1887

Abstract

Multiple genes appear to be common in cyanobacteria; the function of the encoded proteins is, however, still elusive. To characterize the gene family from the cyanobacterium sp. PCC 6803 in detail, genetic analyses were combined with analyses of the expression and localization patterns of the three encoded proteins. While significant expression of all three genes was found, the results obtained clearly indicate physiological differences of the three proteins , and DnaK2 seems to have a key function in . Expression of DnaK3 appears also to be as essential as expression of DnaK2, whereas the gene was deleted without resulting in any distorted phenotype. In line with a suggested privileged function, expression of DnaK2 altered most significantly after heat shock.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.2007/005876-0
2007-06-01
2024-12-08
Loading full text...

Full text loading...

/deliver/fulltext/micro/153/6/1828.html?itemId=/content/journal/micro/10.1099/mic.0.2007/005876-0&mimeType=html&fmt=ahah

References

  1. Alexeyev M. F. 1995; Three kanamycin resistance gene cassettes with different polylinkers. Biotechniques 18:52–56
    [Google Scholar]
  2. Bukau B., Horwich A. L. 1998; The Hsp70 and Hsp60 chaperone machines. Cell 92:351–366 [CrossRef]
    [Google Scholar]
  3. Bukau B., Walker G. C. 1989a; Cellular defects caused by deletion of the Escherichia coli dnaK gene indicate roles for heat shock protein in normal metabolism. J Bacteriol 171:2337–2346
    [Google Scholar]
  4. Bukau B., Walker G. C. 1989b; Delta dnaK52 mutants of Escherichia coli have defects in chromosome segregation and plasmid maintenance at normal growth temperatures. J Bacteriol 171:6030–6038
    [Google Scholar]
  5. Bukau B., Weissman J., Horwich A. 2006; Molecular chaperones and protein quality control. Cell 125:443–451 [CrossRef]
    [Google Scholar]
  6. Chitnis P. R., Nelson N. 1991; Molecular cloning of the genes encoding two chaperone proteins of the cyanobacterium Synechocystis sp. PCC 6803. J Biol Chem 266:58–65
    [Google Scholar]
  7. Choi J. S., Kim D. S., Lee J., Kim S. J., Kim S. I., Kim Y. H., Hong J., Yoo J. S., Suh K. H., Park Y. M. 2000; Proteome analysis of light-induced proteins in Synechocystis sp. PCC 6803: identification of proteins separated by 2D-PAGE using N-terminal sequencing and MALDI-TOF MS. Mol Cells 10:705–711 [CrossRef]
    [Google Scholar]
  8. Cupp-Vickery J. R., Peterson J. C., Ta D. T., Vickery L. E. 2004; Crystal structure of the molecular chaperone HscA substrate binding domain complexed with the IscU recognition peptide ELPPVKIHC. J Mol Biol 342:1265–1278 [CrossRef]
    [Google Scholar]
  9. Flaherty K. M., DeLuca-Flaherty C., McKay D. B. 1990; Three-dimensional structure of the ATPase fragment of a 70K heat-shock cognate protein. Nature 346:623–628 [CrossRef]
    [Google Scholar]
  10. Fulda S., Mikkat S., Huang F., Huckauf J., Marin K., Norling B., Hagemann M. 2006; Proteome analysis of salt stress response in the cyanobacterium Synechocystis sp. strain PCC 6803. Proteomics 6:2733–2745 [CrossRef]
    [Google Scholar]
  11. Gan C. S., Reardon K. F., Wright P. C. 2005; Comparison of protein and peptide prefractionation methods for the shotgun proteomic analysis of Synechocystis sp. PCC 6803. Proteomics 5:2468–2478 [CrossRef]
    [Google Scholar]
  12. Georgopoulos C. P., Lam B., Lundquist-Heil A., Rudolph C. F., Yochem J., Feiss M. 1979; Identification of the C. coli dnaK ( groPC756 ) gene product. Mol Gen Genet 172:143–149 [CrossRef]
    [Google Scholar]
  13. Guzman L. M., Belin D., Carson M. J., Beckwith J. 1995; Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol 177:4121–4130
    [Google Scholar]
  14. Harrison C. 2003; GrpE, a nucleotide exchange factor for DnaK. Cell Stress Chaperones 8:218–224 [CrossRef]
    [Google Scholar]
  15. Harrison C. J., Hayer-Hartl M., Di Liberto M., Hartl F., Kuriyan J. 1997; Crystal structure of the nucleotide exchange factor GrpE bound to the ATPase domain of the molecular chaperone DnaK. Science 276:431–435 [CrossRef]
    [Google Scholar]
  16. Hengge-Aronis R. 2002; Signal transduction and regulatory mechanisms involved in control of the σ S (RpoS) subunit of RNA polymerase. Microbiol Mol Biol Rev 66:373–395 [CrossRef]
    [Google Scholar]
  17. Huang F., Fulda S., Hagemann M., Norling B. 2006; Proteomic screening of salt-stress-induced changes in plasma membranes of Synechocystis sp. strain PCC 6803. Proteomics 6:910–920 [CrossRef]
    [Google Scholar]
  18. Jiang J., Prasad K., Lafer E. M., Sousa R. 2005; Structural basis of interdomain communication in the Hsc70 chaperone. Mol Cell 20:513–524 [CrossRef]
    [Google Scholar]
  19. Kaneko T., Tabata S. 1997; Complete genome structure of the unicellular cyanobacterium Synechocystis sp. PCC6803. Plant Cell Physiol 38:1171–1176 [CrossRef]
    [Google Scholar]
  20. Kaneko T., Sato S., Kotani H., Tanaka A., Asamizu E., Nakamura Y., Miyajima N., Hirosawa M., Sugiura M. other authors 1996; Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res 3:109–136 [CrossRef]
    [Google Scholar]
  21. Kunert A., Hagemann M., Erdmann N. 2000; Construction of promoter probe vectors for Synechocystis sp. PCC 6803 using the light-emitting reporter systems Gfp and LuxAB. J Microbiol Methods 41:185–194 [CrossRef]
    [Google Scholar]
  22. Lelivelt M. J., Kawula T. H. 1995; Hsc66, an Hsp70 homolog in Escherichia coli , is induced by cold shock but not by heat shock. J Bacteriol 177:4900–4907
    [Google Scholar]
  23. Liberek K., Marszalek J., Ang D., Georgopoulos C., Zylicz M. 1991; Escherichia coli DnaJ and GrpE heat shock proteins jointly stimulate ATPase activity of DnaK. Proc Natl Acad Sci U S A 88:2874–2878 [CrossRef]
    [Google Scholar]
  24. Mary I., Tu C. J., Grossman A., Vaulot D. 2004; Effects of high light on transcripts of stress-associated genes for the cyanobacteria Synechocystis sp. PCC 6803 and Prochlorococcus MED4 and MIT9313. Microbiology 150:1271–1281 [CrossRef]
    [Google Scholar]
  25. Mate Z., Sass L., Szekeres M., Vass I., Nagy F. 1998; UV-B-induced differential transcription of psbA genes encoding the D1 protein of photosystem II in the cyanobacterium Synechocystis 6803. J Biol Chem 273:17439–17444 [CrossRef]
    [Google Scholar]
  26. Mogk A., Bukau B., Lutz R., Schumann W. 1999; Construction and analysis of hybrid Escherichia coli-Bacillus subtilis dnaK genes. J Bacteriol 181:1971–1974
    [Google Scholar]
  27. Mohamed A., Eriksson J., Osiewacz H. D., Jansson C. 1993; Differential expression of the psbA genes in the cyanobacterium Synechocystis 6803. Mol Gen Genet 238:161–168
    [Google Scholar]
  28. Nimura K., Yoshikawa H., Takahashi H. 1994a; Sequence analysis of the third dnaK homolog gene in Synechococcus sp. PCC7942. Biochem Biophys Res Commun 205:2016–2017 [CrossRef]
    [Google Scholar]
  29. Nimura K., Yoshikawa H., Takahashi H. 1994b; Identification of dnaK multigene family in Synechococcus sp. PCC7942. Biochem Biophys Res Commun 201:466–471 [CrossRef]
    [Google Scholar]
  30. Nimura K., Yoshikawa H., Takahashi H. 1996; DnaK3, one of the three DnaK proteins of cyanobacterium Synechococcus sp. PCC7942, is quantitatively detected in the thylakoid membrane. Biochem Biophys Res Commun 229:334–340 [CrossRef]
    [Google Scholar]
  31. Nimura K., Takahashi H., Yoshikawa H. 2001; Characterization of the dnaK multigene family in the cyanobacterium Synechococcus sp. strain PCC7942. J Bacteriol 183:1320–1328 [CrossRef]
    [Google Scholar]
  32. Paek K. H., Walker G. C. 1987; Escherichia coli dnaK null mutants are inviable at high temperature. J Bacteriol 169:283–290
    [Google Scholar]
  33. Rippka R., Deruelles J., Waterbury J. B., Herdman M., Stanier R. Y. 1979; Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111:1–61 [CrossRef]
    [Google Scholar]
  34. Rospert S., Chacinska A. 2006; Distinct yet linked: chaperone networks in the eukaryotic cytosol. Genome Biol 7:208 [CrossRef]
    [Google Scholar]
  35. Salih G. F., Jansson C. 1997; Activation of the silent psbA1 gene in the cyanobacterium Synechocystis sp. strain 6803 produces a novel and functional D1 protein. Plant Cell 9:869–878 [CrossRef]
    [Google Scholar]
  36. Sambrook J., Fritsch E. F., Maniatis T. 1989 Molecular Cloning: a Laboratory Manual , 2nd edn. Cold Spring Harbor, USA: Cold Spring Harbor Press;
    [Google Scholar]
  37. Schneider D., Schmidt C. L. 2005; Multiple Rieske proteins in prokaryotes: where and why?. Biochim Biophys Acta 17101–12 [CrossRef]
    [Google Scholar]
  38. Schneider D., Skrzypczak S., Anemuller S., Schmidt C. L., Seidler A., Rögner M. 2002; Heterogeneous Rieske proteins in the cytochrome b6f complex of Synechocystis PCC6803?. J Biol Chem 277:10949–10954 [CrossRef]
    [Google Scholar]
  39. Schneider D., Berry S., Volkmer T., Seidler A., Rögner M. 2004a; PetC1 is the major Rieske iron-sulfur protein in the cytochrome b6f complex of Synechocystis sp. PCC 6803. J Biol Chem 279:39383–39388 [CrossRef]
    [Google Scholar]
  40. Schneider D., Volkmer T., Berry S., Seidler A., Rögner M. 2004b; Characterization of the petC gene family in the cyanobacterium Synechocystis PCC 6803. Cell Mol Biol Lett 9:51–55
    [Google Scholar]
  41. Schoepfer R. 1993; The pRSET family of T7 promoter expression vectors for Escherichia coli. Gene 124:83–85 [CrossRef]
    [Google Scholar]
  42. Seaton B. L., Vickery L. E. 1994; A gene encoding a DnaK/hsp70 homolog in Escherichia coli. Proc Natl Acad Sci U S A 91:2066–2070 [CrossRef]
    [Google Scholar]
  43. Steel G. J., Fullerton D. M., Tyson J. R., Stirling C. J. 2004; Coordinated activation of Hsp70 chaperones. Science 303:98–101 [CrossRef]
    [Google Scholar]
  44. Suzuki I., Simon W. J., Slabas A. R. 2006; The heat shock response of Synechocystis sp. PCC 6803 analysed by transcriptomics and proteomics. J Exp Bot 57:1573–1578 [CrossRef]
    [Google Scholar]
  45. Thompson J. D., Gibson T., Plewniak F., Jeanmougin F., Higgins D. 1997; The clustal_x Windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882 [CrossRef]
    [Google Scholar]
  46. Varvasovszki V., Glatz A., Shigapova N., Josvay K., Vigh L., Horvath I. 2003; Only one dnaK homolog, dnaK2 , is active transcriptionally and is essential in Synechocystis. Biochem Biophys Res Commun 305:641–648 [CrossRef]
    [Google Scholar]
  47. Wang H., Kurochkin A. V., Pang Y., Hu W., Flynn G. C., Zuiderweg E. R. 1998; NMR solution structure of the 21 kDa chaperone protein DnaK substrate binding domain: a preview of chaperone-protein interaction. Biochemistry 37:7929–7940 [CrossRef]
    [Google Scholar]
  48. Williams J. G. K. 1988; Mutations in PSII reaction center. Methods Enzymol 167:766–778
    [Google Scholar]
  49. Yam A. Y.-W., Albanese V., Lin H.-T. J., Frydman J. 2005; Hsp110 cooperates with different cytosolic HSP70 systems in a pathway for de novo folding. J Biol Chem 280:41252–41261 [CrossRef]
    [Google Scholar]
  50. Yoshimune K., Yoshimura T., Esaki N. 1998; Hsc62, a new DnaK homologue of Escherichia coli. Biochem Biophys Res Commun 250:115–118 [CrossRef]
    [Google Scholar]
  51. Zhang Y., Zuiderweg E. R. 2004; The 70-kDa heat shock protein chaperone nucleotide-binding domain in solution unveiled as a molecular machine that can reorient its functional subdomains. Proc Natl Acad Sci U S A 101:10272–10277 [CrossRef]
    [Google Scholar]
  52. Zhu X., Zhao X., Burkholder W. F., Gragerov A., Ogata C. M., Gottesman M. E., Hendrickson W. A. 1996; Structural analysis of substrate binding by the molecular chaperone DnaK. Science 272:1606–1614 [CrossRef]
    [Google Scholar]
/content/journal/micro/10.1099/mic.0.2007/005876-0
Loading
/content/journal/micro/10.1099/mic.0.2007/005876-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error