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. 1994 Jul;176(14):4321–4327. doi: 10.1128/jb.176.14.4321-4327.1994

Replacement of diaminopimelic acid by cystathionine or lanthionine in the peptidoglycan of Escherichia coli.

D Mengin-Lecreulx 1, D Blanot 1, J van Heijenoort 1
PMCID: PMC205645  PMID: 8021219

Abstract

In Escherichia coli, auxotrophy for diaminopimelic acid (A2pm) can be suppressed by growth with exogenous cystathionine or lanthionine. The incorporation of cystathionine into peptidoglycan metabolism was examined with a dapA metC mutant, whereas for lanthionine, a dapA metA mutant strain was used. Analysis of peptidoglycan precursors and sacculi isolated from cells grown with epimeric cystathionine or lanthionine showed that meso-A2pm was totally replaced in the same position by either sulfur-containing amino acid. Moreover, mainly L-allo-cystathionine (95%) or meso-lanthionine (93%) was incorporated into the precursors and sacculi. For this purpose, a new, efficient high-pressure liquid chromatography (HPLC) technique for analysis of the cystathionine isomers was developed. The formation of the UDP-MurNAc tripeptide appeared to be a critical step, since the MurE synthetase accepted meso-lanthionine or D-allo- or L-allo-cystathionine in vitro as good substrates, although with higher Km values. Presumably, the 10-fold-higher UDP-MurNAc-L-Ala-D-Glu pool of cells grown with cystathionine or lanthionine ensured a normal rate of synthesis. The kinetic parameters of the MurF synthetase catalyzing the addition of D-alanyl-D-alanine were very similar for the meso-A2pm-,L-allo-cystathionine-, and meso-lanthionine-containing UDP-MurNAc tripeptides. HPLC analysis of the soluble fragments resulting from 95% digestion by Chalaropsis N-acetylmuramidase of the peptidoglycan material in isolated sacculi revealed that the proportion of the main dimer was far lower in cystathionine and lanthionine sacculi.

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Selected References

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  1. Berger E. A., Heppel L. A. A binding protein involved in the transport of cystine and diaminopimelic acid in Escherichia coli. J Biol Chem. 1972 Dec 10;247(23):7684–7694. [PubMed] [Google Scholar]
  2. Chaloupka J., Strnadová M., Cáslavská J., Veres K. Growth and cell division of Escherichia coli 173-25 in the presence of some analogues of diaminopimelic acid. Z Allg Mikrobiol. 1974;14(4):283–296. doi: 10.1002/jobm.3630140403. [DOI] [PubMed] [Google Scholar]
  3. Dezélée P., Bricas E. Structure of the peptidoglycan in Escherichia coli B and Bacillus megaterium KM. Stereospecific synthesis of two meso-diaminopimelic acid peptides with the tetrapeptide subunit of bacterial cell wall peptidoglycan. Biochemistry. 1970 Feb 17;9(4):823–831. doi: 10.1021/bi00806a015. [DOI] [PubMed] [Google Scholar]
  4. Duncan K., van Heijenoort J., Walsh C. T. Purification and characterization of the D-alanyl-D-alanine-adding enzyme from Escherichia coli. Biochemistry. 1990 Mar 6;29(9):2379–2386. doi: 10.1021/bi00461a023. [DOI] [PubMed] [Google Scholar]
  5. Flouret B., Mengin-Lecreulx D., van Heijenoort J. Reverse-phase high-pressure liquid chromatography of uridine diphosphate N-acetylmuramyl peptide precursors of bacterial cell wall peptidoglycan. Anal Biochem. 1981 Jun;114(1):59–63. doi: 10.1016/0003-2697(81)90451-6. [DOI] [PubMed] [Google Scholar]
  6. Girodeau J. M., Agouridas C., Masson M., Pineau R., Le Goffic F. The lysine pathway as a target for a new genera of synthetic antibacterial antibiotics? J Med Chem. 1986 Jun;29(6):1023–1030. doi: 10.1021/jm00156a021. [DOI] [PubMed] [Google Scholar]
  7. Glauner B., Höltje J. V., Schwarz U. The composition of the murein of Escherichia coli. J Biol Chem. 1988 Jul 25;263(21):10088–10095. [PubMed] [Google Scholar]
  8. Glauner B. Separation and quantification of muropeptides with high-performance liquid chromatography. Anal Biochem. 1988 Aug 1;172(2):451–464. doi: 10.1016/0003-2697(88)90468-x. [DOI] [PubMed] [Google Scholar]
  9. Kawamoto I., Oka T., Nara T. Cell wall composition of Micromonospora olivoasterospora, Micromonospora sagamiensis, and related organisms. J Bacteriol. 1981 May;146(2):527–534. doi: 10.1128/jb.146.2.527-534.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Knüsel F., Nüesch J., Scherrer M., Schmid K. Einfluss von Lanthionin auf das Wachstum einer Diaminopimelinsäure-heterotrophen Mutante von Escherichia coli. Pathol Microbiol (Basel) 1967;30(6):871–879. [PubMed] [Google Scholar]
  11. Mengin-Lecreulx D., Flouret B., van Heijenoort J. Cytoplasmic steps of peptidoglycan synthesis in Escherichia coli. J Bacteriol. 1982 Sep;151(3):1109–1117. doi: 10.1128/jb.151.3.1109-1117.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Mengin-Lecreulx D., Flouret B., van Heijenoort J. Pool levels of UDP N-acetylglucosamine and UDP N-acetylglucosamine-enolpyruvate in Escherichia coli and correlation with peptidoglycan synthesis. J Bacteriol. 1983 Jun;154(3):1284–1290. doi: 10.1128/jb.154.3.1284-1290.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Mengin-Lecreulx D., Michaud C., Richaud C., Blanot D., van Heijenoort J. Incorporation of LL-diaminopimelic acid into peptidoglycan of Escherichia coli mutants lacking diaminopimelate epimerase encoded by dapF. J Bacteriol. 1988 May;170(5):2031–2039. doi: 10.1128/jb.170.5.2031-2039.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Mengin-Lecreulx D., van Heijenoort J. Effect of growth conditions on peptidoglycan content and cytoplasmic steps of its biosynthesis in Escherichia coli. J Bacteriol. 1985 Jul;163(1):208–212. doi: 10.1128/jb.163.1.208-212.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Michaud C., Blanot D., Flouret B., Van Heijenoort J. Partial purification and specificity studies of the D-glutamate-adding and D-alanyl-D-alanine-adding enzymes from Escherichia coli K12. Eur J Biochem. 1987 Aug 3;166(3):631–637. doi: 10.1111/j.1432-1033.1987.tb13560.x. [DOI] [PubMed] [Google Scholar]
  16. Michaud C., Mengin-Lecreulx D., van Heijenoort J., Blanot D. Over-production, purification and properties of the uridine-diphosphate-N-acetylmuramoyl-L-alanyl-D-glutamate: meso-2,6-diaminopimelate ligase from Escherichia coli. Eur J Biochem. 1990 Dec 27;194(3):853–861. doi: 10.1111/j.1432-1033.1990.tb19479.x. [DOI] [PubMed] [Google Scholar]
  17. Nanninga N. Cell division and peptidoglycan assembly in Escherichia coli. Mol Microbiol. 1991 Apr;5(4):791–795. doi: 10.1111/j.1365-2958.1991.tb00751.x. [DOI] [PubMed] [Google Scholar]
  18. Perkins H. R. The configuration of 2,6-diamino-3-hydroxypimelic acid in microbial cell walls. Biochem J. 1969 Dec;115(4):797–805. doi: 10.1042/bj1150797. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. RHULAND L. E., HAMILTON R. D. The functional pathway of lysine biosynthesis in Escherichia coli. Biochim Biophys Acta. 1961 Aug 19;51:525–528. doi: 10.1016/0006-3002(61)90609-6. [DOI] [PubMed] [Google Scholar]
  20. RHULAND L. E. Role of alpha, epsilon-diaminopimelic acid in the cellular integrity of Escherichia coli. J Bacteriol. 1957 Jun;73(6):778–783. doi: 10.1128/jb.73.6.778-783.1957. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Richaud C., Higgins W., Mengin-Lecreulx D., Stragier P. Molecular cloning, characterization, and chromosomal localization of dapF, the Escherichia coli gene for diaminopimelate epimerase. J Bacteriol. 1987 Apr;169(4):1454–1459. doi: 10.1128/jb.169.4.1454-1459.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Richaud C., Mengin-Lecreulx D., Pochet S., Johnson E. J., Cohen G. N., Marlière P. Directed evolution of biosynthetic pathways. Recruitment of cysteine thioethers for constructing the cell wall of Escherichia coli. J Biol Chem. 1993 Dec 25;268(36):26827–26835. [PubMed] [Google Scholar]
  23. Schwarz U., Asmus A., Frank H. Autolytic enzymes and cell division of Escherichia coli. J Mol Biol. 1969 May 14;41(3):419–429. doi: 10.1016/0022-2836(69)90285-x. [DOI] [PubMed] [Google Scholar]
  24. Sundharadas G., Gilvarg C. A new synthesis and some biological properties of beta-hydroxy-alpha, epsilon-diaminopimelic acid. J Biol Chem. 1966 Jul 25;241(14):3276–3282. [PubMed] [Google Scholar]
  25. Van Heijenoort J., Elbaz L., Dezélée P., Petit J. F., Bricas E., Ghuysen J. M. Structure of the meso-diaminopimelic acid containing peptidoglycans in Escherichia coli B and Bacillus megaterium KM. Biochemistry. 1969 Jan;8(1):207–213. doi: 10.1021/bi00829a030. [DOI] [PubMed] [Google Scholar]
  26. Vasstrand E., Jensen H. B., Miron T. Microbore single-column analysis of amino acids and amino sugars specific to bacterial cell wall peptidoglycans. Anal Biochem. 1980 Jun;105(1):154–158. doi: 10.1016/0003-2697(80)90438-8. [DOI] [PubMed] [Google Scholar]
  27. WILKINSON G. N. Statistical estimations in enzyme kinetics. Biochem J. 1961 Aug;80:324–332. doi: 10.1042/bj0800324. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. de Roubin M. R., Mengin-Lecreulx D., van Heijenoort J. Peptidoglycan biosynthesis in Escherichia coli: variations in the metabolism of alanine and D-alanyl-D-alanine. J Gen Microbiol. 1992 Aug;138(Pt 8):1751–1757. doi: 10.1099/00221287-138-8-1751. [DOI] [PubMed] [Google Scholar]

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