1887

Abstract

Cyanobacterial genomes typically encode multiple Hsp70 (DnaK) and Hsp40 (DnaJ) chaperones, and in the genome of the cyanobacterium PCC 6803, three DnaK proteins are encoded together with seven DnaJ proteins. While only two of the DnaJ proteins can complement the growth defect of an Δ strain, only disruption of the gene resulted in a growth defect at elevated temperatures. Based on the domain structure and the phenotype observed following disruption of the encoding gene, Sll0897 can be classified as a canonical heat-shock protein in . Furthermore, most genes could be deleted individually, whereas disruption of the gene encoding the DnaJ Sll1933 failed, which suggests an essential, yet undefined, function for Sll1933. Since after deletion of the remaining genes the phenotypes were not altered, the functions of these DnaJs either are not critical or are taken over by the remaining DnaJs. Nevertheless, only the two genes and could be disrupted in combination, suggesting physiological functions for the two encoded proteins which either are not overlapping and/or can be fulfilled by the remaining DnaJs in the double-disruption strain. Taken together, the present analysis indicates specific and promiscuous functions for multiple DnaJ proteins in .

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.045542-0
2011-05-01
2019-12-14
Loading full text...

Full text loading...

/deliver/fulltext/micro/157/5/1269.html?itemId=/content/journal/micro/10.1099/mic.0.045542-0&mimeType=html&fmt=ahah

References

  1. Acebrón S. P. , Fernández-Sáiz V. , Taneva S. G. , Moro F. , Muga A. . ( 2008; ). DnaJ recruits DnaK to protein aggregates. . J Biol Chem 283:, 1381–1390. [CrossRef] [PubMed]
    [Google Scholar]
  2. Bardwell J. C. , Tilly K. , Craig E. , King J. , Zylicz M. , Georgopoulos C. . ( 1986; ). The nucleotide sequence of the Escherichia coli K12 dnaJ+ gene. A gene that encodes a heat shock protein. . J Biol Chem 261:, 1782–1785.[PubMed]
    [Google Scholar]
  3. Blatch G. L. , Lässle M. . ( 1999; ). The tetratricopeptide repeat: a structural motif mediating protein-protein interactions. . Bioessays 21:, 932–939. [CrossRef] [PubMed]
    [Google Scholar]
  4. Blattner F. R. , Plunkett G. III , Bloch C. A. , Perna N. T. , Burland V. , Riley M. , Collado-Vides J. , Glasner J. D. , Rode C. K. et al. ( 1997; ). The complete genome sequence of Escherichia coli K-12. . Science 277:, 1453–1462. [CrossRef] [PubMed]
    [Google Scholar]
  5. Cheetham M. E. , Caplan A. J. . ( 1998; ). Structure, function and evolution of DnaJ: conservation and adaptation of chaperone function. . Cell Stress Chaperones 3:, 28–36. [CrossRef] [PubMed]
    [Google Scholar]
  6. Chen C. , Xu X. D. . ( 2009; ). DnaJ-like protein gene sll1384 is involved in phototaxis in Synechocystis sp. PCC 6803. . Chin Sci Bull 54:, 4381–4386. [CrossRef]
    [Google Scholar]
  7. Dudek J. , Volkmer J. , Bies C. , Guth S. , Müller A. , Lerner M. , Feick P. , Schäfer K. H. , Morgenstern E. et al. ( 2002; ). A novel type of co-chaperone mediates transmembrane recruitment of DnaK-like chaperones to ribosomes. . EMBO J 21:, 2958–2967. [CrossRef] [PubMed]
    [Google Scholar]
  8. Gamer J. , Multhaup G. , Tomoyasu T. , McCarty J. S. , Rüdiger S. , Schönfeld H. J. , Schirra C. , Bujard H. , Bukau B. . ( 1996; ). A cycle of binding and release of the DnaK, DnaJ and GrpE chaperones regulates activity of the Escherichia coli heat shock transcription factor sigma32. . EMBO J 15:, 607–617.[PubMed]
    [Google Scholar]
  9. Genevaux P. , Georgopoulos C. , Kelley W. L. . ( 2007; ). The Hsp70 chaperone machines of Escherichia coli: a paradigm for the repartition of chaperone functions. . Mol Microbiol 66:, 840–857. [CrossRef] [PubMed]
    [Google Scholar]
  10. Georgopoulos C. P. , Lundquist-Heil A. , Yochem J. , Feiss M. . ( 1980; ). Identification of the E. coli dnaJ gene product. . Mol Gen Genet 178:, 583–588. [CrossRef] [PubMed]
    [Google Scholar]
  11. Greene M. K. , Maskos K. , Landry S. J. . ( 1998; ). Role of the J-domain in the cooperation of Hsp40 with Hsp70. . Proc Natl Acad Sci U S A 95:, 6108–6113. [CrossRef] [PubMed]
    [Google Scholar]
  12. Han W. , Christen P. . ( 2003; ). Mechanism of the targeting action of DnaJ in the DnaK molecular chaperone system. . J Biol Chem 278:, 19038–19043. [CrossRef] [PubMed]
    [Google Scholar]
  13. Holtman C. K. , Chen Y. , Sandoval P. , Gonzales A. , Nalty M. S. , Thomas T. L. , Youderian P. , Golden S. S. . ( 2005; ). High-throughput functional analysis of the Synechococcus elongatus PCC 7942 genome. . DNA Res 12:, 103–115. [CrossRef] [PubMed]
    [Google Scholar]
  14. Kaneko T. , Sato S. , Kotani H. , Tanaka A. , Asamizu E. , Nakamura Y. , Miyajima N. , Hirosawa M. , Sugiura M. et al. ( 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] [PubMed]
    [Google Scholar]
  15. Kaneko T. , Nakamura Y. , Wolk C. P. et al. ( 2001; ). Complete genomic sequence of the filamentous nitrogen-fixing cyanobacterium Anabaena sp. strain PCC 7120 (supplement). . DNA Res 8:, 227–253. [CrossRef]
    [Google Scholar]
  16. Kelley W. L. . ( 1998; ). The J-domain family and the recruitment of chaperone power. . Trends Biochem Sci 23:, 222–227. [CrossRef] [PubMed]
    [Google Scholar]
  17. Kelley W. L. , Georgopoulos C. . ( 1997; ). The T/t common exon of simian virus 40, JC, and BK polyomavirus T antigens can functionally replace the J-domain of the Escherichia coli DnaJ molecular chaperone. . Proc Natl Acad Sci U S A 94:, 3679–3684. [CrossRef] [PubMed]
    [Google Scholar]
  18. Laemmli U. K. . ( 1970; ). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. . Nature 227:, 680–685. [CrossRef] [PubMed]
    [Google Scholar]
  19. Laufen T. , Mayer M. P. , Beisel C. , Klostermeier D. , Mogk A. , Reinstein J. , Bukau B. . ( 1999; ). Mechanism of regulation of Hsp70 chaperones by DnaJ cochaperones. . Proc Natl Acad Sci U S A 96:, 5452–5457. [CrossRef] [PubMed]
    [Google Scholar]
  20. Lu Z. , Cyr D. M. . ( 1998; ). The conserved carboxyl terminus and zinc finger-like domain of the co-chaperone Ydj1 assist Hsp70 in protein folding. . J Biol Chem 273:, 5970–5978. [CrossRef] [PubMed]
    [Google Scholar]
  21. Mayer M. P. , Bukau B. . ( 2005; ). Hsp70 chaperones: cellular functions and molecular mechanism. . Cell Mol Life Sci 62:, 670–684. [CrossRef] [PubMed]
    [Google Scholar]
  22. Nakamura Y. , Kaneko T. , Tabata S. . ( 2000; ). CyanoBase, the genome database for Synechocystis sp. strain PCC6803: status for the year 2000. . Nucleic Acids Res 28:, 72. [CrossRef] [PubMed]
    [Google Scholar]
  23. Nakamura Y. , Kaneko T. , Sato S. , Mimuro M. , Miyashita H. , Tsuchiya T. , Sasamoto S. , Watanabe A. , Kawashima K. et al. ( 2003; ). Complete genome structure of Gloeobacter violaceus PCC 7421, a cyanobacterium that lacks thylakoids (supplement). . DNA Res 10:, 181–201. [CrossRef] [PubMed]
    [Google Scholar]
  24. 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] [PubMed]
    [Google Scholar]
  25. 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] [PubMed]
    [Google Scholar]
  26. Prentki P. , Krisch H. M. . ( 1984; ). In vitro insertional mutagenesis with a selectable DNA fragment. . Gene 29:, 303–313. [CrossRef] [PubMed]
    [Google Scholar]
  27. Rippka R. , Waterbury J. , Cohen-Bazire G. . ( 1974; ). A cyanobacterium which lacks thylakoids. . Arch Microbiol 100:, 419–436. [CrossRef]
    [Google Scholar]
  28. Rippka R. , Deruelles J. , Waterbury J. B. , Herdman M. , Stanier R. Y. . ( 1979; ). Generic assignments, strains histories and properties of pure cultures of cyanobacteria. . J Gen Microbiol 111:, 1–61.[CrossRef]
    [Google Scholar]
  29. Rupprecht E. , Gathmann S. , Fuhrmann E. , Schneider D. . ( 2007; ). Three different DnaK proteins are functionally expressed in the cyanobacterium Synechocystis sp. PCC 6803. . Microbiology 153:, 1828–1841. [CrossRef] [PubMed]
    [Google Scholar]
  30. Rupprecht E. , Fuhrmann E. , Schneider D. . ( 2008; ). Stress regulated dnaK expression in Synechocystis sp. PCC 6803. . In Energy from the Sun, pp. 1327–1330. Edited by Allen J. , Goldbeck J. , Osmond B. . . Dordrecht, The Netherlands:: Springer Science & Media BV;.
    [Google Scholar]
  31. Rupprecht E. , Düppre E. , Schneider D. . ( 2010; ). Similarities and singularities of three DnaK proteins from the cyanobacterium Synechocystis sp. PCC 6803. . Plant Cell Physiol 51:, 1210–1218. [CrossRef] [PubMed]
    [Google Scholar]
  32. Sambrook J. , Russell D. W. . ( 2001; ). Molecular Cloning: a Laboratory Manual, , 3rd edn.. Cold Spring Harbor, NY:: Cold Spring Harbor Laboratory;.
    [Google Scholar]
  33. Sato M. , Yamahata H. , Watanabe S. , Nimura-Matsune K. , Yoshikawa H. . ( 2007; ). Characterization of dnaJ multigene family in the cyanobacterium Synechococcus elongatus PCC 7942. . Biosci Biotechnol Biochem 71:, 1021–1027. [CrossRef] [PubMed]
    [Google Scholar]
  34. Song Y. , Masison D. C. . ( 2005; ). Independent regulation of Hsp70 and Hsp90 chaperones by Hsp70/Hsp90-organizing protein Sti1 (Hop1). . J Biol Chem 280:, 34178–34185. [CrossRef] [PubMed]
    [Google Scholar]
  35. Szabo A. , Korszun R. , Hartl F. U. , Flanagan J. . ( 1996; ). A zinc finger-like domain of the molecular chaperone DnaJ is involved in binding to denatured protein substrates. . EMBO J 15:, 408–417.[PubMed]
    [Google Scholar]
  36. Szyperski T. , Pellecchia M. , Wall D. , Georgopoulos C. , Wüthrich K. . ( 1994; ). NMR structure determination of the Escherichia coli DnaJ molecular chaperone: secondary structure and backbone fold of the N-terminal region (residues 2-108) containing the highly conserved J domain. . Proc Natl Acad Sci U S A 91:, 11343–11347. [CrossRef] [PubMed]
    [Google Scholar]
  37. Truscott K. N. , Voos W. , Frazier A. E. , Lind M. , Li Y. , Geissler A. , Dudek J. , Müller H. , Sickmann A. et al. ( 2003; ). A J-protein is an essential subunit of the presequence translocase-associated protein import motor of mitochondria. . J Cell Biol 163:, 707–713. [CrossRef] [PubMed]
    [Google Scholar]
  38. Tsai J. , Douglas M. G. . ( 1996; ). A conserved HPD sequence of the J-domain is necessary for YDJ1 stimulation of Hsp70 ATPase activity at a site distinct from substrate binding. . J Biol Chem 271:, 9347–9354. [CrossRef] [PubMed]
    [Google Scholar]
  39. Vetting M. W. , Hegde S. S. , Fajardo J. E. , Fiser A. , Roderick S. L. , Takiff H. E. , Blanchard J. S. . ( 2006; ). Pentapeptide repeat proteins. . Biochemistry 45:, 1–10. [CrossRef] [PubMed]
    [Google Scholar]
  40. Wall D. , Zylicz M. , Georgopoulos C. . ( 1994; ). The NH2-terminal 108 amino acids of the Escherichia coli DnaJ protein stimulate the ATPase activity of DnaK and are sufficient for lambda replication. . J Biol Chem 269:, 5446–5451.[PubMed]
    [Google Scholar]
  41. Walsh P. , Bursać D. , Law Y. C. , Cyr D. , Lithgow T. . ( 2004; ). The J-protein family: modulating protein assembly, disassembly and translocation. . EMBO Rep 5:, 567–571. [CrossRef] [PubMed]
    [Google Scholar]
  42. Watanabe S. , Sato M. , Nimura-Matsune K. , Chibazakura T. , Yoshikawa H. . ( 2007; ). Protection of psbAII transcript from ribonuclease degradation in vitro by DnaK2 and DnaJ2 chaperones of the cyanobacterium Synechococcus elongatus PCC 7942. . Biosci Biotechnol Biochem 71:, 279–282. [CrossRef] [PubMed]
    [Google Scholar]
  43. Wegener K. M. , Singh A. K. , Jacobs J. M. , Elvitigala T. , Welsh E. A. , Keren N. , Gritsenko M. A. , Ghosh B. K. , Camp D. G. II et al. ( 2010; ). Global proteomics reveal an atypical strategy for carbon/nitrogen assimilation by a cyanobacterium under diverse environmental perturbations. . Mol Cell Proteomics 9:, 2678–2689. [CrossRef] [PubMed]
    [Google Scholar]
  44. Williams J. G. K. . ( 1988; ). Construction of specific mutations in photosystem II photosynthetic reaction center by genetic engineering methods in Synechocystis 6803. . Methods Enzymol 167:, 766–778. [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.045542-0
Loading
/content/journal/micro/10.1099/mic.0.045542-0
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