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. 1985 Jun;162(3):1191–1195. doi: 10.1128/jb.162.3.1191-1195.1985

Biosynthesis of D-alanyl-lipoteichoic acid by Lactobacillus casei: interchain transacylation of D-alanyl ester residues.

W C Childs 3rd, D J Taron, F C Neuhaus
PMCID: PMC215903  PMID: 3922942

Abstract

Lipoteichoic acid (LTA) from Lactobacillus casei contains poly(glycerophosphate) substituted with D-alanyl ester residues. The distribution of these residues in the in vitro-synthesized polymer is uniform. Esterification of LTA with D-alanine may occur in one of two modes: (i) addition at random or (ii) addition at a defined locus in the poly(glycerophosphate) chain followed by redistribution of the ester residues. A time-dependent transacylation of these residues from D-[14C]alanyl-lipophilic LTA to hydrophilic acceptor was observed. The hydrophilic acceptor was characterized as D-alanyl-hydrophilic LTA. This transacylation requires neither ATP nor the D-alanine incorporation system, i.e., the D-alanine activating enzyme and D-alanine:membrane acceptor ligase. No evidence for an enzyme-catalyzed transacylation reaction was observed. We propose that this process of transacylation may be responsible for the redistribution of D-alanyl residues after esterification to the poly(glycerophosphate). As a result, it is difficult to distinguish between these proposed modes of addition.

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Selected References

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  1. 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]
  2. Brautigan V. M., Childs W. C., 3rd, Neuhaus F. C. Biosynthesis of D-alanyl-lipoteichoic acid in Lactobacillus casei: D-alanyl-lipophilic compounds as intermediates. J Bacteriol. 1981 Apr;146(1):239–250. doi: 10.1128/jb.146.1.239-250.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Cabacungan E., Pieringer R. A. Mode of elongation of the glycerol phosphate polymer of membrane lipoteichoic acid of Streptococcus faecium ATCC 9790. J Bacteriol. 1981 Jul;147(1):75–79. doi: 10.1128/jb.147.1.75-79.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Childs W. C., 3rd, Neuhaus F. C. Biosynthesis of D-alanyl-lipoteichoic acid: characterization of ester-linked D-alanine in the in vitro-synthesized product. J Bacteriol. 1980 Jul;143(1):293–301. doi: 10.1128/jb.143.1.293-301.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Fischer W. D-alanine ester-containing glycerophosphoglycolipids in the membrane of gram-positive bacteria. Biochim Biophys Acta. 1982 May 13;711(2):372–375. doi: 10.1016/0005-2760(82)90048-0. [DOI] [PubMed] [Google Scholar]
  6. Fischer W., Koch H. U., Rösel P., Fiedler F. Alanine ester-containing native lipoteichoic acids do not act as lipoteichoic acid carrier. Isolation, structural and functional characterization. J Biol Chem. 1980 May 25;255(10):4557–4562. [PubMed] [Google Scholar]
  7. Fischer W., Laine R. A., Nakano M. On the relationship between glycerophosphoglycolipids and lipoteichoic acids in Gram-positive bacteria. II. Structures of glycerophosphoglycolipids. Biochim Biophys Acta. 1978 Mar 30;528(3):298–308. doi: 10.1016/0005-2760(78)90019-x. [DOI] [PubMed] [Google Scholar]
  8. Fischer W., Nakano M., Laine R. A., Bohrer W. On the relationship between glycerophosphoglycolipids and lipoteichoic acids in Gram-positive bacteria. I. The occurrence of phosphoglycolipids. Biochim Biophys Acta. 1978 Mar 30;528(3):288–297. doi: 10.1016/0005-2760(78)90018-8. [DOI] [PubMed] [Google Scholar]
  9. Fischer W., Rösel P., Koch H. U. Effect of alanine ester substitution and other structural features of lipoteichoic acids on their inhibitory activity against autolysins of Staphylococcus aureus. J Bacteriol. 1981 May;146(2):467–475. doi: 10.1128/jb.146.2.467-475.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. 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]
  11. Laine R. A., Fischer W. On the relationship between glycerophosphoglycolipids and lipoteichoic acids of gram-positive bacteria. III. Di(glycerophospho)-acylkojibiosyldiacylglycerol and related compounds from Streptococcus lactis NCDO 712. Biochim Biophys Acta. 1978 May 25;529(2):250–262. doi: 10.1016/0005-2760(78)90068-1. [DOI] [PubMed] [Google Scholar]
  12. Lambert P. A., Hancock I. C., Baddiley J. Influence of alanyl ester residues on the binding of magnesium ions to teichoic acids. Biochem J. 1975 Dec;151(3):671–676. doi: 10.1042/bj1510671. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Lambert P. A., Hancock I. C., Baddiley J. Occurrence and function of membrane teichoic acids. Biochim Biophys Acta. 1977 May 31;472(1):1–12. doi: 10.1016/0304-4157(77)90012-0. [DOI] [PubMed] [Google Scholar]
  14. Linzer R., Neuhaus F. C. Biosynthesis of membrane teichoic acid. A role of the D-alanine-activating enzyme. J Biol Chem. 1973 May 10;248(9):3196–3201. [PubMed] [Google Scholar]
  15. Loftfield R. B. The mechanism of aminoacylation of transfer RNA. Prog Nucleic Acid Res Mol Biol. 1972;12:87–128. doi: 10.1016/s0079-6603(08)60660-1. [DOI] [PubMed] [Google Scholar]
  16. Naumova I. B. Teikhoevye Kisloty v peguliatsii Viokhimicheskikh Protsessov u mikroorganizmov. Biokhimiia. 1978 Feb;43(2):195–207. [PubMed] [Google Scholar]
  17. Neuhaus F. C., Linzer R., Reusch V. M., Jr Biosynthesis of membrane teichoic acid: role of the D-alanine-activating enzyme and D-alanine: membrane acceptor ligase. Ann N Y Acad Sci. 1974 May 10;235(0):502–518. doi: 10.1111/j.1749-6632.1974.tb43287.x. [DOI] [PubMed] [Google Scholar]
  18. 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]
  19. Reusch V. M., Jr, Neuhaus F. C. D-Alanine: membrane acceptor ligase from Lactobacillus casei. J Biol Chem. 1971 Oct 25;246(20):6136–6143. [PubMed] [Google Scholar]
  20. SHABAROVA Z. A., HUGHES N. A., BADDILEY J. The influence of adjacent phosphate and hydroxyl groups on amino acid esters. Biochem J. 1962 Apr;83:216–219. doi: 10.1042/bj0830216. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Schneider J. E., Kennedy E. P. A novel phosphodiesterase from Aspergillus niger and its application to the study of membrane-derived oligosaccharides and other glycerol-containing biopolymers. J Biol Chem. 1978 Nov 10;253(21):7738–7743. [PubMed] [Google Scholar]
  22. Taron D. J., Childs W. C., 3rd, Neuhaus F. C. Biosynthesis of D-alanyl-lipoteichoic acid: role of diglyceride kinase in the synthesis of phosphatidylglycerol for chain elongation. J Bacteriol. 1983 Jun;154(3):1110–1116. doi: 10.1128/jb.154.3.1110-1116.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]

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