Transient Membrane-Linked FtsZ Assemblies Precede Z-Ring Formation in Escherichia coli

Walker, Bryant E.; Männik, Jaana

doi:10.1016/j.cub.2019.12.023

Cited by 35 publications

(37 citation statements)

References 50 publications

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“…During the nascent Z-ring stage, low density FtsZ filaments transiently assemble at mid-cell over a wide 92 region, consistent with previous reports 4, [13][14][15] . FtsZ filaments then rapidly condense into a thin mature Z-ring structure, which remains unconstricted but increases in intensity for some time.…”

supporting

confidence: 91%

FtsZ treadmilling is essential for Z-ring condensation and septal constriction initiation inBacillus subtiliscell division

Whitley

Jukes

Tregidgo

et al. 2020

Preprint

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ABSTRACTDespite the central role of division in bacterial physiology, how division proteins work together as a nanoscale machine to divide the cell remains poorly understood. Cell division by cell wall synthesis proteins is guided by the cytoskeleton protein FtsZ, which assembles at mid-cell as a dense Z-ring formed of motile treadmilling filaments1,2. However, although FtsZ treadmilling is essential for cell division, the function of FtsZ treadmilling motility remains unclear2–5. Here, we systematically resolve the function of FtsZ treadmilling across each stage of division in the Gram-positive model organism Bacillus subtilis using a novel combination of nanofabrication, advanced microscopy, and microfluidics to measure the division-protein dynamics in live cells with ultrahigh sensitivity. We find that FtsZ treadmilling has two essential functions: mediating condensation of diffuse FtsZ filaments into a dense Z-ring, and initiating constriction by guiding septal cell wall synthesis. After constriction initiation, FtsZ treadmilling has a dispensable function in accelerating septal constriction rate. Our results show that FtsZ treadmilling is critical for assembling and initiating the bacterial cell division machine.

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supporting

confidence: 91%

FtsZ treadmilling is essential for Z-ring condensation and septal constriction initiation inBacillus subtiliscell division

Whitley

Jukes

Tregidgo

et al. 2020

Preprint

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“…Our results confirm this for PaFtsZ. Recently, two studies that measured the effect of ZapA on treadmilling of FtsZ, and found that ZapA did not slow the FtsZ treadmilling rate in vitro 49 and in vivo 50 . Overall these results suggest that the bundling of FtsZ pfs by ZapA is loose enough that it does not significantly alter treadmilling.…”

Section: Discussionsupporting

confidence: 90%

“…The structure shows that the GDP is trapped in a pocket with no channel that could permit its escape. Now that treadmilling is established as the mechanism for assembly dynamics [14][15][16]49,50 , we can assume that the rate of GTP hydrolysis at steady state measures the rate at which subunits associate to the bottom and dissociate from the top of pfs.…”

Section: Discussionmentioning

confidence: 99%

Assembly properties of bacterial tubulin homolog FtsZ regulated by the positive regulator protein ZipA and ZapA from Pseudomonas aeruginosa

Rahman

Zhang

et al. 2020

Sci Rep

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Bacterial tubulin homolog FtsZ self-assembles into dynamic protofilaments, which forms the scaffold for the contractile ring (Z-ring) to achieve bacterial cell division. Here, we study the biochemical properties of FtsZ from Pseudomonas aeruginosa (PaFtsZ) and the effects of its two positive regulator proteins, ZipA and ZapA. Similar to Escherichia coli FtsZ, PaFtsZ had a strong GTPase activity, ~ 7.8 GTP min-1 FtsZ-1 at pH 7.5, and assembled into mainly short single filaments in vitro. However, PaFtsZ protofilaments were mixtures of straight and “intermediate-curved” (100–300 nm diameter) in pH 7.5 solution and formed some bundles in pH 6.5 solution. The effects of ZipA on PaFtsZ assembly varied with pH. In pH 6.5 buffer ZipA induced PaFtsZ to form large bundles. In pH 7.5 buffer PaFtsZ-ZipA protofilaments were not bundled, but ZipA enhanced PaFtsZ assembly and promoted more curved filaments. Comparable to ZapA from other bacterial species, ZapA from P. aeruginosa induced PaFtsZ protofilaments to associate into long straight loose bundles and/or sheets at both pH 6.5 and pH 7.5, which had little effect on the GTPase activity of PaFtsZ. These results provide us further information that ZipA functions as an enhancer of FtsZ curved filaments, while ZapA works as a stabilizer of FtsZ straight filaments.

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“…Inhibition of FtsZ polymerization is obviously crucial to counteract FtsZ ring formation prior to the start of cell division, but it is still required at other times to prevent aberrant ring formation by the majority of cellular FtsZ that is present outside the central ring (20). Furthermore, as nonring FtsZ seems to form oligomers transiently attached to the membrane (20,21), inhibition at this location becomes crucial and the cell has developed a robust mechanism based on the action of the Min system. Our results support the idea that SlmA likely acts coordinately with this system at the membrane.…”

Section: Discussionmentioning

confidence: 99%

The Nucleoid Occlusion Protein SlmA Binds to Lipid Membranes

Robles-Ramos

Margolin²,

Sobrinos-Sanguino

et al. 2020

mBio

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Protection of the chromosome from scission by the division machinery during cytokinesis is critical for bacterial survival and fitness. This is achieved by nucleoid occlusion, which, in conjunction with other mechanisms, ensures formation of the division ring at midcell. In Escherichia coli, this mechanism is mediated by SlmA, a specific DNA binding protein that antagonizes assembly of the central division protein FtsZ into a productive ring in the vicinity of the chromosome. Here, we provide evidence supporting direct interaction of SlmA with lipid membranes, tuned by its binding partners FtsZ and SlmA binding sites (SBS) on chromosomal DNA. Reconstructions in minimal membrane systems that mimic cellular environments show that SlmA binds to lipid-coated microbeads or locates at the edge of microfluidic-generated microdroplets, inside which the protein is encapsulated. DNA fragments containing SBS sequences do not seem to be recruited to the membrane by SlmA but instead compete with SlmA’s ability to bind lipids. The interaction of SlmA with FtsZ modulates this behavior, ultimately triggering membrane localization of the SBS sequences alongside the two proteins. The ability of SlmA to bind lipids uncovered in this work extends the interaction network of this multivalent regulator beyond its well-known protein and nucleic acid recognition, which may have implications in the overall spatiotemporal control of division ring assembly. IMPORTANCE Successful bacterial proliferation relies on the spatial and temporal precision of cytokinesis and its regulation by systems that protect the integrity of the nucleoid. In Escherichia coli, one of these protectors is SlmA protein, which binds to specific DNA sites around the nucleoid and helps to shield the nucleoid from inappropriate bisection by the cell division septum. Here, we discovered that SlmA not only interacts with the nucleoid and septum-associated cell division proteins but also binds directly to cytomimetic lipid membranes, adding a novel putative mechanism for regulating the local activity of these cell division proteins. We find that interaction between SlmA and lipid membranes is regulated by SlmA’s DNA binding sites and protein binding partners as well as chemical conditions, suggesting that the SlmA-membrane interactions are important for fine-tuning the regulation of nucleoid integrity during cytokinesis.

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Transient Membrane-Linked FtsZ Assemblies Precede Z-Ring Formation in Escherichia coli

Cited by 35 publications

References 50 publications

FtsZ treadmilling is essential for Z-ring condensation and septal constriction initiation inBacillus subtiliscell division

FtsZ treadmilling is essential for Z-ring condensation and septal constriction initiation inBacillus subtiliscell division

Assembly properties of bacterial tubulin homolog FtsZ regulated by the positive regulator protein ZipA and ZapA from Pseudomonas aeruginosa

The Nucleoid Occlusion Protein SlmA Binds to Lipid Membranes

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