1887

Abstract

The structural diversity of wall teichoic acid (WTA) was investigated using biochemical and NMR analyses among 19 strains of , of which seven were previously established to contain a glycerol-type backbone, whereas the remaining 12 strains possess ribitol-containing WTA. Despite the fact that the WTAs consisted of identical components, namely phosphoric acid, alditol (glycerol or ribitol) and glucose, comparative analysis of the H and C NMR spectra indicated the presence of six different structures, based on the observed differences in the anomeric signals of glucose residues. To determine the six WTA structures, their repeating units were prepared by alkaline hydrolysis, followed by fractionation on HPLC, and analysis by NMR spectroscopy using synthetic molecules as a reference. The structures of the six isolates were established as 1-α--glucosyl--glycerol 3-phosphate, 1-α--kojibiosyl--glycerol 3-phosphate, 1-α--nigerosyl--glycerol 3-phosphate, 4-α--kojibiosylribitol 1-phosphate and 1,5-linked di-(2,4-di-α--glucosylribitol) phosphate. The backbone structures appeared to be 3,6′-linked poly(1-α--glucosyl--glycerol phosphate) for the glycerol-type WTA and 1,5-linked poly(ribitol phosphate) for the ribitol-containing WTA. Moreover, in the analysis of the alkaline hydrolysates on HPLC, only single structures of repeating units were released from each WTA, indicating the high structural uniformity of the WTA in each strain. Notably, analyses of lipoteichoic acid isolated from representative strains harbouring the six different WTAs revealed the universal presence of a 1,3-linked poly(glycerol phosphate) chain, substituted at C-2 of the glycerol residues with glucose residues. These findings provide fundamental information on WTA structural variability in , which seems likely to play a pivotal role in the physiology of this bacterial species.

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2012-11-01
2024-04-26
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References

  1. Allen R. J. ( 1940). The estimation of phosphorus. Biochem J 34:858–865 [PubMed]
    [Google Scholar]
  2. Ames B. N. ( 1966). Assay of inorganic phosphate, total phosphate and phosphatases. Methods Enzymol 8:115–118 [View Article]
    [Google Scholar]
  3. Andre G., Deghorain M., Bron P. A., van Swam I. I., Kleerebezem M., Hols P., Dufrene Y. F. ( 2011). Fluorescence and atomic force microscopy imaging of wall teichoic acids in Lactobacillus plantarum . ACS Chem Biol 6:366–376 [View Article] [PubMed]
    [Google Scholar]
  4. Archibald A. R., Coapes H. E. ( 1971). The wall teichoic acids of Lactobacillus plantarum N.I.R.D.C106. Location of the phosphodiester groups and separation of the chains. Biochem J 124:449–460 [PubMed]
    [Google Scholar]
  5. Archibald A. R., Baddiley J., Buchanan J. G. ( 1961). The ribitol teichoic acid from Lactobacillus arabinosus walls: isolation and structure of ribitol glucosides. Biochem J 81:124–134 [PubMed]
    [Google Scholar]
  6. Armstrong J. J., Baddiley J., Buchanan J. G. ( 1960). Structure of the ribitol teichoic acid from the walls of Bacillus subtilis . Biochem J 76:610–621 [PubMed]
    [Google Scholar]
  7. Baddiley J., Buchanan J. G., Rajbhandary U. L., Sanderson A. R. ( 1962). Teichoic acid from the walls of Staphylococcus aureus H. Structure of the N-acetylglucosaminyl-ribitol residues. Biochem J 82:439–448 [PubMed]
    [Google Scholar]
  8. Cheng Y., Promadej N., Kim J. W., Kathariou S. ( 2008). Teichoic acid glycosylation mediated by gtcA is required for phage adsorption and susceptibility of Listeria monocytogenes serotype 4b. Appl Environ Microbiol 74:1653–1655 [View Article] [PubMed]
    [Google Scholar]
  9. D’Elia M. A., Millar K. E., Beveridge T. J., Brown E. D. ( 2006a). Wall teichoic acid polymers are dispensable for cell viability in Bacillus subtilis . J Bacteriol 188:8313–8316 [View Article] [PubMed]
    [Google Scholar]
  10. D’Elia M. A., Pereira M. P., Chung Y. S., Zhao W., Chau A., Kenney T. J., Sulavik M. C., Black T. A., Brown E. D. ( 2006b). Lesions in teichoic acid biosynthesis in Staphylococcus aureus lead to a lethal gain of function in the otherwise dispensable pathway. J Bacteriol 188:4183–4189 [View Article] [PubMed]
    [Google Scholar]
  11. De Boer W. R., Kruyssen F. J., Wouters J. T. M., Kruk C. ( 1976). The structure of teichoic acid from Bacillus subtilis var. niger WM as determined by C nuclear-magnetic-resonance spectroscopy. Eur J Biochem 62:1–6 [View Article] [PubMed]
    [Google Scholar]
  12. Delcour J., Ferain T., Deghorain M., Palumbo E., Hols P. ( 1999). The biosynthesis and functionality of the cell-wall of lactic acid bacteria. Antonie van Leeuwenhoek 76:159–184 [View Article] [PubMed]
    [Google Scholar]
  13. DuBois M., Gilles K. A., Hamilton J. K., Rebers P. A., Smith F. ( 1956). Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356 [View Article]
    [Google Scholar]
  14. Endl J., Seidl H. P., Fiedler F., Schleider K. H. ( 1983). Chemical composition and structure of cell wall teichoic acids of staphylococci. Arch Microbiol 135:215–223 [View Article] [PubMed]
    [Google Scholar]
  15. Eugster M. R., Haug M. C., Huwiler S. G., Loessner M. J. ( 2011). The cell wall binding domain of Listeria bacteriophage endolysin PlyP35 recognizes terminal GlcNAc residues in cell wall teichoic acid. Mol Microbiol 81:1419–1432 [View Article] [PubMed]
    [Google Scholar]
  16. García E., García J. L., García P., Arrarás A., Sánchez-Puelles J. M., López R. ( 1988). Molecular evolution of lytic enzymes of Streptococcus pneumoniae and its bacteriophages. Proc Natl Acad Sci U S A 85:914–918 [View Article] [PubMed]
    [Google Scholar]
  17. Jang K. S., Baik J. E., Han S. H., Chung D. K., Kim B. G. ( 2011). Multi-spectrometric analyses of lipoteichoic acids isolated from Lactobacillus plantarum . Biochem Biophys Res Commun 407:823–830 [View Article] [PubMed]
    [Google Scholar]
  18. Kandler O., Weiss N. ( 1986). Genus Lactobacillus Beijerinck 1901, 212AL. Bergey’s Manual of Systematic Bacteriology1209–1234 Sneath P. H. A., Mair N. S., Sharpe M. E., Holt J. G. Baltimore, MD: Williams & Wilkins;
    [Google Scholar]
  19. Kelemen M. V., Baddiley J. ( 1961). Structure of the intracellular glycerol teichoic acid from Lactobacillus casei A.T.C.C. 7469. Biochem J 80:246–254 [PubMed]
    [Google Scholar]
  20. Kleerebezem M., Boekhorst J., van Kranenburg R., Molenaar D., Kuipers O. P., Leer R., Tarchini R., Peters S. A., Sandbrink H. M. & other authors ( 2003). Complete genome sequence of Lactobacillus plantarum WCFS1. Proc Natl Acad Sci U S A 100:1990–1995 [View Article] [PubMed]
    [Google Scholar]
  21. Kleerebezem M., Hols P., Bernard E., Rolain T., Zhou M., Siezen R. J., Bron P. A. ( 2010). The extracellular biology of the lactobacilli. FEMS Microbiol Rev 34:199–230 [View Article] [PubMed]
    [Google Scholar]
  22. Lei X. H., Fiedler F., Lan Z., Kathariou S. ( 2001). A novel serotype-specific gene cassette (gltA-gltB) is required for expression of teichoic acid-associated surface antigens in Listeria monocytogenes of serotype 4b. J Bacteriol 183:1133–1139 [View Article] [PubMed]
    [Google Scholar]
  23. Morath S., Geyer A., Hartung T. ( 2001). Structure–function relationship of cytokine induction by lipoteichoic acid from Staphylococcus aureus . J Exp Med 193:393–398 [View Article] [PubMed]
    [Google Scholar]
  24. Naumova I. B., Shashkov A. S., Tul’skaya E. M., Streshinskaya G. M., Kozlova Y. I., Potekhina N. V., Evtushenko L. I., Stackebrandt E. ( 2001). Cell wall teichoic acids: structural diversity, species specificity in the genus Nocardiopsis, and chemotaxonomic perspective. FEMS Microbiol Rev 25:269–283 [View Article] [PubMed]
    [Google Scholar]
  25. Neuhaus F. C., Baddiley J. ( 2003). A continuum of anionic charge: structures and functions of d-alanyl-teichoic acids in Gram-positive bacteria. Microbiol Mol Biol Rev 67:686–723 [View Article] [PubMed]
    [Google Scholar]
  26. Pooley H. M., Paschoud D., Karamata D. ( 1987). The gtaB marker in Bacillus subtilis 168 is associated with a deficiency in UDPglucose pyrophosphorylase. J Gen Microbiol 133:3481–3493 [PubMed]
    [Google Scholar]
  27. Potekhina N. V., Shashkov A. S., Evtushenko L. I., Senchenkova S. N., Naumova I. B. ( 2003). A mannitol teichoic acid containing rhamnose and pyruvic acid acetal from the cell wall of Brevibacterium permense VKM Ac‐2280. Carbohydr Res 338:2745–2749 [PubMed] [CrossRef]
    [Google Scholar]
  28. Potekhina N. V., Tul'skaya E. M., Naumova I. B., Shashkov A. S., Evtushenko I. L. ( 1993). Erythritolteichoic acid in the cell wall of Glycomyces tenuis VKM Ac-1250. Eur J Biochem 218:371–375 [PubMed] [CrossRef]
    [Google Scholar]
  29. Räisänen L., Draing C., Pfitzenmaier M., Schubert K., Jaakonsaari T., von Aulock S., Hartung T., Alatossava T. ( 2007). Molecular interaction between lipoteichoic acids and Lactobacillus delbrueckii phages depends on d-alanyl and α-glucose substitution of poly(glycerophosphate) backbones. J Bacteriol 189:4135–4140 [CrossRef]
    [Google Scholar]
  30. Sadovskaya I., Vinogradov E., Li J., Jabbouri S. ( 2004). Structural elucidation of the extracellular and cell-wall teichoic acids of Staphylococcus epidermidis RP62A, a reference biofilm-positive strain. Carbohydr Res 339:1467–1473 [View Article] [PubMed]
    [Google Scholar]
  31. Sánchez Carballo P. M., Vilen H., Palva A., Holst O. ( 2010). Structural characterization of teichoic acids from Lactobacillus brevis . Carbohydr Res 345:538–542 [View Article] [PubMed]
    [Google Scholar]
  32. Shashkov A. S., Streshinskaya G. M., Gnilozub V. A., Evtushenko L. I., Naumova I. B. ( 1995). Poly(arabitol phosphate) teichoic acid in the cell wall of Agromyces cerinus subsp. cerinus VKM Ac-1340T. FEBS Lett 371:163–166 [View Article] [PubMed]
    [Google Scholar]
  33. Shaw N., Baddiley J. ( 1964). The teichoic acid from the walls of Lactobacillus buchneri N.C.I.B. 8007. Biochem J 93:317–321 [PubMed]
    [Google Scholar]
  34. Tomita S., Furihata K., Nukada T., Satoh E., Uchimura T., Okada S. ( 2009). Structures of two monomeric units of teichoic acid prepared from the cell wall of Lactobacillus plantarum NRIC 1068. Biosci Biotechnol Biochem 73:530–535 [View Article] [PubMed]
    [Google Scholar]
  35. Tomita S., Irisawa T., Tanaka N., Nukada T., Satoh E., Uchimura T., Okada S. ( 2010). Comparison of components and synthesis genes of cell wall teichoic acid among Lactobacillus plantarum strains. Biosci Biotechnol Biochem 74:928–933 [View Article] [PubMed]
    [Google Scholar]
  36. Uchikawa K., Sekikawa I., Azuma I. ( 1986). Structural studies on teichoic acids in cell walls of several serotypes of Listeria monocytogenes . J Biochem 99:315–327 [PubMed]
    [Google Scholar]
  37. van der Veen J. M. ( 1963). An n.m.r. study of the glycoside link in glycosides of glucose and galactose. J Org Chem 28:564–566 [View Article]
    [Google Scholar]
  38. Vinogradov E., Sadovskaya I., Li J., Jabbouri S. ( 2006). Structural elucidation of the extracellular and cell-wall teichoic acids of Staphylococcus aureus MN8m, a biofilm forming strain. Carbohydr Res 341:738–743 [View Article] [PubMed]
    [Google Scholar]
  39. Vollmer W. ( 2008). Structural variation in the glycan strands of bacterial peptidoglycan. FEMS Microbiol Rev 32:287–306 [View Article] [PubMed]
    [Google Scholar]
  40. Wang Y., Chen C., Ai L., Zhou F., Zhou Z., Wang L., Zhang H., Chen W., Guo B. ( 2011). Complete genome sequence of the probiotic Lactobacillus plantarum ST-III. J Bacteriol 193:313–314 [View Article] [PubMed]
    [Google Scholar]
  41. Weidenmaier C., Peschel A. ( 2008). Teichoic acids and related cell-wall glycopolymers in Gram-positive physiology and host interactions. Nat Rev Microbiol 6:276–287 [View Article] [PubMed]
    [Google Scholar]
  42. Wicken A. J., Baddiley J. ( 1963). Structure of intracellular teichoic acids from group D streptococci. Biochem J 87:54–62 [PubMed]
    [Google Scholar]
  43. Xia G., Kohler T., Peschel A. ( 2010a). The wall teichoic acid and lipoteichoic acid polymers of Staphylococcus aureus . Int J Med Microbiol 300:148–154 [View Article] [PubMed]
    [Google Scholar]
  44. Xia G., Maier L., Sanchez-Carballo P., Li M., Otto M., Holst O., Peschel A. ( 2010b). Glycosylation of wall teichoic acid in Staphylococcus aureus by TarM. J Biol Chem 285:13405–13415 [View Article] [PubMed]
    [Google Scholar]
  45. Yamamoto H., Miyake Y., Hisaoka M., Kurosawa S., Sekiguchi J. ( 2008). The major and minor wall teichoic acids prevent the sidewall localization of vegetative dl-endopeptidase LytF in Bacillus subtilis . Mol Microbiol 70:297–310 [View Article] [PubMed]
    [Google Scholar]
  46. Young F. E. ( 1967). Requirement of glucosylated teichoic acid for adsorption of phage in Bacillus subtilis 168. Proc Natl Acad Sci U S A 58:2377–2384 [View Article] [PubMed]
    [Google Scholar]
  47. Zhang Z. Y., Liu C., Zhu Y. Z., Zhong Y., Zhu Y. Q., Zheng H. J., Zhao G. P., Wang S. Y., Guo X. K. ( 2009). Complete genome sequence of Lactobacillus plantarum JDM1. J Bacteriol 191:5020–5021 [View Article] [PubMed]
    [Google Scholar]
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