1887

Abstract

Recently it has been shown that is competent for natural genetic transformation. This property is widespread among streptococci and may include all members of the genus. Upon entering the competent state, streptococci start transcribing a number of competence-specific genes whose products are required for binding, uptake and processing of transforming DNA. In addition to the core competence genes, competent streptococci express a number of accessory genes that are dispensable for transformation in the laboratory, but presumably play an important role under natural conditions. In , one of these accessory genes encodes a competence-specific murein hydrolase termed CbpD. Experimental evidence indicates that pneumococcal CbpD is part of a predatory mechanism that lyses noncompetent sister cells or members of closely related species in order to release homologous DNA that can be taken up by the competent attacker cells. Competent LMG18311 cells produce a CbpD-like protein, Stu0039, which might have the same or a similar function. In the present study we have characterized this protein and shown that it is a murein hydrolase with a novel type of cell surface-binding domain. Furthermore, we show that Stu0039 is rapidly inactivated by HO produced during aerobic growth of We propose that this inactivation mechanism has evolved for self-protection purposes to prevent extensive autolysis in a competent population. Interestingly, in contrast to pneumococcal CbpD, which does not affect the transformation properties of the producer strain, deletion of Stu0039 reduces the transformability of .

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.056150-0
2012-04-01
2019-10-15
Loading full text...

Full text loading...

/deliver/fulltext/micro/158/4/877.html?itemId=/content/journal/micro/10.1099/mic.0.056150-0&mimeType=html&fmt=ahah

References

  1. Bateman A., Rawlings N. D.. ( 2003;). The CHAP domain: a large family of amidases including GSP amidase and peptidoglycan hydrolases. . Trends Biochem Sci 28:, 234–237. [CrossRef][PubMed]
    [Google Scholar]
  2. Berg K. H., Ohnstad H. S., Håvarstein L. S.. ( 2012;). LytF, a novel competence-regulated murein hydrolase in the genus Streptococcus. . J Bacteriol 194:, 627–635. [CrossRef][PubMed]
    [Google Scholar]
  3. Biørnstad T. J., Håvarstein L. S.. ( 2011;). ClpC acts as a negative regulator of competence in Streptococcus thermophilus. . Microbiology 157:, 1676–1684. [CrossRef][PubMed]
    [Google Scholar]
  4. Blomqvist T., Steinmoen H., Håvarstein L. S.. ( 2006;). Natural genetic transformation: a novel tool for efficient genetic engineering of the dairy bacterium Streptococcus thermophilus. . Appl Environ Microbiol 72:, 6751–6756. [CrossRef][PubMed]
    [Google Scholar]
  5. Bolotin A., Quinquis B., Renault P., Sorokin A., Ehrlich S. D., Kulakauskas S., Lapidus A., Goltsman E., Mazur M.. & other authors ( 2004;). Complete sequence and comparative genome analysis of the dairy bacterium Streptococcus thermophilus. . Nat Biotechnol 22:, 1554–1558. [CrossRef][PubMed]
    [Google Scholar]
  6. Claverys J. P., Martin B., Håvarstein L. S.. ( 2007;). Competence-induced fratricide in streptococci. . Mol Microbiol 64:, 1423–1433. [CrossRef][PubMed]
    [Google Scholar]
  7. Dubnau D.. ( 1999;). DNA uptake in bacteria. . Annu Rev Microbiol 53:, 217–244. [CrossRef][PubMed]
    [Google Scholar]
  8. Eaton R. E., Jacques N. A.. ( 2010;). Deletion of competence-induced genes over-expressed in biofilms caused transformation deficiencies in Streptococcus mutans. . Mol Oral Microbiol 25:, 406–417. [CrossRef][PubMed]
    [Google Scholar]
  9. Eldholm V., Johnsborg O., Haugen K., Ohnstad H. S., Håvarstein L. S.. ( 2009;). Fratricide in Streptococcus pneumoniae: contributions and role of the cell wall hydrolases CbpD, LytA and LytC. . Microbiology 155:, 2223–2234. [CrossRef][PubMed]
    [Google Scholar]
  10. Eldholm V., Johnsborg O., Straume D., Ohnstad H. S., Berg K. H., Hermoso J. A., Håvarstein L. S.. ( 2010;). Pneumococcal CbpD is a murein hydrolase that requires a dual cell envelope binding specificity to kill target cells during fratricide. . Mol Microbiol 76:, 905–917. [CrossRef][PubMed]
    [Google Scholar]
  11. Fontaine L., Boutry C., de Frahan M. H., Delplace B., Fremaux C., Horvath P., Boyaval P., Hols P.. ( 2010;). A novel pheromone quorum-sensing system controls the development of natural competence in Streptococcus thermophilus and Streptococcus salivarius. . J Bacteriol 192:, 1444–1454. [CrossRef][PubMed]
    [Google Scholar]
  12. Gardan R., Besset C., Guillot A., Gitton C., Monnet V.. ( 2009;). The oligopeptide transport system is essential for the development of natural competence in Streptococcus thermophilus strain LMD-9. . J Bacteriol 191:, 4647–4655. [CrossRef][PubMed]
    [Google Scholar]
  13. Guiral S., Mitchell T. J., Martin B., Claverys J. P.. ( 2005;). Competence-programmed predation of noncompetent cells in the human pathogen Streptococcus pneumoniae: genetic requirements. . Proc Natl Acad Sci U S A 102:, 8710–8715. [CrossRef][PubMed]
    [Google Scholar]
  14. Hahn J., Maier B., Haijema B. J., Sheetz M., Dubnau D.. ( 2005;). Transformation proteins and DNA uptake localize to the cell poles in Bacillus subtilis. . Cell 122:, 59–71. [CrossRef][PubMed]
    [Google Scholar]
  15. Håvarstein L. S., Martin B., Johnsborg O., Granadel C., Claverys J. P.. ( 2006;). New insights into the pneumococcal fratricide: relationship to clumping and identification of a novel immunity factor. . Mol Microbiol 59:, 1297–1307. [CrossRef][PubMed]
    [Google Scholar]
  16. Hols P., Hancy F., Fontaine L., Grossiord B., Prozzi D., Leblond-Bourget N., Decaris B., Bolotin A., Delorme C.. & other authors ( 2005;). New insights in the molecular biology and physiology of Streptococcus thermophilus revealed by comparative genomics. . FEMS Microbiol Rev 29:, 435–463.[PubMed]
    [Google Scholar]
  17. Johnsborg O., Håvarstein L. S.. ( 2009;). Regulation of natural genetic transformation and acquisition of transforming DNA in Streptococcus pneumoniae. . FEMS Microbiol Rev 33:, 627–642. [CrossRef][PubMed]
    [Google Scholar]
  18. Johnsborg O., Eldholm V., Bjørnstad M. L., Håvarstein L. S.. ( 2008;). A predatory mechanism dramatically increases the efficiency of lateral gene transfer in Streptococcus pneumoniae and related commensal species. . Mol Microbiol 69:, 245–253. [CrossRef][PubMed]
    [Google Scholar]
  19. Kausmally L., Johnsborg O., Lunde M., Knutsen E., Håvarstein L. S.. ( 2005;). Choline-binding protein D (CbpD) in Streptococcus pneumoniae is essential for competence-induced cell lysis. . J Bacteriol 187:, 4338–4345. [CrossRef][PubMed]
    [Google Scholar]
  20. Laemmli U. K.. ( 1970;). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. . Nature 227:, 680–685. [CrossRef][PubMed]
    [Google Scholar]
  21. Layec S., Decaris B., Leblond-Bourget N.. ( 2008;). Diversity of Firmicutes peptidoglycan hydrolases and specificities of those involved in daughter cell separation. . Res Microbiol 159:, 507–515. [CrossRef][PubMed]
    [Google Scholar]
  22. Leclerc D., Asselin A.. ( 1989;). Detection of bacterial cell wall hydrolases after denaturing polyacrylamide gel electrophoresis. . Can J Microbiol 35:, 749–753. [CrossRef][PubMed]
    [Google Scholar]
  23. Miller J. H.. ( 1972;). Experiments in Molecular Genetics. Cold Spring Harbor, NY:: Cold Spring Harbor Laboratory;.
    [Google Scholar]
  24. O’Sullivan D. J., Klaenhammer T. R.. ( 1993;). High- and low-copy-number Lactococcus shuttle cloning vectors with features for clone screening. . Gene 137:, 227–231. [CrossRef][PubMed]
    [Google Scholar]
  25. Peterson S. N., Sung C. K., Cline R., Desai B. V., Snesrud E. C., Luo P., Walling J., Li H., Mintz M.. & other authors ( 2004;). Identification of competence pheromone responsive genes in Streptococcus pneumoniae by use of DNA microarrays. . Mol Microbiol 51:, 1051–1070. [CrossRef][PubMed]
    [Google Scholar]
  26. Podbielski A., Spellerberg B., Woischnik M., Pohl B., Lütticken R.. ( 1996;). Novel series of plasmid vectors for gene inactivation and expression analysis in group A streptococci (GAS). . Gene 177:, 137–147. [CrossRef][PubMed]
    [Google Scholar]
  27. Rigden D. J., Jedrzejas M. J., Galperin M. Y.. ( 2003;). Amidase domains from bacterial and phage autolysins define a family of γ-d,l-glutamate-specific amidohydrolases. . Trends Biochem Sci 28:, 230–234. [CrossRef][PubMed]
    [Google Scholar]
  28. Sambrook J., Fritsch E. F., Maniatis T.. ( 1989;). Molecular Cloning: a Laboratory Manual, , 2nd edn.. Cold Spring Harbor, NY:: Cold Spring Harbor Laboratory;.
    [Google Scholar]
  29. Sánchez-Puelles J. M., Sanz J. M., García J. L., García E.. ( 1990;). Cloning and expression of gene fragments encoding the choline-binding domain of pneumococcal murein hydrolases. . Gene 89:, 69–75. [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.056150-0
Loading
/content/journal/micro/10.1099/mic.0.056150-0
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