Skip to main content
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1973 Feb;70(2):385–389. doi: 10.1073/pnas.70.2.385

Regulation of Macromolecular Biosynthesis in a Mutant of Escherichia coli Defective in Membrane Phospholipid Biosynthesis

Michael Glaser 1, William H Bayer 1, Robert 1, M Bell 1, P Roy Vagelos 1
PMCID: PMC433265  PMID: 4568726

Abstract

Nucleic acid and protein synthesis were studied in temperature-sensitive mutants defective in phospholipid synthesis. The defect is due to a single mutation in glycerol 3-phosphate acyltransferase (EC 2.3.1.15). The results show that at the restrictive temperature not only does phospholipid synthesis cease, but DNA, RNA, and protein synthesis also cease. Active transport continues, however, indicating that the cells do not become leaky or lose their energy supply. These results suggest that phospholipid synthesis is coupled to DNA, RNA, and protein synthesis.

Keywords: temperature-sensitive glycerol 3-phosphate acyltransferase, protein, active transport

Full text

PDF
387

Selected References

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

  1. Ames G. F. Lipids of Salmonella typhimurium and Escherichia coli: structure and metabolism. J Bacteriol. 1968 Mar;95(3):833–843. doi: 10.1128/jb.95.3.833-843.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. BLIGH E. G., DYER W. J. A rapid method of total lipid extraction and purification. Can J Biochem Physiol. 1959 Aug;37(8):911–917. doi: 10.1139/o59-099. [DOI] [PubMed] [Google Scholar]
  3. Blumenthal T., Landers T. A., Weber K. Bacteriophage Q replicase contains the protein biosynthesis elongation factors EF Tu and EF Ts. Proc Natl Acad Sci U S A. 1972 May;69(5):1313–1317. doi: 10.1073/pnas.69.5.1313. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Brutlag D., Schekman R., Kornberg A. A possible role for RNA polymerase in the initiation of M13 DNA synthesis. Proc Natl Acad Sci U S A. 1971 Nov;68(11):2826–2829. doi: 10.1073/pnas.68.11.2826. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cashel M., Gallant J. Two compounds implicated in the function of the RC gene of Escherichia coli. Nature. 1969 Mar 1;221(5183):838–841. doi: 10.1038/221838a0. [DOI] [PubMed] [Google Scholar]
  6. Cashel M. The control of ribonucleic acid synthesis in Escherichia coli. IV. Relevance of unusual phosphorylated compounds from amino acid-starved stringent strains. J Biol Chem. 1969 Jun 25;244(12):3133–3141. [PubMed] [Google Scholar]
  7. Cozzarelli N. R., Koch J. P., Hayashi S., Lin E. C. Growth stasis by accumulated L-alpha-glycerophosphate in Escherichia coli. J Bacteriol. 1965 Nov;90(5):1325–1329. doi: 10.1128/jb.90.5.1325-1329.1965. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Cronan J. E., Jr, Birge C. H., Vagelos P. R. Evidence for two genes specifically involved in unsaturated fatty acid biosynthesis in Escherichia coli. J Bacteriol. 1969 Nov;100(2):601–604. doi: 10.1128/jb.100.2.601-604.1969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Cronan J. E., Jr, Godson G. N. Mutants of Escherichia coli with temperature-sensitive lesions in membrane phospholipid synthesis: genetic analysis of glycerol-3-phosphate acyltransferase mutants. Mol Gen Genet. 1972;116(3):199–210. doi: 10.1007/BF00269765. [DOI] [PubMed] [Google Scholar]
  10. Cronan J. E., Jr, Ray T. K., Vagelos P. R. Selection and characterization of an E. coli mutant defective in membrane lipid biosynthesis. Proc Natl Acad Sci U S A. 1970 Mar;65(3):737–744. doi: 10.1073/pnas.65.3.737. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Cronan J. E., Vagelos P. R. Metabolism and function of the membrane phospholipids of Escherichia coli. Biochim Biophys Acta. 1972 Feb 14;265(1):25–60. doi: 10.1016/0304-4157(72)90018-4. [DOI] [PubMed] [Google Scholar]
  12. Fox C. F. A lipid requirement for induction of lactose transport in Escherichia coli. Proc Natl Acad Sci U S A. 1969 Jul;63(3):850–855. doi: 10.1073/pnas.63.3.850. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. HAYASHI S., KOCH J. P., LIN E. C. ACTIVE TRANSPORT OF L-ALPHA-GLYCEROPHOSPHATE IN ESCHERICHIA COLI. J Biol Chem. 1964 Sep;239:3098–3105. [PubMed] [Google Scholar]
  14. Henning U., Dennert G., Rehn K., Deppe G. Effects of oleate starvation in a fatty acid auxotroph of Escherichia coli K-12. J Bacteriol. 1969 May;98(2):784–796. doi: 10.1128/jb.98.2.784-796.1969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hsu C. C., Fox C. F. Induction of the lactose transport system in a lipid-synthesis-defective mutant of Escherichia coli. J Bacteriol. 1970 Aug;103(2):410–416. doi: 10.1128/jb.103.2.410-416.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Izui K. A lipid requirement for induction of alkaline phosphatase, one of periplasmic enzymes, in Escherichia coli. Biochem Biophys Res Commun. 1971 Dec 17;45(6):1506–1512. doi: 10.1016/0006-291x(71)90190-2. [DOI] [PubMed] [Google Scholar]
  17. KOCH J. P., HAYASHI S., LIN E. C. THE CONTROL OF DISSIMILATION OF GLYCEROL AND L-ALPHA-GLYCEROPHOSPHATE IN ESCHERICHIA COLI. J Biol Chem. 1964 Sep;239:3106–3108. [PubMed] [Google Scholar]
  18. Kass L. R. The antibacterial activity of 3-decynoyl-n-acetylcysteamine. Inhibition in vivo of beta-hydroxydecanoyl thioester dehydrase. J Biol Chem. 1968 Jun 25;243(12):3223–3228. [PubMed] [Google Scholar]
  19. Kito M., Pizer L. I. Purification and regulatory properties of the biosynthetic L-glycerol 3-phosphate dehydrogenase from Escherichia coli. J Biol Chem. 1969 Jun 25;244(12):3316–3323. [PubMed] [Google Scholar]
  20. Lillich T. T., White D. C. Phospholipid metabolism in the absence of net phospholipid synthesis in a glycerol-requiring mutant of Bacillus subtilis. J Bacteriol. 1971 Sep;107(3):790–797. doi: 10.1128/jb.107.3.790-797.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Mavis R. D., Bell R. M., Vagelos P. R. Effect of phospholipase C hydrolysis of membrane phospholipids on membranous enzymes. J Biol Chem. 1972 May 10;247(9):2835–2841. [PubMed] [Google Scholar]
  22. Mavis R. D., Vagelos P. R. The effect of phospholipid fatty acid composition in membranous enzymes in Escherichia coli. J Biol Chem. 1972 Feb 10;247(3):652–659. [PubMed] [Google Scholar]
  23. Medveczky N., Rosenberg H. Phosphate transport in Escherichia coli. Biochim Biophys Acta. 1971 Aug 13;241(2):494–506. doi: 10.1016/0005-2736(71)90048-4. [DOI] [PubMed] [Google Scholar]
  24. Mindich L. Control of fatty acid synthesis in bacteria. J Bacteriol. 1972 Apr;110(1):96–102. doi: 10.1128/jb.110.1.96-102.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Mindich L. Induction of Staphylococcus aureus Lactose Permease in the Absence of Glycerolipid Synthesis. Proc Natl Acad Sci U S A. 1971 Feb;68(2):420–424. doi: 10.1073/pnas.68.2.420. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Mindich L. Membrane synthesis in Bacillus subtilis. I. Isolation and properties of strains bearing mutations in glycerol metabolism. J Mol Biol. 1970 Apr 28;49(2):415–432. doi: 10.1016/0022-2836(70)90254-8. [DOI] [PubMed] [Google Scholar]
  27. Mindich L. Membrane synthesis in Bacillus subtilis. II. Integration of membrane proteins in the absence of lipid synthesis. J Mol Biol. 1970 Apr 28;49(2):433–439. doi: 10.1016/0022-2836(70)90255-x. [DOI] [PubMed] [Google Scholar]
  28. Overath P., Hill F. F., Lamnek-Hirsch I. Biogenesis of E. coli membrane: evidence for randomization of lipid phase. Nat New Biol. 1971 Dec 29;234(52):264–267. doi: 10.1038/newbio234264a0. [DOI] [PubMed] [Google Scholar]
  29. Ray P. H., White D. C. Effect of glycerol deprivation on the phospholipid metabolism of a glycerol auxotroph of Staphylococcus aureus. J Bacteriol. 1972 Feb;109(2):668–677. doi: 10.1128/jb.109.2.668-677.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Ray T. K., Cronan J. E., Jr, Mavis R. D., Vagelos P. R. The specific acylation of glycerol 3-phosphate to monoacylglycerol 3-phosphate in Escherichia coli. Evidence for a single enzyme conferring this specificity. J Biol Chem. 1970 Dec 10;245(23):6442–6448. [PubMed] [Google Scholar]
  31. Robbins A. R., Rotman B. Inhibition of methylgalactoside transport in Escherichia coli upon the cessation of unsaturated fatty acid biosynthesis. Proc Natl Acad Sci U S A. 1972 Aug;69(8):2125–2129. doi: 10.1073/pnas.69.8.2125. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Rosenbaum-Oliver D., Zamenhof S. Degree of participation of exogenous thymidine in the overall deoxyribonucleic acid synthesis in Escherichia coli. J Bacteriol. 1972 May;110(2):585–591. doi: 10.1128/jb.110.2.585-591.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Scharff R., Hendler R. W., Nanninga N., Burgess A. H. Respiration and protein synthesis in Escherichia coli membrane-envelope fragments. IV. Chemical and cytological characterization and biosynthetic capabilities of fragments obtained by mild procedures. J Cell Biol. 1972 Apr;53(1):1–23. doi: 10.1083/jcb.53.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Silbert D. F. Arrangement of fatty acyl groups in phosphatidylethanolamine from a fatty acid auxotroph of Escherichia coli. Biochemistry. 1970 Sep 1;9(18):3631–3640. doi: 10.1021/bi00820a021. [DOI] [PubMed] [Google Scholar]
  35. Singer S. J., Nicolson G. L. The fluid mosaic model of the structure of cell membranes. Science. 1972 Feb 18;175(4023):720–731. doi: 10.1126/science.175.4023.720. [DOI] [PubMed] [Google Scholar]
  36. Sokawa Y., Nakao E., Kaziro Y. On the nature of the control by RC gene in e. coli: amino acid-dependent control of lipid synthesis. Biochem Biophys Res Commun. 1968 Oct 10;33(1):108–112. doi: 10.1016/0006-291x(68)90263-5. [DOI] [PubMed] [Google Scholar]
  37. Sugino A., Hirose S., Okazaki R. RNA-linked nascent DNA fragments in Escherichia coli. Proc Natl Acad Sci U S A. 1972 Jul;69(7):1863–1867. doi: 10.1073/pnas.69.7.1863. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Willecke K., Mindich L. Induction of citrate transport in Bacillus subtilis during the absence of phospholipid synthesis. J Bacteriol. 1971 May;106(2):514–518. doi: 10.1128/jb.106.2.514-518.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Winkler H. H., Wilson T. H. The role of energy coupling in the transport of beta-galactosides by Escherichia coli. J Biol Chem. 1966 May 25;241(10):2200–2211. [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES