Origin of Contractile Force during Cell Division of Bacteria

Ghosh, Biplab; Sain, Anirban

doi:10.1103/physrevlett.101.178101

Cited by 53 publications

(50 citation statements)

References 23 publications

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“…Third, we found that septum closure is not driven by Z-ring density (FtsZ concentration in the ring) because reduced density in the ΔminC, ΔmatP, and MCI23 strains led to both increases and decreases in septum closure rate, and increased density in the ftsz84 mutant strain did not alter septum closure rate. The Z-ring indeed condenses during the constriction period as previously proposed (35,38,42,43); however, this condensation may be a natural consequence of Z-ring remodeling in response to the gradually reducing septum diameter. Fourth, we found that septum closure cannot be coupled to FtsZ's assembly dynamics during the cell cycle, because three mutations (ftsz84, ΔminC, and ΔmatP) resulted in delayed Z-ring stabilization at midcell but did not lead to systematic changes in the septum closure rate.…”

Section: Discussionsupporting

confidence: 66%

“…Proposed Z-ring force generation models predict that Z-ring structure would be remodeled in different ways as it contracts [i.e., thickening (46), widening (44), condensing (43), or disassembling (38,39,42)]. To determine whether the Z-ring undergoes such structural remodeling in vivo, we examined Z-ring structures using the single-molecule-based superresolution technique, photoactivated localization microscopy (PALM) (47).…”

Section: Resultsmentioning

confidence: 99%

“…The duration of visible cell constriction, τ c , can thus be divided into phase I (from the first visible cell wall indentation to the initiation of Z-ring disassembly) and phase II (Z-ring disassembly). The substantial duration of constriction phase I suggests that, although theoretical models suggest that Z-ring disassembly can drive constriction (38,39,42), constriction can both initiate and proceed without Z-ring disassembly in vivo.…”

Section: Constriction Initiation and Progress Does Not Require Z-ringmentioning

confidence: 99%

“…Having established methods to measure septum closure rates, we next investigated whether the average rate would be altered under perturbed Z-ring properties, which would be expected if Z-ring contraction drives septum closure. We first examined the effects of reduced FtsZ GTPase activity, because GTP hydrolysis-dependent FtsZ protofilament bending and/or disassembly have been prominent hypotheses for force generation by the Z-ring (38,39,42).…”

Section: Constriction Initiation and Progress Does Not Require Z-ringmentioning

confidence: 99%

“…For example, purified, membrane-tethered FtsZ was shown to assemble into ring-like structures that deform and constrict liposome membranes (30)(31)(32)(33)(34)(35). Mechanistically, it has been proposed that a constrictive force could be generated by the bending of FtsZ protofilaments because of their preferred curvature or GTP hydrolysis-induced conformation change (36)(37)(38)(39)(40)(41), immediate reannealing of FtsZ protofilaments upon GTP hydrolysis-induced subunit loss (42), condensation of FtsZ protofilaments caused by their lateral affinity (43), or a combination of these mechanisms (38,42,44,45). However, these proposed mechanisms have been difficult to test in vivo because of the essentiality of FtsZ, the limited ability to spatially resolve the Z-ring structure in small bacterial cells, and the lack of sensitive methods to monitor Z-ring contraction and the rate of septum closure.…”

mentioning

confidence: 99%

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Defining the rate-limiting processes of bacterial cytokinesis

Coltharp

Buss

Plumer

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

161

216

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Bacterial cytokinesis is accomplished by the essential ‘divisome’ machinery. The most widely conserved divisome component, FtsZ, is a tubulin homolog that polymerizes into the ‘FtsZ-ring’ (‘Z-ring’). Previous in vitro studies suggest that Z-ring contraction serves as a major constrictive force generator to limit the progression of cytokinesis. Here, we applied quantitative superresolution imaging to examine whether and how Z-ring contraction limits the rate of septum closure during cytokinesis in Escherichia coli cells. Surprisingly, septum closure rate was robust to substantial changes in all Z-ring properties proposed to be coupled to force generation: FtsZ’s GTPase activity, Z-ring density, and the timing of Z-ring assembly and disassembly. Instead, the rate was limited by the activity of an essential cell wall synthesis enzyme and further modulated by a physical divisome–chromosome coupling. These results challenge a Z-ring–centric view of bacterial cytokinesis and identify cell wall synthesis and chromosome segregation as limiting processes of cytokinesis.

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Section: Discussionsupporting

confidence: 66%

Section: Resultsmentioning

confidence: 99%

Section: Constriction Initiation and Progress Does Not Require Z-ringmentioning

confidence: 99%

Section: Constriction Initiation and Progress Does Not Require Z-ringmentioning

confidence: 99%

mentioning

confidence: 99%

See 3 more Smart Citations

Defining the rate-limiting processes of bacterial cytokinesis

Coltharp

Buss

Plumer

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

161

216

View full text Add to dashboard Cite

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

Coltharp¹,

Xiao²

2016

BioEssays

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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.

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Supramolecular cellular filament systems: How and why do they form?

Popp

Robinson

2012

Cytoskeleton

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All cells, from simple bacteria to complex human tissues, rely on extensive networks of protein fibers to help maintain their proper form and function. These filament systems usually do not operate as single filaments, but form complex suprastructures, which are essential for specific cellular functions. Here, we describe the progress in determining the architectures of molecular filamentous suprastructures, the principles leading to their formation, and the mechanisms by which they may facilitate function. The complex eukaryotic cytoskeleton is tightly regulated by a large number of actin-or microtubule-associated proteins. In contrast, recently discovered bacterial actins and tubulins have few associated regulatory proteins. Hence, the quest to find basic principles that govern the formation of filamentous suprastructures is simplified in bacteria. Three common principles, which have been probed extensively during evolution, can be identified that lead to suprastructures formation: cationic counterion fluctuations; self-association into liquid crystals; and molecular crowding. The underlying physics of these processes will be discussed with respect to physiological circumstance. [Carballido-Lopez and Errington, 2003] and ParM [Bugge-Jensen and Gerdes, 1999], and the MT homolog, FtsZ [L€ owe and Amos, 1998], have also been shown to exist in prokaryotic cells. The functions of actin filaments in both eukaryotic and prokaryotic cells are diverse and range from movement, DNA segregation, and cell division to transport of molecular cargoes [L€ owe and Amos, 2009]. Actin-like and tubulin-like filaments are dynamic, force providing systems that produce movement in cellular objects, such as DNA plasmids or cell membranes. This is often achieved through organizing many filaments to point at the object and selectively elongating those filaments in the direction of the object in order to create pressure on the object.All cellular filament systems share a common feature, in that they frequently adopt supramolecular structures in the form of bundles, sheets, nets, helices, or toroids. Recently, substantial progress has been made in unraveling the molecular details of these suprastructures and in their molecular mechanisms of formation. Suprastructures have been reconstituted in vitro and high resolution electron microscopy images have been obtained that provide insight into their formation and possible cellular functions. This overview will summarize the current knowledge of assembly mechanisms of cytoskeletal filament systems in both eukaryotic and prokaryotic cells. In this respect, bacterial filament systems are of particular interest because of their novelty and their limited numbers of binding partners, making these systems more suitable to define the underlying physical principles leading to complex filament structure formation. In particular, the bacterial cell division protein FtsZ illustrates how suprastructures, and in particular their lateral bonds, can be essential in executing its physiological role of mem...

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Origin of Contractile Force during Cell Division of Bacteria

Cited by 53 publications

References 23 publications

Defining the rate-limiting processes of bacterial cytokinesis

Defining the rate-limiting processes of bacterial cytokinesis

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

Supramolecular cellular filament systems: How and why do they form?

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