Skip to main content
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1993 Apr;175(7):1961–1970. doi: 10.1128/jb.175.7.1961-1970.1993

Modulation of the heat shock response by one-carbon metabolism in Escherichia coli.

D J Gage 1, F C Neidhardt 1
PMCID: PMC204276  PMID: 8458838

Abstract

A genetic screen designed to isolate mutants of Escherichia coli W3110 altered in the ability to induce the heat shock response identified a strain unable to induce the heat shock proteins in a rich, defined medium lacking methionine after exposure to 2,4-dinitrophenol. This strain also grew slowly at 28 degrees C and linearly at 42 degrees C in this medium. The abnormal induction of the heat shock proteins and abnormal growth at both high and low temperatures were reversed when methionine was included in the growth medium. The mutation responsible for these phenotypes mapped to the glyA gene, a biosynthetic gene encoding the enzyme that converts serine and tetrahydrofolate to glycine and 5,10-methylenetetrahydrofolate. This reaction is the major source of glycine and one-carbon units in the cell. Because fixed one-carbon units, in the form of methionine, allowed mutant cells to induce the heat shock response after exposure to 2,4-dinitrophenol, a one-carbon restriction may be responsible for the phenotypes described above.

Full text

PDF
1970

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Alfano C., McMacken R. Heat shock protein-mediated disassembly of nucleoprotein structures is required for the initiation of bacteriophage lambda DNA replication. J Biol Chem. 1989 Jun 25;264(18):10709–10718. [PubMed] [Google Scholar]
  2. Alfano C., McMacken R. Ordered assembly of nucleoprotein structures at the bacteriophage lambda replication origin during the initiation of DNA replication. J Biol Chem. 1989 Jun 25;264(18):10699–10708. [PubMed] [Google Scholar]
  3. Altman E., Kumamoto C. A., Emr S. D. Heat-shock proteins can substitute for SecB function during protein export in Escherichia coli. EMBO J. 1991 Feb;10(2):239–245. doi: 10.1002/j.1460-2075.1991.tb07943.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Blumenthal R. M., Reeh S., Pedersen S. Regulation of transcription factor rho and the alpha subunit of RNA polymerase in Escherichia coli B/r. Proc Natl Acad Sci U S A. 1976 Jul;73(7):2285–2288. doi: 10.1073/pnas.73.7.2285. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Clarke L., Carbon J. A colony bank containing synthetic Col El hybrid plasmids representative of the entire E. coli genome. Cell. 1976 Sep;9(1):91–99. doi: 10.1016/0092-8674(76)90055-6. [DOI] [PubMed] [Google Scholar]
  6. Cole J. R., Olsson C. L., Hershey J. W., Grunberg-Manago M., Nomura M. Feedback regulation of rRNA synthesis in Escherichia coli. Requirement for initiation factor IF2. J Mol Biol. 1987 Dec 5;198(3):383–392. doi: 10.1016/0022-2836(87)90288-9. [DOI] [PubMed] [Google Scholar]
  7. Dodson M., McMacken R., Echols H. Specialized nucleoprotein structures at the origin of replication of bacteriophage lambda. Protein association and disassociation reactions responsible for localized initiation of replication. J Biol Chem. 1989 Jun 25;264(18):10719–10725. [PubMed] [Google Scholar]
  8. Enequist H. G., Hirst T. R., Harayama S., Hardy S. J., Randall L. L. Energy is required for maturation of exported proteins in Escherichia coli. Eur J Biochem. 1981 May 15;116(2):227–233. doi: 10.1111/j.1432-1033.1981.tb05323.x. [DOI] [PubMed] [Google Scholar]
  9. Gamer J., Bujard H., Bukau B. Physical interaction between heat shock proteins DnaK, DnaJ, and GrpE and the bacterial heat shock transcription factor sigma 32. Cell. 1992 May 29;69(5):833–842. doi: 10.1016/0092-8674(92)90294-m. [DOI] [PubMed] [Google Scholar]
  10. Gething M. J., Sambrook J. Protein folding in the cell. Nature. 1992 Jan 2;355(6355):33–45. doi: 10.1038/355033a0. [DOI] [PubMed] [Google Scholar]
  11. Gottesman S., Squires C., Pichersky E., Carrington M., Hobbs M., Mattick J. S., Dalrymple B., Kuramitsu H., Shiroza T., Foster T. Conservation of the regulatory subunit for the Clp ATP-dependent protease in prokaryotes and eukaryotes. Proc Natl Acad Sci U S A. 1990 May;87(9):3513–3517. doi: 10.1073/pnas.87.9.3513. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Grossman A. D., Erickson J. W., Gross C. A. The htpR gene product of E. coli is a sigma factor for heat-shock promoters. Cell. 1984 Sep;38(2):383–390. doi: 10.1016/0092-8674(84)90493-8. [DOI] [PubMed] [Google Scholar]
  13. Jerez C., Weissbach H. Methylation of newly synthesized ribosomal protein L11 in a DNA-directed in vitro system. J Biol Chem. 1980 Sep 25;255(18):8706–8710. [PubMed] [Google Scholar]
  14. Kitagawa M., Wada C., Yoshioka S., Yura T. Expression of ClpB, an analog of the ATP-dependent protease regulatory subunit in Escherichia coli, is controlled by a heat shock sigma factor (sigma 32). J Bacteriol. 1991 Jul;173(14):4247–4253. doi: 10.1128/jb.173.14.4247-4253.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kroh H. E., Simon L. D. The ClpP component of Clp protease is the sigma 32-dependent heat shock protein F21.5. J Bacteriol. 1990 Oct;172(10):6026–6034. doi: 10.1128/jb.172.10.6026-6034.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Landick R., Vaughn V., Lau E. T., VanBogelen R. A., Erickson J. W., Neidhardt F. C. Nucleotide sequence of the heat shock regulatory gene of E. coli suggests its protein product may be a transcription factor. Cell. 1984 Aug;38(1):175–182. doi: 10.1016/0092-8674(84)90538-5. [DOI] [PubMed] [Google Scholar]
  17. Lark C. Methylation-dependent DNA synthesis in Escherichia coli mediated by DNA polymerase I. J Bacteriol. 1979 Jan;137(1):44–50. doi: 10.1128/jb.137.1.44-50.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Maurizi M. R., Clark W. P., Kim S. H., Gottesman S. Clp P represents a unique family of serine proteases. J Biol Chem. 1990 Jul 25;265(21):12546–12552. [PubMed] [Google Scholar]
  19. Nau F. The methylation of tRNA. Biochimie. 1976;58(6):629–645. doi: 10.1016/s0300-9084(76)80387-2. [DOI] [PubMed] [Google Scholar]
  20. Nyström T., Neidhardt F. C. Cloning, mapping and nucleotide sequencing of a gene encoding a universal stress protein in Escherichia coli. Mol Microbiol. 1992 Nov;6(21):3187–3198. doi: 10.1111/j.1365-2958.1992.tb01774.x. [DOI] [PubMed] [Google Scholar]
  21. O'Farrell P. H. High resolution two-dimensional electrophoresis of proteins. J Biol Chem. 1975 May 25;250(10):4007–4021. [PMC free article] [PubMed] [Google Scholar]
  22. Otsuji N., Soejima T., Maki S., Shinagawa H. Cloning of colicin E1 tolerant tolC (mtcB) gene of Escherichia coli K12 and identification of its gene product. Mol Gen Genet. 1982;187(1):30–36. doi: 10.1007/BF00384379. [DOI] [PubMed] [Google Scholar]
  23. PIZER L. I. GLYCINE SYNTHESIS AND METABOLISM IN ESCHERICHIA COLI. J Bacteriol. 1965 Apr;89:1145–1150. doi: 10.1128/jb.89.4.1145-1150.1965. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Pedersen S., Reeh S. V. Analysis of the proteins synthesized in ultraviolet light-irradiated Escherichia coli following infection with the bacteriophages lambdadrifd 18 and lambdadfus-3. Mol Gen Genet. 1976 Mar 30;144(3):339–343. doi: 10.1007/BF00341733. [DOI] [PubMed] [Google Scholar]
  25. Plamann M. D., Stauffer L. T., Urbanowski M. L., Stauffer G. V. Complete nucleotide sequence of the E. coli glyA gene. Nucleic Acids Res. 1983 Apr 11;11(7):2065–2075. doi: 10.1093/nar/11.7.2065. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Rollins C. M., Dahlquist F. W. Methylation of chemotaxis-specific proteins in Escherichia coli cells permeable to S-adenosylmethionine. Biochemistry. 1980 Sep 30;19(20):4627–4632. doi: 10.1021/bi00561a014. [DOI] [PubMed] [Google Scholar]
  27. Sakakibara Y. The dnaK gene of Escherichia coli functions in initiation of chromosome replication. J Bacteriol. 1988 Feb;170(2):972–979. doi: 10.1128/jb.170.2.972-979.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Singer M., Baker T. A., Schnitzler G., Deischel S. M., Goel M., Dove W., Jaacks K. J., Grossman A. D., Erickson J. W., Gross C. A. A collection of strains containing genetically linked alternating antibiotic resistance elements for genetic mapping of Escherichia coli. Microbiol Rev. 1989 Mar;53(1):1–24. doi: 10.1128/mr.53.1.1-24.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Skowyra D., Georgopoulos C., Zylicz M. The E. coli dnaK gene product, the hsp70 homolog, can reactivate heat-inactivated RNA polymerase in an ATP hydrolysis-dependent manner. Cell. 1990 Sep 7;62(5):939–944. doi: 10.1016/0092-8674(90)90268-j. [DOI] [PubMed] [Google Scholar]
  30. Squires C. L., Pedersen S., Ross B. M., Squires C. ClpB is the Escherichia coli heat shock protein F84.1. J Bacteriol. 1991 Jul;173(14):4254–4262. doi: 10.1128/jb.173.14.4254-4262.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Stauffer G. V., Plamann M. D., Stauffer L. T. Construction and expression of hybrid plasmids containing the Escherichia coli glyA genes. Gene. 1981 Jun-Jul;14(1-2):63–72. doi: 10.1016/0378-1119(81)90148-7. [DOI] [PubMed] [Google Scholar]
  32. Straus D. B., Walter W. A., Gross C. A. The heat shock response of E. coli is regulated by changes in the concentration of sigma 32. Nature. 1987 Sep 24;329(6137):348–351. doi: 10.1038/329348a0. [DOI] [PubMed] [Google Scholar]
  33. Straus D., Walter W., Gross C. A. DnaK, DnaJ, and GrpE heat shock proteins negatively regulate heat shock gene expression by controlling the synthesis and stability of sigma 32. Genes Dev. 1990 Dec;4(12A):2202–2209. doi: 10.1101/gad.4.12a.2202. [DOI] [PubMed] [Google Scholar]
  34. Tilly K., McKittrick N., Zylicz M., Georgopoulos C. The dnaK protein modulates the heat-shock response of Escherichia coli. Cell. 1983 Sep;34(2):641–646. doi: 10.1016/0092-8674(83)90396-3. [DOI] [PubMed] [Google Scholar]
  35. VanBogelen R. A., Hutton M. E., Neidhardt F. C. Gene-protein database of Escherichia coli K-12: edition 3. Electrophoresis. 1990 Dec;11(12):1131–1166. doi: 10.1002/elps.1150111205. [DOI] [PubMed] [Google Scholar]
  36. VanBogelen R. A., Neidhardt F. C. Ribosomes as sensors of heat and cold shock in Escherichia coli. Proc Natl Acad Sci U S A. 1990 Aug;87(15):5589–5593. doi: 10.1073/pnas.87.15.5589. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Vasudevan S. G., Armarego W. L., Shaw D. C., Lilley P. E., Dixon N. E., Poole R. K. Isolation and nucleotide sequence of the hmp gene that encodes a haemoglobin-like protein in Escherichia coli K-12. Mol Gen Genet. 1991 Apr;226(1-2):49–58. doi: 10.1007/BF00273586. [DOI] [PubMed] [Google Scholar]
  38. Wanner B. L., Kodaira R., Neidhardt F. C. Physiological regulation of a decontrolled lac operon. J Bacteriol. 1977 Apr;130(1):212–222. doi: 10.1128/jb.130.1.212-222.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Whitney E. N. The tolC locus in Escherichia coli K12. Genetics. 1971 Jan;67(1):39–53. doi: 10.1093/genetics/67.1.39. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Wild J., Altman E., Yura T., Gross C. A. DnaK and DnaJ heat shock proteins participate in protein export in Escherichia coli. Genes Dev. 1992 Jul;6(7):1165–1172. doi: 10.1101/gad.6.7.1165. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES