Opin Plant Biol6:500–506[CrossRef]
    [Google Scholar]
  32. Shyu Y. T., Foegeding P. 1991; Calmodulin antagonists inhibit germination of Bacillus cereus T spores. J Appl Bacteriol70:233–238[CrossRef]
    [Google Scholar]
  33. Smith R. J. 1988; Calcium mediated regulation in the cyanobacteria?. In Biochemistry of the Algae and Cyanobacteria pp185–199 Edited by Rogers L. J., Gallon J. R.. Oxford: Clarendon Press;
    [Google Scholar]
  34. Smith R. J., Wilkins A. 1988; A correlation between intracellular calcium and incident irradiance in Nostoc 6720. New Phytol109:157–161[CrossRef]
    [Google Scholar]
  35. Smith R. J., Hobson S., Ellis I. R. 1987; Evidence for calcium-mediated regulation of heterocyst frequency and nitrogenase activity in Nostoc 6720. New Phytol105:531–541[CrossRef]
    [Google Scholar]
  36. Straley S. C., Plano G. V., Skrzypek E., Haddix P. L., Fields K. A. 1993; Regulation by Ca2+ in the Yersinia low-Ca2+ response. Mol Microbiol8:1005–1010[CrossRef]
    [Google Scholar]
  37. Tisa L. S., Adler J. 1992; Calcium ions are involved in Escherichia coli chemotaxis. Proc Natl Acad Sci U S A89:11804–11808[CrossRef]
    [Google Scholar]
  38. Tisa L. S., Adler J. 1995; Chemotactic properties of Escherichia coli mutants having abnormal Ca2+ content. J Bacteriol177:7112–7118
    [Google Scholar]
  39. Torrecilla I., Bonilla I, Leganés F., Fernández-Piñas F. 2000; Use of recombinant aequorin to study calcium homeostasis and monitor calcium transients in response to heat and cold shock in cyanobacteria. Plant Physiol123:161–176[CrossRef]
    [Google Scholar]
  40. Torrecilla I., Bonilla I, Leganés F., Fernández-Piñas F. 2001; Calcium transients in response to salinity and osmotic stress in the nitrogen-fixing cyanobacterium Anabaena sp. PCC7120, expressing cytosolic apoaequorin. Plant Cell Environ24:641–648[CrossRef]
    [Google Scholar]
  41. Torrecilla I., Bonilla I, Leganés F., Fernández-Piñas F. 2004; Light-to-dark transitions trigger a transient increase in intracellular Ca2+ modulated by the redox state of the photosynthetic electron transport chain in the cyanobacterium Anabaenasp. PCC7120. Plant Cell Environ27:810–819[CrossRef]
    [Google Scholar]
  42. Watkins N. J., Knight M. R., Trewavas A. J., Campbell A. K. 1995; Free calcium transients in chemotactic and non-chemotactic strains of Escherichia coli determined by using recombinant aequorin. Biochem J306:865–869
    [Google Scholar]
  43. Wherten M., Lundgren T. 2001; Intracellular Ca2+ mobilization and kinase activity during acylated homoserine lactone-dependent quorum sensing inSerratia liquefaciens. J Biol Chem276:6468–6472[CrossRef]
    [Google Scholar]
  44. Wolk C. P. 1996; Heterocyst formation. Annu Rev Genet30:59–78[CrossRef]
    [Google Scholar]
  45. Wolk C. P. 2000; Heterocyst formation in Anabaena. In Prokaryotic development pp83–104 Edited by Brun Y. V., Shimkets L. J.. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  46. Wolk P., Ernst A., Elhai J. 1994; Heterocyst metabolism and development. In The Molecular Biology of Cyanobacteria pp769–823 Edited by Bryant D. A.. Dordrecht: Kluwer Academic Publishers;
    [Google Scholar]
  47. Wood N. B., Haselkorn R. 1980; Control of phycobiliprotein proteolysis and heterocyst differentiation in Anabaena. J Bacteriol141:1375–1385
    [Google Scholar]
  48. Yu X. C., Margolin W. 1997; Ca2+-mediated GTP-dependent dynamic assembly of bacterial cell division protein FtsZ into asters and polymer networks in vitro. EMBO J16:5455–5463[CrossRef]
    [Google Scholar]
  49. Zhao J., LaClaire J. W., Brand J. J. 1991; Calcium and heterocyst development in Anabaena 7120. In Abstracts of the VII International Symposium on Photosynthetic Prokaryotesp– 105 University of Massachusetts; Amherst, USA:
    [Google Scholar]
  50. Zhou R., Wei X., Jiang N., Li H., Dong Y., Hsi K. L., Zhao J. 1998; Evidence that HetR protein is an unusual serine-type protease. Proc Natl Acad Sci U S A95:4959–4963[CrossRef]
    [Google Scholar]
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