This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Kovács, M.
Right arrow Articles by Brückner, R.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Kovács, M.
Right arrow Articles by Brückner, R.

 Previous Article  |  Next Article 

Journal of Bacteriology, August 2006, p. 5797-5805, Vol. 188, No. 16
0021-9193/06/$08.00+0     doi:10.1128/JB.00336-06
Copyright © 2006, American Society for Microbiology. All Rights Reserved.

A Functional dlt Operon, Encoding Proteins Required for Incorporation of D-Alanine in Teichoic Acids in Gram-Positive Bacteria, Confers Resistance to Cationic Antimicrobial Peptides in Streptococcus pneumoniae

Márta Kovács,1 Alexander Halfmann,1 Iris Fedtke,2 Manuel Heintz,1 Andreas Peschel,2 Waldemar Vollmer,3 Regine Hakenbeck,1 and Reinhold Brückner1*

Department of Microbiology, University of Kaiserslautern, D-67663 Kaiserslautern, Germany,1 Cellular and Molecular Microbiology, Department of Medical Microbiology and Hygiene, University of Tübingen, D-72076 Tübingen, Germany,2 Department of Microbial Genetics, University of Tübingen, D-72076 Tübingen, Germany3

Received 8 March 2006/ Accepted 26 May 2006

Streptococcus pneumoniae is one of the few species within the group of low-G +C gram-positive bacteria reported to contain no D-alanine in teichoic acids, although the dltABCD operon encoding proteins responsible for D-alanylation is present in the genomes of two S. pneumoniae strains, the laboratory strain R6 and the clinical isolate TIGR4. The annotation of dltA in R6 predicts a protein, D-alanine-D-alanyl carrier protein ligase (Dcl), that is shorter at the amino terminus than all other Dcl proteins. Translation of dltA could also start upstream of the annotated TTG start codon at a GTG, resulting in the premature termination of dltA translation at a stop codon. Applying a novel integrative translation probe plasmid with Escherichia coli 'lacZ as a reporter, we could demonstrate that dltA translation starts at the upstream GTG. Consequently, S. pneumoniae R6 is a dltA mutant, whereas S. pneumoniae D39, the parental strain of R6, and Rx, another derivative of D39, contained intact dltA genes. Repair of the stop codon in dltA of R6 and insertional inactivation of dltA in D39 and Rx yielded pairs of dltA-deficient and dltA-proficient strains. Subsequent phenotypic analysis showed that dltA inactivation resulted in enhanced sensitivity to the cationic antimicrobial peptides nisin and gallidermin, a phenotype fully consistent with those of dltA mutants of other gram-positive bacteria. In addition, mild alkaline hydrolysis of heat-inactivated whole cells released D-alanine from dltA-proficient strains, but not from dltA mutants. The results of our study suggest that, as in many other low-G+C gram-positive bacteria, teichoic acids of S. pneumoniae contain D-alanine residues in order to protect this human pathogen against the actions of cationic antimicrobial peptides.

* Corresponding author. Mailing address: University of Kaiserslautern, Department of Microbiology, Paul Ehrlich Straße 23, D-67663 Kaiserslautern, Germany. Phone: 49 631 205 2353. Fax: 49 631 205 3799. E-mail: rbrueckn{at}rhrk.uni-kl.de.

Journal of Bacteriology, August 2006, p. 5797-5805, Vol. 188, No. 16
0021-9193/06/$08.00+0     doi:10.1128/JB.00336-06
Copyright © 2006, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Becker, P., Hakenbeck, R., Henrich, B. (2009). An ABC Transporter of Streptococcus pneumoniae Involved in Susceptibility to Vancoresmycin and Bacitracin. Antimicrob. Agents Chemother. 53: 2034-2041 [Abstract] [Full Text]  
  • Samant, S., Hsu, F.-F., Neyfakh, A. A., Lee, H. (2009). The Bacillus anthracis Protein MprF Is Required for Synthesis of Lysylphosphatidylglycerols and for Resistance to Cationic Antimicrobial Peptides. J. Bacteriol. 191: 1311-1319 [Abstract] [Full Text]  
  • Baur, S., Marles-Wright, J., Buckenmaier, S., Lewis, R. J., Vollmer, W. (2009). Synthesis of CDP-Activated Ribitol for Teichoic Acid Precursors in Streptococcus pneumoniae. J. Bacteriol. 191: 1200-1210 [Abstract] [Full Text]  
  • Beiter, K., Wartha, F., Hurwitz, R., Normark, S., Zychlinsky, A., Henriques-Normark, B. (2008). The Capsule Sensitizes Streptococcus pneumoniae to {alpha}-Defensins Human Neutrophil Proteins 1 to 3. Infect. Immun. 76: 3710-3716 [Abstract] [Full Text]  
  • Fittipaldi, N., Sekizaki, T., Takamatsu, D., Harel, J., Dominguez-Punaro, M. d. l. C., Von Aulock, S., Draing, C., Marois, C., Kobisch, M., Gottschalk, M. (2008). D-Alanylation of Lipoteichoic Acid Contributes to the Virulence of Streptococcus suis. Infect. Immun. 76: 3587-3594 [Abstract] [Full Text]  
  • Giaouris, E., Briandet, R., Meyrand, M., Courtin, P., Chapot-Chartier, M.-P. (2008). Variations in the Degree of D-Alanylation of Teichoic Acids in Lactococcus lactis Alter Resistance to Cationic Antimicrobials but Have No Effect on Bacterial Surface Hydrophobicity and Charge. Appl. Environ. Microbiol. 74: 4764-4767 [Abstract] [Full Text]  
  • Kramer, N. E., Hasper, H. E., van den Bogaard, P. T. C., Morath, S., de Kruijff, B., Hartung, T., Smid, E. J., Breukink, E., Kok, J., Kuipers, O. P. (2008). Increased D-alanylation of lipoteichoic acid and a thickened septum are main determinants in the nisin resistance mechanism of Lactococcus lactis. Microbiology 154: 1755-1762 [Abstract] [Full Text]  
  • Seo, H. S., Cartee, R. T., Pritchard, D. G., Nahm, M. H. (2008). A New Model of Pneumococcal Lipoteichoic Acid Structure Resolves Biochemical, Biosynthetic, and Serologic Inconsistencies of the Current Model. J. Bacteriol. 190: 2379-2387 [Abstract] [Full Text]  
  • Rice, K. C., Bayles, K. W. (2008). Molecular Control of Bacterial Death and Lysis. Microbiol. Mol. Biol. Rev. 72: 85-109 [Abstract] [Full Text]  
  • Formstone, A., Carballido-Lopez, R., Noirot, P., Errington, J., Scheffers, D.-J. (2008). Localization and Interactions of Teichoic Acid Synthetic Enzymes in Bacillus subtilis. J. Bacteriol. 190: 1812-1821 [Abstract] [Full Text]  
  • Harder, J., Glaser, R., Schroder, J.-M. (2007). Review: Human antimicrobial proteins effectors of innate immunity. Innate Immunity 13: 317-338 [Abstract]  
  • Menendez, A., Fernandez, L., Reimundo, P., Guijarro, J. A. (2007). Genes required for Lactococcus garvieae survival in a fish host. Microbiology 153: 3286-3294 [Abstract] [Full Text]  
  • Jordan, S., Rietkotter, E., Strauch, M. A., Kalamorz, F., Butcher, B. G., Helmann, J. D., Mascher, T. (2007). LiaRS-dependent gene expression is embedded in transition state regulation in Bacillus subtilis. Microbiology 153: 2530-2540 [Abstract] [Full Text]  
  • Fittipaldi, N., Gottschalk, M., Vanier, G., Daigle, F., Harel, J. (2007). Use of Selective Capture of Transcribed Sequences To Identify Genes Preferentially Expressed by Streptococcus suis upon Interaction with Porcine Brain Microvascular Endothelial Cells. Appl. Environ. Microbiol. 73: 4359-4364 [Abstract] [Full Text]  
  • Velez, M. P., Verhoeven, T. L. A., Draing, C., Von Aulock, S., Pfitzenmaier, M., Geyer, A., Lambrichts, I., Grangette, C., Pot, B., Vanderleyden, J., De Keersmaecker, S. C. J. (2007). Functional Analysis of D-Alanylation of Lipoteichoic Acid in the Probiotic Strain Lactobacillus rhamnosus GG. Appl. Environ. Microbiol. 73: 3595-3604 [Abstract] [Full Text]  
  • Li, M., Lai, Y., Villaruz, A. E., Cha, D. J., Sturdevant, D. E., Otto, M. (2007). Gram-positive three-component antimicrobial peptide-sensing system. Proc. Natl. Acad. Sci. USA 104: 9469-9474 [Abstract] [Full Text]  


Copyright © 2009 by the American Society for Microbiology.   For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»