Requirement of essential Pbp2x and GpsB for septal ring closure in Streptococcus pneumoniae D39

Mol Microbiol. 2013 Dec;90(5):939-55. doi: 10.1111/mmi.12408. Epub 2013 Oct 17.

Abstract

Bacterial cell shapes are manifestations of programs carried out by multi-protein machines that synthesize and remodel the resilient peptidoglycan (PG) mesh and other polymers surrounding cells. GpsB protein is conserved in low-GC Gram-positive bacteria and is not essential in rod-shaped Bacillus subtilis, where it plays a role in shuttling penicillin-binding proteins (PBPs) between septal and side-wall sites of PG synthesis. In contrast, we report here that GpsB is essential in ellipsoid-shaped, ovococcal Streptococcus pneumoniae (pneumococcus), and depletion of GpsB leads to formation of elongated, enlarged cells containing unsegregated nucleoids and multiple, unconstricted rings of fluorescent-vancomycin staining, and eventual lysis. These phenotypes are similar to those caused by selective inhibition of Pbp2x by methicillin that prevents septal PG synthesis. Dual-protein 2D and 3D-SIM (structured illumination) immunofluorescence microscopy (IFM) showed that GpsB and FtsZ have overlapping, but not identical, patterns of localization during cell division and that multiple, unconstricted rings of division proteins FtsZ, Pbp2x, Pbp1a and MreC are in elongated cells depleted of GpsB. These patterns suggest that GpsB, like Pbp2x, mediates septal ring closure. This first dual-protein 3D-SIM IFM analysis also revealed separate positioning of Pbp2x and Pbp1a in constricting septa, consistent with two separable PG synthesis machines.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Bacterial Proteins / metabolism
  • Bacterial Proteins / physiology*
  • Cell Division
  • Cytoskeletal Proteins / metabolism
  • Gene Deletion
  • Imaging, Three-Dimensional
  • Methicillin / pharmacology
  • Microscopy, Fluorescence
  • Penicillin-Binding Proteins / physiology
  • Peptidoglycan / metabolism*
  • Peptidyl Transferases / physiology
  • Phenotype
  • Protein Transport
  • Streptococcus pneumoniae / cytology*
  • Streptococcus pneumoniae / genetics
  • Streptococcus pneumoniae / metabolism*
  • Virulence Factors / metabolism
  • Virulence Factors / physiology*

Substances

  • Bacterial Proteins
  • Cytoskeletal Proteins
  • FtsZ protein, Bacteria
  • GpsB protein, Streptococcus pneumoniae
  • Penicillin-Binding Proteins
  • Peptidoglycan
  • Virulence Factors
  • PBP 2x protein, Streptococcus
  • PBP1a protein, Streptococcus pneumoniae
  • Peptidyl Transferases
  • Methicillin