Movement dynamics of divisome proteins and PBP2x:FtsW in cells of Streptococcus pneumoniae

Proc Natl Acad Sci U S A. 2019 Feb 19;116(8):3211-3220. doi: 10.1073/pnas.1816018116. Epub 2019 Feb 4.

Abstract

Bacterial cell division and peptidoglycan (PG) synthesis are orchestrated by the coordinated dynamic movement of essential protein complexes. Recent studies show that bidirectional treadmilling of FtsZ filaments/bundles is tightly coupled to and limiting for both septal PG synthesis and septum closure in some bacteria, but not in others. Here we report the dynamics of FtsZ movement leading to septal and equatorial ring formation in the ovoid-shaped pathogen, Streptococcus pneumoniae Conventional and single-molecule total internal reflection fluorescence microscopy (TIRFm) showed that nascent rings of FtsZ and its anchoring and stabilizing proteins FtsA and EzrA move out from mature septal rings coincident with MapZ rings early in cell division. This mode of continuous nascent ring movement contrasts with a failsafe streaming mechanism of FtsZ/FtsA/EzrA observed in a ΔmapZ mutant and another Streptococcus species. This analysis also provides several parameters of FtsZ treadmilling in nascent and mature rings, including treadmilling velocity in wild-type cells and ftsZ(GTPase) mutants, lifetimes of FtsZ subunits in filaments and of entire FtsZ filaments/bundles, and the processivity length of treadmilling of FtsZ filament/bundles. In addition, we delineated the motion of the septal PBP2x transpeptidase and its FtsW glycosyl transferase-binding partner relative to FtsZ treadmilling in S. pneumoniae cells. Five lines of evidence support the conclusion that movement of the bPBP2x:FtsW complex in septa depends on PG synthesis and not on FtsZ treadmilling. Together, these results support a model in which FtsZ dynamics and associations organize and distribute septal PG synthesis, but do not control its rate in S. pneumoniae.

Keywords: FtsZ treadmilling; PBP2x:FtsW shared dynamics; TIRF microscopy; microhole vertical imaging; nascent ring formation.

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 / genetics*
  • Cell Division / genetics
  • Cytoskeletal Proteins / genetics
  • Cytoskeletal Proteins / ultrastructure
  • Cytoskeleton / genetics
  • Cytoskeleton / ultrastructure
  • Escherichia coli / genetics
  • GTP Phosphohydrolases / genetics
  • Humans
  • Membrane Proteins / genetics*
  • Microscopy, Fluorescence
  • Penicillin-Binding Proteins / genetics*
  • Peptidoglycan / biosynthesis
  • Peptidoglycan / genetics
  • Pneumococcal Infections / genetics
  • Pneumococcal Infections / microbiology*
  • Streptococcus pneumoniae / genetics*
  • Streptococcus pneumoniae / pathogenicity
  • Streptococcus pneumoniae / ultrastructure

Substances

  • Bacterial Proteins
  • Cytoskeletal Proteins
  • Membrane Proteins
  • Penicillin-Binding Proteins
  • Peptidoglycan
  • FtsW protein, Bacteria
  • PBP 2x protein, Streptococcus
  • GTP Phosphohydrolases