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. 1995 Feb;177(3):544–550. doi: 10.1128/jb.177.3.544-550.1995

Archaeal grpE: transcription in two different morphologic stages of Methanosarcina mazei and comparison with dnaK and dnaJ.

E Conway De Macario 1, M Clarens 1, A J Macario 1
PMCID: PMC176626  PMID: 7836285

Abstract

Transcription of the heat shock gene grpE was studied in two different morphologic stages of the archaeon Methanosarcina mazei S-6 that differ in resistance to physical and chemical traumas: single cells and packets. While single cells are directly exposed to environmental changes, such as temperature elevations, cells in packets are surrounded by intercellular and peripheral material that keeps them together in a globular structure which can reach several millimeters in diameter. grpE transcript levels determined by Northern (RNA) blotting peaked after a 15-min heat shock in single cells. In contrast, the highest transcript levels in packets were observed after the longest heat shock tested, 60 min. The same response profiles were demonstrated by primer extension experiments and S1 nuclease analysis. A comparison of the grpE response to heat shock with those of dnaK and dnaJ showed that the grpE transcript level was the most increased, closely followed by that of the dnaK transcript, with that of the dnaJ gene being the least augmented. Transcription of grpE started at the same site under normal and heat shock temperatures, and the transcript was consistently approximately 700 bases long. Codon usage patterns revealed that the three archaeal genes use most codons and have the same codon preference for 61% of the amino acids.

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Selected References

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  1. Bolliger L., Deloche O., Glick B. S., Georgopoulos C., Jenö P., Kronidou N., Horst M., Morishima N., Schatz G. A mitochondrial homolog of bacterial GrpE interacts with mitochondrial hsp70 and is essential for viability. EMBO J. 1994 Apr 15;13(8):1998–2006. doi: 10.1002/j.1460-2075.1994.tb06469.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Boone D. R., Mah R. A. Effects of Calcium, Magnesium, pH, and Extent of Growth on the Morphology of Methanosarcina mazei S-6. Appl Environ Microbiol. 1987 Jul;53(7):1699–1700. doi: 10.1128/aem.53.7.1699-1700.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Brown J. W., Daniels C. J., Reeve J. N. Gene structure, organization, and expression in archaebacteria. Crit Rev Microbiol. 1989;16(4):287–338. doi: 10.3109/10408418909105479. [DOI] [PubMed] [Google Scholar]
  4. Conway de Macario E., Dugan C. B., Macario A. J. Identification of a grpE heat-shock gene homolog in the archaeon Methanosarcina mazei. J Mol Biol. 1994 Jul 1;240(1):95–101. doi: 10.1006/jmbi.1994.1422. [DOI] [PubMed] [Google Scholar]
  5. Cowing D. W., Bardwell J. C., Craig E. A., Woolford C., Hendrix R. W., Gross C. A. Consensus sequence for Escherichia coli heat shock gene promoters. Proc Natl Acad Sci U S A. 1985 May;82(9):2679–2683. doi: 10.1073/pnas.82.9.2679. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Craig E. A., Gambill B. D., Nelson R. J. Heat shock proteins: molecular chaperones of protein biogenesis. Microbiol Rev. 1993 Jun;57(2):402–414. doi: 10.1128/mr.57.2.402-414.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Harris J. E. Spontaneous Disaggregation of Methanosarcina mazei S-6 and Its Use in the Development of Genetic Techniques for Methanosarcina spp. Appl Environ Microbiol. 1987 Oct;53(10):2500–2504. doi: 10.1128/aem.53.10.2500-2504.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Hausner W., Thomm M. Purification and characterization of a general transcription factor, aTFB, from the archaeon Methanococcus thermolithotrophicus. J Biol Chem. 1993 Nov 15;268(32):24047–24052. [PubMed] [Google Scholar]
  9. Ikeda E., Yoshida S., Mitsuzawa H., Uno I., Toh-e A. YGE1 is a yeast homologue of Escherichia coli grpE and is required for maintenance of mitochondrial functions. FEBS Lett. 1994 Feb 21;339(3):265–268. doi: 10.1016/0014-5793(94)80428-1. [DOI] [PubMed] [Google Scholar]
  10. Johnston R. F., Pickett S. C., Barker D. L. Autoradiography using storage phosphor technology. Electrophoresis. 1990 May;11(5):355–360. doi: 10.1002/elps.1150110503. [DOI] [PubMed] [Google Scholar]
  11. Klenk H. P., Palm P., Lottspeich F., Zillig W. Component H of the DNA-dependent RNA polymerases of Archaea is homologous to a subunit shared by the three eucaryal nuclear RNA polymerases. Proc Natl Acad Sci U S A. 1992 Jan 1;89(1):407–410. doi: 10.1073/pnas.89.1.407. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Laloraya S., Gambill B. D., Craig E. A. A role for a eukaryotic GrpE-related protein, Mge1p, in protein translocation. Proc Natl Acad Sci U S A. 1994 Jul 5;91(14):6481–6485. doi: 10.1073/pnas.91.14.6481. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Lipinska B., King J., Ang D., Georgopoulos C. Sequence analysis and transcriptional regulation of the Escherichia coli grpE gene, encoding a heat shock protein. Nucleic Acids Res. 1988 Aug 11;16(15):7545–7562. doi: 10.1093/nar/16.15.7545. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Macario A. J., Dugan C. B., Clarens M., Conway de Macario E. dnaJ in Archaea. Nucleic Acids Res. 1993 Jun 11;21(11):2773–2773. doi: 10.1093/nar/21.11.2773. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Macario A. J., Dugan C. B., Conway de Macario E. A dnaK homolog in the archaebacterium Methanosarcina mazei S6. Gene. 1991 Dec 1;108(1):133–137. doi: 10.1016/0378-1119(91)90498-z. [DOI] [PubMed] [Google Scholar]
  16. Macario A. J., Dugan C. B., Conway de Macario E. An archaeal trkA homolog near dnaK and dnaJ. Biochim Biophys Acta. 1993 Dec 14;1216(3):495–498. doi: 10.1016/0167-4781(93)90022-6. [DOI] [PubMed] [Google Scholar]
  17. Marsh T. L., Reich C. I., Whitelock R. B., Olsen G. J. Transcription factor IID in the Archaea: sequences in the Thermococcus celer genome would encode a product closely related to the TATA-binding protein of eukaryotes. Proc Natl Acad Sci U S A. 1994 May 10;91(10):4180–4184. doi: 10.1073/pnas.91.10.4180. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Narberhaus F., Giebeler K., Bahl H. Molecular characterization of the dnaK gene region of Clostridium acetobutylicum, including grpE, dnaJ, and a new heat shock gene. J Bacteriol. 1992 May;174(10):3290–3299. doi: 10.1128/jb.174.10.3290-3299.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Ohta T., Saito K., Kuroda M., Honda K., Hirata H., Hayashi H. Molecular cloning of two new heat shock genes related to the hsp70 genes in Staphylococcus aureus. J Bacteriol. 1994 Aug;176(15):4779–4783. doi: 10.1128/jb.176.15.4779-4783.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Ouzounis C., Sander C. TFIIB, an evolutionary link between the transcription machineries of archaebacteria and eukaryotes. Cell. 1992 Oct 16;71(2):189–190. doi: 10.1016/0092-8674(92)90347-f. [DOI] [PubMed] [Google Scholar]
  21. Parsell D. A., Lindquist S. The function of heat-shock proteins in stress tolerance: degradation and reactivation of damaged proteins. Annu Rev Genet. 1993;27:437–496. doi: 10.1146/annurev.ge.27.120193.002253. [DOI] [PubMed] [Google Scholar]
  22. Pühler G., Leffers H., Gropp F., Palm P., Klenk H. P., Lottspeich F., Garrett R. A., Zillig W. Archaebacterial DNA-dependent RNA polymerases testify to the evolution of the eukaryotic nuclear genome. Proc Natl Acad Sci U S A. 1989 Jun;86(12):4569–4573. doi: 10.1073/pnas.86.12.4569. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Reeve J. N. Molecular biology of methanogens. Annu Rev Microbiol. 1992;46:165–191. doi: 10.1146/annurev.mi.46.100192.001121. [DOI] [PubMed] [Google Scholar]
  24. Robinson R. W. Life Cycles in the Methanogenic Archaebacterium Methanosarcina mazei. Appl Environ Microbiol. 1986 Jul;52(1):17–27. doi: 10.1128/aem.52.1.17-27.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Rowlands T., Baumann P., Jackson S. P. The TATA-binding protein: a general transcription factor in eukaryotes and archaebacteria. Science. 1994 May 27;264(5163):1326–1329. doi: 10.1126/science.8191287. [DOI] [PubMed] [Google Scholar]
  26. Schmiel D. H., Wyrick P. B. Another putative heat-shock gene and aminoacyl-tRNA synthetase gene are located upstream from the grpE-like and dnaK-like genes in Chlamydia trachomatis. Gene. 1994 Jul 22;145(1):57–63. doi: 10.1016/0378-1119(94)90322-0. [DOI] [PubMed] [Google Scholar]
  27. Schröder H., Langer T., Hartl F. U., Bukau B. DnaK, DnaJ and GrpE form a cellular chaperone machinery capable of repairing heat-induced protein damage. EMBO J. 1993 Nov;12(11):4137–4144. doi: 10.1002/j.1460-2075.1993.tb06097.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Sowers K. R., Gunsalus R. P. Adaptation for growth at various saline concentrations by the archaebacterium Methanosarcina thermophila. J Bacteriol. 1988 Feb;170(2):998–1002. doi: 10.1128/jb.170.2.998-1002.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Tilly K., Hauser R., Campbell J., Ostheimer G. J. Isolation of dnaJ, dnaK, and grpE homologues from Borrelia burgdorferi and complementation of Escherichia coli mutants. Mol Microbiol. 1993 Feb;7(3):359–369. doi: 10.1111/j.1365-2958.1993.tb01128.x. [DOI] [PubMed] [Google Scholar]
  30. Wetzstein M., Schumann W. Nucleotide sequence of a Bacillus subtilis gene homologous to the grpE gene of E. coli located immediately upstream of the dnaK gene. Nucleic Acids Res. 1990 Mar 11;18(5):1289–1289. doi: 10.1093/nar/18.5.1289. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Wetzstein M., Völker U., Dedio J., Löbau S., Zuber U., Schiesswohl M., Herget C., Hecker M., Schumann W. Cloning, sequencing, and molecular analysis of the dnaK locus from Bacillus subtilis. J Bacteriol. 1992 May;174(10):3300–3310. doi: 10.1128/jb.174.10.3300-3310.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Woese C. R., Kandler O., Wheelis M. L. Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc Natl Acad Sci U S A. 1990 Jun;87(12):4576–4579. doi: 10.1073/pnas.87.12.4576. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Xun L., Boone D. R., Mah R. A. Control of the Life Cycle of Methanosarcina mazei S-6 by Manipulation of Growth Conditions. Appl Environ Microbiol. 1988 Aug;54(8):2064–2068. doi: 10.1128/aem.54.8.2064-2068.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Yao R., Macario A. J., Conway de Macario E. An archaeal S-layer gene homolog with repetitive subunits. Biochim Biophys Acta. 1994 Nov 22;1219(3):697–700. doi: 10.1016/0167-4781(94)90230-5. [DOI] [PubMed] [Google Scholar]
  35. Ziemienowicz A., Skowyra D., Zeilstra-Ryalls J., Fayet O., Georgopoulos C., Zylicz M. Both the Escherichia coli chaperone systems, GroEL/GroES and DnaK/DnaJ/GrpE, can reactivate heat-treated RNA polymerase. Different mechanisms for the same activity. J Biol Chem. 1993 Dec 5;268(34):25425–25431. [PubMed] [Google Scholar]

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