MinC, MinD, and MinE drive counter-oscillation of early-cell-division proteins prior to Escherichia coli septum formation

mBio. 2013 Dec 10;4(6):e00856-13. doi: 10.1128/mBio.00856-13.

Abstract

Bacterial cell division initiates with the formation of a ring-like structure at the cell center composed of the tubulin homolog FtsZ (the Z-ring), which acts as a scaffold for the assembly of the cell division complex, the divisome. Previous studies have suggested that the divisome is initially composed of FtsZ polymers stabilized by membrane anchors FtsA and ZipA, which then recruit the remaining division proteins. The MinCDE proteins prevent the formation of the Z-ring at poles by oscillating from pole to pole, thereby ensuring that the concentration of the Z-ring inhibitor, MinC, is lowest at the cell center. We show that prior to septum formation, the early-division proteins ZipA, ZapA, and ZapB, along with FtsZ, assemble into complexes that counter-oscillate with respect to MinC, and with the same period. We propose that FtsZ molecules distal from high concentrations of MinC form relatively slowly diffusing filaments that are bound by ZapAB and targeted to the inner membrane by ZipA or FtsA. These complexes may facilitate the early stages of divisome assembly at midcell. As MinC oscillates toward these complexes, FtsZ oligomerization and bundling are inhibited, leading to shorter or monomeric FtsZ complexes, which become less visible by epifluorescence microscopy because of their rapid diffusion. Reconstitution of FtsZ-Min waves on lipid bilayers shows that FtsZ bundles partition away from high concentrations of MinC and that ZapA appears to protect FtsZ from MinC by inhibiting FtsZ turnover.

Importance: A big issue in biology for the past 100 years has been that of how a cell finds its middle. In Escherichia coli, over 20 proteins assemble at the cell center at the time of division. We show that the MinCDE proteins, which prevent the formation of septa at the cell pole by inhibiting FtsZ, drive the counter-oscillation of early-cell-division proteins ZapA, ZapB, and ZipA, along with FtsZ. We propose that FtsZ forms filaments at the pole where the MinC concentration is the lowest and acts as a scaffold for binding of ZapA, ZapB, and ZipA: such complexes are disassembled by MinC and reform within the MinC oscillation period before accumulating at the cell center at the time of division. The ability of FtsZ to be targeted to the cell center in the form of oligomers bound by ZipA and ZapAB may facilitate the early stages of divisome assembly.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine Triphosphatases / metabolism*
  • Bacterial Proteins / metabolism
  • Cell Cycle Proteins / metabolism*
  • Cell Division*
  • Cytoskeletal Proteins / metabolism
  • Escherichia coli / physiology*
  • Escherichia coli Proteins / metabolism*
  • Membrane Proteins / metabolism*

Substances

  • Bacterial Proteins
  • Cell Cycle Proteins
  • Cytoskeletal Proteins
  • Escherichia coli Proteins
  • FtsZ protein, Bacteria
  • Membrane Proteins
  • MinC protein, E coli
  • MinE protein, E coli
  • Adenosine Triphosphatases
  • MinD protein, E coli