Beyond force generation: Why is a dynamic ring of FtsZ polymers essential for bacterial cytokinesis?

Abstract

Summary We propose that the essential function of the most highly-conserved protein in bacterial cytokinesis, FtsZ, is not to generate a mechanical force to drive cell division. Rather, we suggest that FtsZ acts as a signal-processing hub to coordinate cell wall synthesis at the division septum with a diverse array of cellular processes, ensuring that the cell divides smoothly at the correct time and place, and with the correct septum morphology. Here, we explore how the polymerization properties of FtsZ, which have been widely attributed to force generation, can also be advantageous in this signal processing role. We suggest mechanisms by which FtsZ senses and integrates both mechanical and biochemical signals, and conclude by proposing experiments to investigate how FtsZ contributes to the remarkable spatial and temporal precision of bacterial cytokinesis.

Gain‐of‐function variants of FtsA form diverse oligomeric structures on lipids and enhance FtsZ protofilament bundling

“…The FtsZ ring focuses in a narrow band in order to successfully synthesize the division septum (Coltharp and Xiao, ). One focusing mechanism in E. coli likely involves FtsZ filament crosslinking or lateral interactions (Lan et al , ; Dajkovic et al , ; Milam et al , ; Szwedziak et al , ; Haeusser et al , ; Coltharp et al , ), the structures and potential roles of which were recently reviewed (Erickson and Osawa, ; Krupka and Margolin, ).…”

Peptidoglycan synthesis drives an FtsZ-treadmilling-independent step of cytokinesis

“…One would therefore expect that addition of PC190723 would prevent Phase 2 cells, that were halfway through the process of septum synthesis, from completing this process. As this was not the case, we wondered if redirecting PG synthesis to the septum, driven by septal recruitment of MurJ, would provide the constrictive driving force for cytokinesis, as previously suggested for E. coli 23,24 , and result in septum closure independent of FtsZ treadmilling.…”

“…In one model, this force has been proposed to be derived from FtsZ, either from the chemical energy of GTP hydrolysis which could promote bending of the FtsZ polymers or from the affinity of FtsZ filaments to bundle, which could result in condensation of the Z-ring 24,28 . Alternatively, PG synthesis has been suggested to be the force for cytokinesis 23,24 .…”

“…In one model, this force has been proposed to be derived from FtsZ, either from the chemical energy of GTP hydrolysis which could promote bending of the FtsZ polymers or from the affinity of FtsZ filaments to bundle, which could result in condensation of the Z-ring 24,28 . Alternatively, PG synthesis has been suggested to be the force for cytokinesis 23,24 . We propose that cytokinesis occurs in two steps: an initial, slow one, dependent on FtsZ treadmilling, for which FtsZ may be the driving force and that may be responsible for the initial invagination of the cell membrane, followed by a second, faster step, for which PG synthesis provides the driving force.…”

How bacterial cell division might cheat turgor pressure – a unified mechanism of septal division in Gram‐positive and Gram‐negative bacteria

“…Coltharp and Xiao [13, 14] suggested that the force from bending FtsZ protofilaments would be insufficient to constrict the IM against the turgor pressure generated by the high osmolarity of the bacterial cytoplasm. They suggested that the major force for constriction is likely generated by inward growth of the PG wall, pushing the IM from the outside.…”