1887

Abstract

Teichoic acids (TAs) are important for growth, biofilm formation, adhesion and virulence of Gram-positive bacterial pathogens. The chemical structures of the TAs vary between bacteria, though they typically consist of zwitterionic polymers that are anchored to either the peptidoglycan layer as in the case of wall teichoic acid (WTA) or the cell membrane and named lipoteichoic acid (LTA). The polymers are modified with -alanines and a lack of this decoration leads to increased susceptibility to cationic antimicrobial peptides. Four proteins, DltA–D, are essential for the incorporation of -alanines into cell wall polymers and it has been established that DltA transfers -alanines in the cytoplasm of the cell onto the carrier protein DltC. However, two conflicting models have been proposed for the remainder of the mechanism. Using a cellular protein localization and membrane topology analysis, we show here that DltC does not traverse the membrane and that DltD is anchored to the outside of the cell. These data are in agreement with the originally proposed model for -alanine incorporation through a process that has been proposed to proceed via a -alanine undecaprenyl phosphate membrane intermediate. Furthermore, we found that WTA isolated from a strain lacking LTA contains only a small amount of -alanine, indicating that LTA has a role, either direct or indirect, in the efficient -alanine incorporation into WTA in living cells.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.069898-0
2013-09-01
2024-10-04
Loading full text...

Full text loading...

/deliver/fulltext/micro/159/9/1868.html?itemId=/content/journal/micro/10.1099/mic.0.069898-0&mimeType=html&fmt=ahah

References

  1. Bernal P., Zloh M., Taylor P. W.( 2009). Disruption of  -alanyl esterification of Staphylococcus aureus cell wall teichoic acid by the β-lactam resistance modifier (−)-epicatechin gallate. J Antimicrob Chemother 63:1156–1162 [View Article][PubMed]
    [Google Scholar]
  2. Brown S., Zhang Y. H., Walker S.( 2008). A revised pathway proposed for Staphylococcus aureus wall teichoic acid biosynthesis based on in vitro reconstitution of the intracellular steps. Chem Biol 15:12–21 [View Article][PubMed]
    [Google Scholar]
  3. Brown S., Xia G., Luhachack L. G., Campbell J., Meredith T. C., Chen C., Winstel V., Gekeler C., Irazoqui J. E.& other authors ( 2012). Methicillin resistance in Staphylococcus aureus requires glycosylated wall teichoic acids. Proc Natl Acad Sci U S A 109:18909–18914 [View Article][PubMed]
    [Google Scholar]
  4. Bubeck Wardenburg J., Schneewind O.( 2008). Vaccine protection against Staphylococcus aureus pneumonia. J Exp Med 205:287–294 [View Article][PubMed]
    [Google Scholar]
  5. Childs W. C. III, Taron D. J., Neuhaus F. C.( 1985). Biosynthesis of d-alanyl-lipoteichoic acid by Lactobacillus casei: interchain transacylation of d-alanyl ester residues. J Bacteriol 162:1191–1195[PubMed]
    [Google Scholar]
  6. Collins L. V., Kristian S. A., Weidenmaier C., Faigle M., Van Kessel K. P., Van Strijp J. A., Götz F., Neumeister B., Peschel A.( 2002). Staphylococcus aureus strains lacking d-alanine modifications of teichoic acids are highly susceptible to human neutrophil killing and are virulence attenuated in mice. J Infect Dis 186:214–219 [View Article][PubMed]
    [Google Scholar]
  7. Corrigan R. M., Abbott J. C., Burhenne H., Kaever V., Gründling A.( 2011). c-di-AMP is a new second messenger in Staphylococcus aureus with a role in controlling cell size and envelope stress. PLoS Pathog 7:e1002217 [View Article][PubMed]
    [Google Scholar]
  8. Debabov D. V., Heaton M. P., Zhang Q., Stewart K. D., Lambalot R. H., Neuhaus F. C.( 1996). The d-alanyl carrier protein in Lactobacillus casei: cloning, sequencing, and expression of dltC. J Bacteriol 178:3869–3876[PubMed]
    [Google Scholar]
  9. Debabov D. V., Kiriukhin M. Y., Neuhaus F. C.( 2000). Biosynthesis of lipoteichoic acid in Lactobacillus rhamnosus: role of DltD in d-alanylation. J Bacteriol 182:2855–2864 [View Article][PubMed]
    [Google Scholar]
  10. DeDent A., Bae T., Missiakas D. M., Schneewind O.( 2008). Signal peptides direct surface proteins to two distinct envelope locations of Staphylococcus aureus.. EMBO J 27:2656–2668 [View Article][PubMed]
    [Google Scholar]
  11. Du L., He Y., Luo Y.( 2008). Crystal structure and enantiomer selection by d-alanyl carrier protein ligase DltA from Bacillus cereus.. Biochemistry 47:11473–11480 [View Article][PubMed]
    [Google Scholar]
  12. Fischer W.( 1994). Lipoteichoic acid and lipids in the membrane of Staphylococcus aureus.. Med Microbiol Immunol (Berl) 183:61–76 [View Article][PubMed]
    [Google Scholar]
  13. Fischer W., Rösel P., Koch H. U.( 1981). Effect of alanine ester substitution and other structural features of lipoteichoic acids on their inhibitory activity against autolysins of Staphylococcus aureus.. J Bacteriol 146:467–475[PubMed]
    [Google Scholar]
  14. Gross M., Cramton S. E., Götz F., Peschel A.( 2001). Key role of teichoic acid net charge in Staphylococcus aureus colonization of artificial surfaces. Infect Immun 69:3423–3426 [View Article][PubMed]
    [Google Scholar]
  15. Gründling A., Schneewind O.( 2007a). Genes required for glycolipid synthesis and lipoteichoic acid anchoring in Staphylococcus aureus.. J Bacteriol 189:2521–2530 [View Article][PubMed]
    [Google Scholar]
  16. Gründling A., Schneewind O.( 2007b). Synthesis of glycerol phosphate lipoteichoic acid in Staphylococcus aureus.. Proc Natl Acad Sci U S A 104:8478–8483 [View Article][PubMed]
    [Google Scholar]
  17. Haas R., Koch H. U., Fischer W.( 1984). Alanyl turnover from lipoteichoic acid to teichoic acid in Staphylococcus aureus.. FEMS Microbiol Lett 21:27–31 [View Article]
    [Google Scholar]
  18. Hankins J. V., Madsen J. A., Giles D. K., Brodbelt J. S., Trent M. S.( 2012). Amino acid addition to Vibrio cholerae LPS establishes a link between surface remodeling in Gram-positive and Gram-negative bacteria. Proc Natl Acad Sci U S A 109:8722–8727 [View Article][PubMed]
    [Google Scholar]
  19. Heaton M. P., Neuhaus F. C.( 1994). Role of the d-alanyl carrier protein in the biosynthesis of d-alanyl-lipoteichoic acid. J Bacteriol 176:681–690[PubMed]
    [Google Scholar]
  20. Hofmann K.( 2000). A superfamily of membrane-bound O-acyltransferases with implications for wnt signaling. Trends Biochem Sci 25:111–112 [View Article][PubMed]
    [Google Scholar]
  21. Karatsa-Dodgson M., Wörmann M. E., Gründling A.( 2010). In vitro analysis of the Staphylococcus aureus lipoteichoic acid synthase enzyme using fluorescently labeled lipids. J Bacteriol 192:5341–5349 [View Article][PubMed]
    [Google Scholar]
  22. Koch H. U., Haas R., Fischer W.( 1984). The role of lipoteichoic acid biosynthesis in membrane lipid metabolism of growing Staphylococcus aureus.. Eur J Biochem 138:357–363 [View Article][PubMed]
    [Google Scholar]
  23. Koch H. U., Döker R., Fischer W.( 1985). Maintenance of d-alanine ester substitution of lipoteichoic acid by reesterification in Staphylococcus aureus.. J Bacteriol 164:1211–1217[PubMed]
    [Google Scholar]
  24. Kopp U., Roos M., Wecke J., Labischinski H.( 1996). Staphylococcal peptidoglycan interpeptide bridge biosynthesis: a novel antistaphylococcal target?. Microb Drug Resist 2:29–41 [View Article][PubMed]
    [Google Scholar]
  25. Koprivnjak T., Mlakar V., Swanson L., Fournier B., Peschel A., Weiss J. P.( 2006). Cation-induced transcriptional regulation of the dlt operon of Staphylococcus aureus.. J Bacteriol 188:3622–3630 [View Article][PubMed]
    [Google Scholar]
  26. Kristian S. A., Datta V., Weidenmaier C., Kansal R., Fedtke I., Peschel A., Gallo R. L., Nizet V.( 2005). d-alanylation of teichoic acids promotes group a Streptococcus antimicrobial peptide resistance, neutrophil survival, and epithelial cell invasion. J Bacteriol 187:6719–6725 [View Article][PubMed]
    [Google Scholar]
  27. Lambert P. A., Hancock I. C., Baddiley J.( 1975). Influence of alanyl ester residues on the binding of magnesium ions to teichoic acids. Biochem J 151:671–676[PubMed]
    [Google Scholar]
  28. Lu D., Wörmann M. E., Zhang X., Schneewind O., Gründling A., Freemont P. S.( 2009). Structure-based mechanism of lipoteichoic acid synthesis by Staphylococcus aureus LtaS. Proc Natl Acad Sci U S A 106:1584–1589 [View Article][PubMed]
    [Google Scholar]
  29. Mazmanian S. K., Liu G., Jensen E. R., Lenoy E., Schneewind O.( 2000). Staphylococcus aureus sortase mutants defective in the display of surface proteins and in the pathogenesis of animal infections. Proc Natl Acad Sci U S A 97:5510–5515 [View Article][PubMed]
    [Google Scholar]
  30. 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]
  31. Neuhaus F. C., Heaton M. P., Debabov D. V., Zhang Q.( 1996). The dlt operon in the biosynthesis of d-alanyl-lipoteichoic acid in Lactobacillus casei.. Microb Drug Resist 2:77–84 [View Article][PubMed]
    [Google Scholar]
  32. Oku Y., Kurokawa K., Matsuo M., Yamada S., Lee B. L., Sekimizu K.( 2009). Pleiotropic roles of polyglycerolphosphate synthase of lipoteichoic acid in growth of Staphylococcus aureus cells. J Bacteriol 191:141–151 [View Article][PubMed]
    [Google Scholar]
  33. Osman K. T., Du L., He Y., Luo Y.( 2009). Crystal structure of Bacillus cereus d-alanyl carrier protein ligase (DltA) in complex with ATP. J Mol Biol 388:345–355 [View Article][PubMed]
    [Google Scholar]
  34. Perego M., Glaser P., Minutello A., Strauch M. A., Leopold K., Fischer W.( 1995). Incorporation of d-alanine into lipoteichoic acid and wall teichoic acid in Bacillus subtilis. Identification of genes and regulation. J Biol Chem 270:15598–15606 [View Article][PubMed]
    [Google Scholar]
  35. Peschel A., Otto M., Jack R. W., Kalbacher H., Jung G., Götz F.( 1999). Inactivation of the dlt operon in Staphylococcus aureus confers sensitivity to defensins, protegrins, and other antimicrobial peptides. J Biol Chem 274:8405–8410 [View Article][PubMed]
    [Google Scholar]
  36. Poyart C., Pellegrini E., Marceau M., Baptista M., Jaubert F., Lamy M. C., Trieu-Cuot P.( 2003). Attenuated virulence of Streptococcus agalactiae deficient in d-alanyl-lipoteichoic acid is due to an increased susceptibility to defensins and phagocytic cells. Mol Microbiol 49:1615–1625 [View Article][PubMed]
    [Google Scholar]
  37. Reichmann N. T., Gründling A.( 2011). Location, synthesis and function of glycolipids and polyglycerolphosphate lipoteichoic acid in Gram-positive bacteria of the phylum Firmicutes.. FEMS Microbiol Lett 319:97–105 [View Article][PubMed]
    [Google Scholar]
  38. Schirner K., Marles-Wright J., Lewis R. J., Errington J.( 2009). Distinct and essential morphogenic functions for wall- and lipo-teichoic acids in Bacillus subtilis.. EMBO J 28:830–842 [View Article][PubMed]
    [Google Scholar]
  39. Shindou H., Hishikawa D., Harayama T., Yuki K., Shimizu T.( 2009). Recent progress on acyl CoA: lysophospholipid acyltransferase research. J Lipid Res 50:Suppl.S46–S51 [View Article][PubMed]
    [Google Scholar]
  40. Strandén A. M., Ehlert K., Labischinski H., Berger-Bächi B.( 1997). Cell wall monoglycine cross-bridges and methicillin hypersusceptibility in a femAB null mutant of methicillin-resistant Staphylococcus aureus.. J Bacteriol 179:9–16[PubMed]
    [Google Scholar]
  41. Volkman B. F., Zhang Q., Debabov D. V., Rivera E., Kresheck G. C., Neuhaus F. C.( 2001). Biosynthesis of d-alanyl-lipoteichoic acid: the tertiary structure of apo-d-alanyl carrier protein. Biochemistry 40:7964–7972 [View Article][PubMed]
    [Google Scholar]
  42. Walter J., Loach D. M., Alqumber M., Rockel C., Hermann C., Pfitzenmaier M., Tannock G. W.( 2007). d-alanyl ester depletion of teichoic acids in Lactobacillus reuteri 100-23 results in impaired colonization of the mouse gastrointestinal tract. Environ Microbiol 9:1750–1760 [View Article][PubMed]
    [Google Scholar]
  43. Weidenmaier C., Kokai-Kun J. F., Kristian S. A., Chanturiya T., Kalbacher H., Gross M., Nicholson G., Neumeister B., Mond J. J., Peschel A.( 2004). Role of teichoic acids in Staphylococcus aureus nasal colonization, a major risk factor in nosocomial infections. Nat Med 10:243–245 [View Article][PubMed]
    [Google Scholar]
  44. Wörmann M. E., Reichmann N. T., Malone C. L., Horswill A. R., Gründling A.( 2011). Proteolytic cleavage inactivates the Staphylococcus aureus lipoteichoic acid synthase. J Bacteriol 193:5279–5291 [View Article][PubMed]
    [Google Scholar]
  45. 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]
  46. 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]
  47. Yonus H., Neumann P., Zimmermann S., May J. J., Marahiel M. A., Stubbs M. T.( 2008). Crystal structure of DltA. Implications for the reaction mechanism of non-ribosomal peptide synthetase adenylation domains. J Biol Chem 283:32484–32491 [View Article][PubMed]
    [Google Scholar]
/content/journal/micro/10.1099/mic.0.069898-0
Loading
/content/journal/micro/10.1099/mic.0.069898-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error