Competence-Programmed Predation of Noncompetent Cells in the Human Pathogen Streptococcus pneumoniae: Genetic Requirements

Natural competence for genetic transformation is the best-characterized feature of the major human pathogen Streptococcus pneumoniae. Recent studies have shown the virulence of competence-deficient mutants to be attenuated, but the nature of the connection between competence and virulence remained u...

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Published inProceedings of the National Academy of Sciences - PNAS Vol. 102; no. 24; pp. 8710 - 8715
Main Authors Guiral, Sébastien, Mitchell, Tim J., Martin, Bernard, Claverys, Jean-Pierre, Losick, Richard M.
Format Journal Article
LanguageEnglish
Published United States National Academy of Sciences 14.06.2005
National Acad Sciences
SeriesFrom the Cover
Subjects
Amidohydrolases - genetics
Amidohydrolases - metabolism
Autolysis
Bacteria
Bacterial Proteins - genetics
Bacterial Proteins - metabolism
Bacteriocins
Bacteriocins - metabolism
Bacteriolysis - genetics
Biological Sciences
Blood cells
Cell culture techniques
Cellular immunity
Delta cells
DNA
DNA Primers
Genetics
Immunity
Life Sciences
Microbiology
Microbiology and Parasitology
Models, Biological
Mutagenesis
N-Acetylmuramoyl-L-alanine Amidase - metabolism
Peptides
Plasmids - genetics
Pneumonia
Streptococcus pneumoniae - genetics
Streptococcus pneumoniae - pathogenicity
Streptolysins - metabolism
Transformation, Bacterial - genetics
Virulence
Virulence factors
Virulence Factors - genetics
Virulence Factors - metabolism
competence
predation
lysis
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Summary:Natural competence for genetic transformation is the best-characterized feature of the major human pathogen Streptococcus pneumoniae. Recent studies have shown the virulence of competence-deficient mutants to be attenuated, but the nature of the connection between competence and virulence remained unknown. Here we document the release, triggered by competent cells, of virulence factors (e.g., the cytolytic toxin pneumolysin) from noncompetent cells. This phenomenon, which we name allolysis, involves a previously undescribed bacteriocin system consisting of a two-peptide bacteriocin, CibAB, and its immunity factor, CibC; the major autolysin, LytA, and lysozyme, LytC; and a proposed new amidase, CbpD. We show that CibAB are absolutely required for allolysis, whereas LytA and LytC can be supplied either by the competent cells or by the targeted cells. We propose that allolysis constitutes a competence-programmed mechanism of predation of noncompetent cells, which benefits to the competent cells and contributes to virulence by coordinating the release of virulence factors.
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content type line 23
See Commentary on page 8401.
Edited by Richard M. Losick, Harvard University, Cambridge, MA, and approved April 23, 2005
Author contributions: B.M. and J.-P.C. designed research; S.G. performed research; T.J.M. contributed new reagents/analytic tools; S.G., B.M., and J.-P.C. analyzed data; and J.-P.C. wrote the paper.
Abbreviations: CSP, competence-stimulating peptide; ABC, ATP-binding cassette; NC, noncompetent; HH, hemolytic halo.
This paper was submitted directly (Track II) to the PNAS office.
ISSN:0027-8424
1091-6490
DOI:10.1073/pnas.0500879102