Skip to main content
NCBI home page
Biochemical Journal logoLink to Biochemical Journal
. 1972 Mar;127(1):11–25. doi: 10.1042/bj1270011

The mechanism of wall synthesis in bacteria. The organization of enzymes and isoprenoid phosphates in the membrane

R G Anderson 1, Helen Hussey 1, J Baddiley 1
PMCID: PMC1178555  PMID: 4627447

Abstract

1. The synthesis of peptidoglycan and teichoic acids by cell-free preparations from Bacillus licheniformis A.T.C.C. 9945 and Bacillus subtilis N.C.T.C. 3610 has been studied under a variety of conditions. 2. It was shown that poly(glycerol phosphate) is synthesized through a lipid intermediate, and it is concluded from this and other work that all major bacterial wall polymers are formed in a similar manner through such intermediates. 3. Close interrelation between the synthesis of peptidoglycan and teichoic acids was demonstrated, and inhibition studies confirm that the polyprenol phosphate molecules participating in the synthesis of peptidoglycan are shared with the systems that synthesize teichoic acids. 4. Nucleotides for the synthesis of one polymer are inhibitory towards synthesis of the other, and these effects can be enhanced or diminished by preincubation of the enzyme system with appropriate nucleotide precursors. 5. It is concluded that the return of undecaprenol phosphate to a common pool occurs only after the completion of polymer chains, and not after each cycle in the attachment of individual repeating units. This and other observations support a model for bacterial wall synthesis in which the multi-enzyme systems for each polymer are closely aligned in the membrane, with a molecule of undecaprenol phosphate located between them in a manner that enables it to be shared. The general mechanisms of wall synthesis and its control are discussed.

Full text

PDF
11

Selected References

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

  1. ANDERSON J. S., MATSUHASHI M., HASKIN M. A., STROMINGER J. L. LIPID-PHOSPHOACETYLMURAMYL-PENTAPEPTIDE AND LIPID-PHOSPHODISACCHARIDE-PENTAPEPTIDE: PRESUMED MEMBRANE TRANSPORT INTERMEDIATES IN CELL WALL SYNTHESIS. Proc Natl Acad Sci U S A. 1965 Apr;53:881–889. doi: 10.1073/pnas.53.4.881. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Anderson J. S., Matsuhashi M., Haskin M. A., Strominger J. L. Biosythesis of the peptidoglycan of bacterial cell walls. II. Phospholipid carriers in the reaction sequence. J Biol Chem. 1967 Jul 10;242(13):3180–3190. [PubMed] [Google Scholar]
  3. BADDILEY J., BUCHANAN J. G., CARSS B., MATHIAS A. P., SANDERSON A. R. The isolation of cytidine diphosphate glycerol, cytidine diphosphate ribitol and mannitol 1-phosphate from Lactobacillus arabinosus. Biochem J. 1956 Dec;64(4):599–603. doi: 10.1042/bj0640599. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. BURGER M. M., GLASER L. THE SYNTHESIS OF TEICHOIC ACIDS. I. POLYGLYCEROPHOSPHATE. J Biol Chem. 1964 Oct;239:3168–3177. [PubMed] [Google Scholar]
  5. Baddiley J., Blumsom N. L., Douglas L. J. The biosynthesis of the wall teichoic acid in Staphylococcus lactis I3. Biochem J. 1968 Dec;110(3):565–571. doi: 10.1042/bj1100565. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Brooks D., Baddiley J. A lipid intermediate in the synthesis of a poly-(N-acetylglucosamine 1-phosphate) from the wall of Staphylococcus lactis N.C.T.C. 2102. Biochem J. 1969 Nov;115(2):307–314. doi: 10.1042/bj1150307. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Burger M. M., Glaser L. The synthesis of teichoic acids. V. Polyglucosylglycerol phosphate and polygalactosylglycerol phosphate. J Biol Chem. 1966 Jan 25;241(2):494–506. [PubMed] [Google Scholar]
  8. Douglas L. J., Baddiley J. A lipid intermediate in the biosynthesis of a teichoic acid. FEBS Lett. 1968 Aug;1(2):114–116. doi: 10.1016/0014-5793(68)80034-1. [DOI] [PubMed] [Google Scholar]
  9. GLASER L., BURGER M. M. THE SYNTHESIS OF TEICHOIC ACIDS. 3. GLUCOSYLATION OF POLYGLYCEROPHOSPHATE. J Biol Chem. 1964 Oct;239:3187–3191. [PubMed] [Google Scholar]
  10. HANES C. S., ISHERWOOD F. A. Separation of the phosphoric esters on the filter paper chromatogram. Nature. 1949 Dec 31;164(4183):1107-12, illust. doi: 10.1038/1641107a0. [DOI] [PubMed] [Google Scholar]
  11. Hancock I. C., Baddiley J. Biosynthesis of the wall teichoic acid in Bacillus licheniformis. Biochem J. 1972 Mar;127(1):27–37. doi: 10.1042/bj1270027. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Higashi Y., Siewert G., Strominger J. L. Biosynthesis of the peptidoglycan of bacterial cell walls. XIX. Isoprenoid alcohol phosphokinase. J Biol Chem. 1970 Jul 25;245(14):3683–3690. [PubMed] [Google Scholar]
  13. Higashi Y., Strominger J. L., Sweeley C. C. Biosynthesis of the peptidoglycan of bacterial cell walls. XXI. Isolation of free C55-isoprenoid alcohol and of lipid intermediates in peptidoglycan synthesis from Staphylococcus aureus. J Biol Chem. 1970 Jul 25;245(14):3697–3702. [PubMed] [Google Scholar]
  14. Higashi Y., Strominger J. L., Sweeley C. C. Structure of a lipid intermediate in cell wall peptidoglycan synthesis: a derivative of a C55 isoprenoid alcohol. Proc Natl Acad Sci U S A. 1967 Jun;57(6):1878–1884. doi: 10.1073/pnas.57.6.1878. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. JORDAN D. C. Effect of vancomycin on the synthesis of the cell wall mucopeptide of Staphylococcus aureus. Biochem Biophys Res Commun. 1961 Nov 20;6:167–170. doi: 10.1016/0006-291x(61)90122-x. [DOI] [PubMed] [Google Scholar]
  16. KELEMEN M. V., BADDILEY J. Structure of the intracellular glycerol teichoic acid from Lactobacillus casei A.T.C.C. 7469. Biochem J. 1961 Aug;80:246–254. doi: 10.1042/bj0800246. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. KREBS H. A., HEMS R. Some reactions of adenosine and inosine phosphates in animal tissues. Biochim Biophys Acta. 1953 Sep-Oct;12(1-2):172–180. doi: 10.1016/0006-3002(53)90136-x. [DOI] [PubMed] [Google Scholar]
  18. LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
  19. PALADINI A. C., LELOIR L. F. Studies on uridine-diphosphate-glucose. Biochem J. 1952 Jun;51(3):426–430. doi: 10.1042/bj0510426. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. PATTERSON M. S., GREENE R. C. MEASUREMENT OF LOW ENERGY BETA-EMITTERS IN AQUEOUS SOLUTION BY LIQUID SCINTILLATION COUNTING OF EMULSIONS. Anal Chem. 1965 Jun;37:854–857. doi: 10.1021/ac60226a017. [DOI] [PubMed] [Google Scholar]
  21. REISSIG J. L., STORMINGER J. L., LELOIR L. F. A modified colorimetric method for the estimation of N-acetylamino sugars. J Biol Chem. 1955 Dec;217(2):959–966. [PubMed] [Google Scholar]
  22. REYNOLDS P. E. Studies on the mode of action of vancomycin. Biochim Biophys Acta. 1961 Sep 16;52:403–405. doi: 10.1016/0006-3002(61)90698-9. [DOI] [PubMed] [Google Scholar]
  23. Siewert G., Strominger J. L. Bacitracin: an inhibitor of the dephosphorylation of lipid pyrophosphate, an intermediate in the biosynthesis of the peptidoglycan of bacterial cell walls. Proc Natl Acad Sci U S A. 1967 Mar;57(3):767–773. doi: 10.1073/pnas.57.3.767. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. TREVELYAN W. E., PROCTER D. P., HARRISON J. S. Detection of sugars on paper chromatograms. Nature. 1950 Sep 9;166(4219):444–445. doi: 10.1038/166444b0. [DOI] [PubMed] [Google Scholar]
  25. Watkinson R. J., Hussey H., Baddiley J. Shared lipid phosphate carrier in the biosynthesis of teichoic acid and peptidoglycan. Nat New Biol. 1971 Jan 13;229(2):57–59. doi: 10.1038/newbio229057a0. [DOI] [PubMed] [Google Scholar]

Articles from Biochemical Journal are provided here courtesy of The Biochemical Society

RESOURCES