Bacterial Filament Systems: Toward Understanding Their Emergent Behavior and Cellular Functions

Abstract

Bacteria use homologs of eukaryotic cytoskeletal filaments to conduct many different tasks, controlling cell shape, division, and DNA segregation. These filaments, combined with factors that regulate their polymerization, create emergent self-organizing machines. Here, we summarize the current understanding of the assembly of these polymers and their spatial regulation by accessory factors, framing them in the context of being dynamical systems. We highlight how comparing the in vivo dynamics of the filaments with those measured in vitro has provided insight into the regulation, emergent behavior, and cellular functions of these polymeric systems.

Keywords: FtsZ; MreB; actin; bacteria; cell biology; cytoskeleton; tubulin.

FIGURE 1.

Summary of three-component plasmid segregation systems. A common theme among the ParM, AlfA, and TubZ spindles is the spatial regulation of polymer stability. a, the polymers have differing degrees of inherent instability (stable in blue, unstable in red). ParM is dynamically unstable, TubZ treadmills, and AlfA is stable over minutes, although it is destabilized by free AlfB. b, polymers within the spindle are stabilized in two ways: 1) interactions with the DNA-binding protein and plasmid DNA, and 2) lateral interactions with neighboring filaments. c, the native properties of each polymer combined with the regulation conferred by the other factors cause filaments in the spindle to be stable relative to those elsewhere in the cell, which favors filament elongation at kinetochores. The black arrows depict the direction of traveling plasmids.

FIGURE 2.

a, schematic of proteins at the division site. FtsZ polymers are anchored to the membrane through early divisome proteins (e.g. ZipA and FtsA). Other early proteins (e.g. ZapA and FzlA) that stabilize the Z-ring are not shown. Subsequently, late proteins (e.g. FtsKQLNBIW), including cell wall synthesis enzymes, arrive to continue divisome assembly. b, two models of Z-ring structure. The first model (left) suggests that FtsZ filaments form a continuous ring or compressed helix. The second model (right) proposes that the ring is made of short, disorganized polymers with a few lateral contacts. c, spatial regulation of FtsZ polymerization in the cell. Both positive and negative regulators are spatially organized in the cell to focus the Z-ring. The concentrations of regulators along the cell length are plotted, showing that destabilizing factors are located at the poles and over the chromosome, whereas stabilizing factors are at the division plane. This schematic reflects the overall spatial organization in E. coli and C. crescentus.

FIGURE 3.

a, models of MreB polymer organization in vivo. The initial model proposed that MreB polymers make up a cell-spanning helix. The updated model suggests that disconnected polymers move circumferentially around the rod-shaped cell; their motions are otherwise uncoordinated. Moving MreB is shown as arrows. b, schematic of proteins involved in elongation. MreB filaments bind to the membrane and interact with peptidoglycan synthesis enzymes in the periplasm through transmembrane connector proteins. Cell wall synthesis drives MreB motion, indicated by the red arrow.