The PASTA domain of penicillin-binding protein SpoVD is dispensable for endospore cortex peptidoglycan assembly in Free

Abstract

Peptidoglycan is the major structural component of the bacterial cell wall. enicillin-inding roteins (PBPs), located at the exterior of the cytoplasmic membrane, play a major role in peptidoglycan synthesis and remodelling. A PASTA domain (enicillin-binding protein nd erine/hreonine kinase ssociated domain) of about 65 residues is found at the C-terminal end of some PBPs and eukaryotic-like protein serine/threonine kinases in a variety of bacteria. The function of PASTA domains is not understood, but some of them are thought to bind uncross linked peptidoglycan. has 16 different PBPs, but only 2 of them, Pbp2b and SpoVD, contain a PASTA domain. SpoVD is specific for sporulation and essential for endospore cortex peptidoglycan synthesis. We have studied the role of the PASTA domain in SpoVD by deleting this domain and analysing the effects on endospore formation and subcellular localization of SpoVD. Our results demonstrate that the PASTA domain in SpoVD is not essential for cortex synthesis and not important for targeting SpoVD to the forespore outer membrane during sporulation.

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2015-02-01
2024-03-29
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References

  1. Beilharz K., Nováková L., Fadda D., Branny P., Massidda O., Veening J. W. 2012; Control of cell division in Streptococcus pneumoniae by the conserved Ser/Thr protein kinase StkP. Proc Natl Acad Sci U S A 109:E905–E913 [View Article][PubMed]
    [Google Scholar]
  2. Bugg T. D. H., Braddick D., Dowson C. G., Roper D. I. 2011; Bacterial cell wall assembly: still an attractive antibacterial target. Trends Biotechnol 29:167–173 [View Article][PubMed]
    [Google Scholar]
  3. Bukowska-Faniband E., Hederstedt L. 2013; Cortex synthesis during Bacillus subtilis sporulation depends on the transpeptidase activity of SpoVD. FEMS Microbiol Lett 346:65–72 [View Article][PubMed]
    [Google Scholar]
  4. Calvanese L., Falcigno L., Maglione C., Marasco D., Ruggiero A., Squeglia F., Berisio R., D’Auria G. 2014; Structural and binding properties of the PASTA domain of PonA2, a key penicillin binding protein from Mycobacterium tuberculosis. Biopolymers 101:712–719 [View Article][PubMed]
    [Google Scholar]
  5. Chen J. C., Viollier P. H., Shapiro L. 2005; A membrane metalloprotease participates in the sequential degradation of a Caulobacter polarity determinant. Mol Microbiol 55:1085–1103 [View Article][PubMed]
    [Google Scholar]
  6. Crow A., Lewin A., Hecht O., Carlsson Möller M., Moore G. R., Hederstedt L., Le Brun N. E. 2009; Crystal structure and biophysical properties of Bacillus subtilis BdbD. An oxidizing thiol : disulfide oxidoreductase containing a novel metal site. J Biol Chem 284:23719–23733 [View Article][PubMed]
    [Google Scholar]
  7. Daniel R. A., Drake S., Buchanan C. E., Scholle R., Errington J. 1994; The Bacillus subtilis spoVD gene encodes a mother-cell-specific penicillin-binding protein required for spore morphogenesis. J Mol Biol 235:209–220 [View Article][PubMed]
    [Google Scholar]
  8. Daniel R. A., Harry E. J., Errington J. 2000; Role of penicillin-binding protein PBP 2B in assembly and functioning of the division machinery of Bacillus subtilis. Mol Microbiol 35:299–311 [View Article][PubMed]
    [Google Scholar]
  9. de Jong I. G., Veening J. W., Kuipers O. P. 2010; Heterochronic phosphorelay gene expression as a source of heterogeneity in Bacillus subtilis spore formation. J Bacteriol 192:2053–2067 [View Article][PubMed]
    [Google Scholar]
  10. Doherty G. P., Bailey K., Lewis P. J. 2010; Stage-specific fluorescence intensity of GFP and mCherry during sporulation in Bacillus subtilis. BMC Res Notes 3:303[PubMed]
    [Google Scholar]
  11. Eichenberger P. 2012; Genomics and cellular biology of endospore formation. In Bacillus: Cellular and Molecular Biology pp. 319–350 Edited by Graumann P. Norfolk: Caister Academic Press;
    [Google Scholar]
  12. Fay A., Meyer P., Dworkin J. 2010; Interactions between late-acting proteins required for peptidoglycan synthesis during sporulation. J Mol Biol 399:547–561 [View Article][PubMed]
    [Google Scholar]
  13. Fleurie A., Cluzel C., Guiral S., Freton C., Galisson F., Zanella-Cleon I., Di Guilmi A. M., Grangeasse C. 2012; Mutational dissection of the S/T-kinase StkP reveals crucial roles in cell division of Streptococcus pneumoniae. Mol Microbiol 83:746–758 [View Article][PubMed]
    [Google Scholar]
  14. Fortnagel P., Freese E. 1968; Analysis of sporulation mutants. II. Mutants blocked in the citric acid cycle. J Bacteriol 95:1431–1438[PubMed]
    [Google Scholar]
  15. Fraipont C., Alexeeva S., Wolf B., van der Ploeg R., Schloesser M., den Blaauwen T., Nguyen-Distèche M. 2011; The integral membrane FtsW protein and peptidoglycan synthase PBP3 form a subcomplex in Escherichia coli. Microbiology 157:251–259 [View Article][PubMed]
    [Google Scholar]
  16. Gordon E., Mouz N., Duée E., Dideberg O. 2000; The crystal structure of the penicillin-binding protein 2x from Streptococcus pneumoniae and its acyl-enzyme form: implication in drug resistance. J Mol Biol 299:477–485 [View Article][PubMed]
    [Google Scholar]
  17. Hanahan D., Jessee J., Bloom F. R. 1991; Plasmid transformation of Escherichia coli and other bacteria. Methods Enzymol 204:63–113 [View Article][PubMed]
    [Google Scholar]
  18. Harwood C. R., Archibald A. R. 1990; Growth maintenance and general techniques. In Molecular Biological Methods for Bacillus pp. 1–26 Edited by Harwood C. R., Cutting S. M. Chichester: Wiley;
    [Google Scholar]
  19. Hoch J. A. 1991; Genetic analysis in Bacillus subtilis. Methods Enzymol 204:305–320 [View Article][PubMed]
    [Google Scholar]
  20. Johansson P., Hederstedt L. 1999; Organization of genes for tetrapyrrole biosynthesis in Gram-positive bacteria. Microbiology 145:529–538 [View Article][PubMed]
    [Google Scholar]
  21. Liu Y. M., Carlsson Möller M., Petersen L., Söderberg C. A. G., Hederstedt L. 2010; Penicillin-binding protein SpoVD disulphide is a target for StoA in Bacillus subtilis forespores. Mol Microbiol 75:46–60 [View Article][PubMed]
    [Google Scholar]
  22. Maestro B., Novaková L., Hesek D., Lee M., Leyva E., Mobashery S., Sanz J. M., Branny P. 2011; Recognition of peptidoglycan and β-lactam antibiotics by the extracellular domain of the Ser/Thr protein kinase StkP from Streptococcus pneumoniae. FEBS Lett 585:357–363 [View Article][PubMed]
    [Google Scholar]
  23. Marmur J. 1963; A procedure for the isolation of deoxyribonucleic acid from microorganisms. Methods Enzymol 6:726–738 [View Article]
    [Google Scholar]
  24. Maurer P., Todorova K., Sauerbier J., Hakenbeck R. 2012; Mutations in Streptococcus pneumoniae penicillin-binding protein 2x: importance of the C-terminal penicillin-binding protein and serine/threonine kinase-associated domains for beta-lactam binding. Microb Drug Resist 18:314–321 [View Article][PubMed]
    [Google Scholar]
  25. Mir M., Asong J., Li X. R., Cardot J., Boons G. J., Husson R. N. 2011; The extracytoplasmic domain of the Mycobacterium tuberculosis Ser/Thr kinase PknB binds specific muropeptides and is required for PknB localization. PLoS Pathog 7:e1002182 [View Article][PubMed]
    [Google Scholar]
  26. Morlot C., Bayle L., Jacq M., Fleurie A., Tourcier G., Galisson F., Vernet T., Grangeasse C., Di Guilmi A. M. 2013; Interaction of penicillin-binding protein 2x and Ser/Thr protein kinase StkP, two key players in Streptococcus pneumoniae R6 morphogenesis. Mol Microbiol 90:88–102[PubMed]
    [Google Scholar]
  27. Nicholson W. L., Setlow P. 1990; Sporulation germination and outgrowth. In Molecular Biological Methods for Bacillus pp. 391–450 Edited by Harwood C. R., Cutting S. M. Chichester: Wiley;
    [Google Scholar]
  28. Peters K., Schweizer I., Beilharz K., Stahlmann C., Veening J. W., Hakenbeck R., Denapaite D. 2014; Streptococcus pneumoniae PBP2x mid-cell localization requires the C-terminal PASTA domains and is essential for cell shape maintenance. Mol Microbiol 92:733–755 [View Article][PubMed]
    [Google Scholar]
  29. Piggot P. J., Hilbert D. W. 2004; Sporulation of Bacillus subtilis. Curr Opin Microbiol 7:579–586 [View Article][PubMed]
    [Google Scholar]
  30. Sambrook J., Russell D. W. 2001 Molecular Cloning: a Laboratory Manual Cold Spring Harbor, 3rd edn. NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  31. Schägger H., von Jagow G. 1987; Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal Biochem 166:368–379 [View Article][PubMed]
    [Google Scholar]
  32. Shah I. M., Laaberki M. H., Popham D. L., Dworkin J. 2008; A eukaryotic-like Ser/Thr kinase signals bacteria to exit dormancy in response to peptidoglycan fragments. Cell 135:486–496 [View Article][PubMed]
    [Google Scholar]
  33. Squeglia F., Marchetti R., Ruggiero A., Lanzetta R., Marasco D., Dworkin J., Petoukhov M., Molinaro A., Berisio R., Silipo A. 2011; Chemical basis of peptidoglycan discrimination by PrkC, a key kinase involved in bacterial resuscitation from dormancy. J Am Chem Soc 133:20676–20679 [View Article][PubMed]
    [Google Scholar]
  34. Todd J. A., Roberts A. N., Johnstone K., Piggot P. J., Winter G., Ellar D. J. 1986; Reduced heat resistance of mutant spores after cloning and mutagenesis of the Bacillus subtilis gene encoding penicillin-binding protein 5. J Bacteriol 167:257–264[PubMed]
    [Google Scholar]
  35. Typas A., Banzhaf M., Gross C. A., Vollmer W. 2012; From the regulation of peptidoglycan synthesis to bacterial growth and morphology. Nat Rev Microbiol 10:123–136[PubMed]
    [Google Scholar]
  36. Warth A. D. 1978; Molecular structure of the bacterial spore. Adv Microb Physiol 17:1–45 [View Article][PubMed]
    [Google Scholar]
  37. Warth A. D., Strominger J. L. 1972; Structure of the peptidoglycan from spores of Bacillus subtilis. Biochemistry 11:1389–1396 [View Article][PubMed]
    [Google Scholar]
  38. Yanouri A., Daniel R. A., Errington J., Buchanan C. E. 1993; Cloning and sequencing of the cell division gene pbpB, which encodes penicillin-binding protein 2B in Bacillus subtilis. J Bacteriol 175:7604–7616[PubMed]
    [Google Scholar]
  39. Yeats C., Finn R. D., Bateman A. 2002; The PASTA domain: a beta-lactam-binding domain. Trends Biochem Sci 27:438–440 [View Article][PubMed]
    [Google Scholar]
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