3D-SIM Super Resolution Microscopy Reveals a Bead-Like Arrangement for FtsZ and the Division Machinery: Implications for Triggering Cytokinesis

Strauss, Michael P.; Liew, Andrew T. F.; Turnbull, Lynne; Whitchurch, Cynthia B.; Monahan, Leigh G.; Harry, Elizabeth J.

doi:10.1371/journal.pbio.1001389

Cited by 196 publications

(209 citation statements)

References 65 publications

(104 reference statements)

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“…The midcell percentage (p mid ) of FtsZ-mEos2 remained constant until the Z-ring diameter reached ∼250 nm (Fig. 3F), consistent with previous studies that monitored early stages of Z-ring closure (diameter, >300 nm) (43,51). However, in cells with smaller diameters (<250 nm), p mid decreased significantly (Fig.…”

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

confidence: 90%

“…We showed that the Z-ring is not a smooth structure but instead comprises clusters of FtsZ protofilaments that loosely associate into a 3D bundle (19,48). This heterogeneous morphology has also been observed with several different fluorescent protein tags (19), in different bacterial species (51)(52)(53)(54), by immuno-superresolution imaging targeting native FtsZ (19,54), by superresolution imaging of FtsZ-binding proteins (19,54), and in an early electron cryotomography (ECT) study (37). Here, we further demonstrate that an FtsZ-GFP fusion colocalizes with native FtsZ in midcell clusters in two-color superresolution imaging using antibodies against native FtsZ and GFP (SI Appendix, Fig.…”

Section: Resultssupporting

confidence: 55%

“…These studies support a smooth, continuous Z-ring organization. However, Z-ring discontinuity has been observed in many bacterial species (19,37,48,(51)(52)(53)(54), and incomplete Z-rings have been shown to lead to cell wall indentation (110), suggesting that ring completion is not required for Z-ring function. We suggest that the continuous and discontinuous organizations reflect different dynamic states of the Z-ring modulated by FtsZ's GTPase activity, which is known to promote the fracture of long FtsZ polymers (111) and to modulate FtsZ turnover dynamics (82).…”

Section: Discussionmentioning

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.

160

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: Constriction Initiation and Progress Does Not Require Z-ringsupporting

confidence: 90%

Section: Resultssupporting

confidence: 55%

Section: Discussionmentioning

confidence: 99%

See 1 more Smart Citation

Defining the rate-limiting processes of bacterial cytokinesis

Coltharp

Buss

Plumer

et al. 2016

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

160

216

View full text Add to dashboard Cite

show abstract

“…Following studies using highresolution fluorescence microscopy techniques revealed that such was the case in many other bacterial species (Strauss et al 2012, Rowlett & Margolin 2014, Jacq et al 2015. It was also hypothesized that GTP-bound FtsZ assemble into straight protofilaments at many nucleation points at the mid-cell and attach themselves to the membrane (Lu et al 2000).…”

Section: :9mentioning

confidence: 98%

Lessons from bacterial homolog of tubulin, FtsZ for microtubule dynamics

Battaje

Panda

2017

Endocrine-Related Cancer

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FtsZ, a homolog of tubulin, is found in almost all bacteria and archaea where it has a primary role in cytokinesis. Evidence for structural homology between FtsZ and tubulin came from their crystal structures and identification of the GTP box. Tubulin and FtsZ constitute a distinct family of GTPases and show striking similarities in many of their polymerization properties. The differences between them, more so, the complexities of microtubule dynamic behavior in comparison to that of FtsZ, indicate that the evolution to tubulin is attributable to the incorporation of the complex functionalities in higher organisms. FtsZ and microtubules function as polymers in cell division but their roles differ in the division process. The structural and partial functional homology has made the study of their dynamic properties more interesting. In this review, we focus on the application of the information derived from studies on FtsZ dynamics to study microtubule dynamics and vice versa. The structural and functional aspects that led to the establishment of the homology between the two proteins are explained to emphasize the network of FtsZ and microtubule studies and how they are connected.

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“…However, this is technically challenging at present, and image acquisition is slow. The first super-resolution images of the bacterial divisome came from IFM of B. subtilis FtsZ (STED), B. subtilis cells producing FtsZ-GFP as the only copy of FtsZ in the cell (3D-SIM), and Staphylococcus aureus cells producing FtsZ-GFP as a label with native FtsZ present (3D-SIM) [66,68,76]. These studies revealed that FtsZ formed a patchy, discontinuousappearing structure, with clear areas of low fluorescence around the ring circumference.…”

Section: Super-resolution Of the Divisome: Is The Z-ring A Patchy Tormentioning

confidence: 99%

The bacterial divisome: ready for its close-up

Rowlett

Margolin²

2015

Phil. Trans. R. Soc. B

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One contribution of 12 to a theme issue 'The bacterial cell envelope'. Bacterial cells divide by targeting a transmembrane protein machine to the division site and regulating its assembly and disassembly so that cytokinesis occurs at the correct time in the cell cycle. The structure and dynamics of this machine (divisome) in bacterial model systems are coming more clearly into focus, thanks to incisive cell biology methods in combination with biochemical and genetic approaches. The main conserved structural element of the machine is the tubulin homologue FtsZ, which assembles into a circumferential ring at the division site that is stabilized and anchored to the inner surface of the cytoplasmic membrane by FtsZ-binding proteins. Once this ring is in place, it recruits a series of transmembrane proteins that ultimately trigger cytokinesis. This review will survey the methods used to characterize the structure of the bacterial divisome, focusing mainly on the Escherichia coli model system, as well as the challenges that remain. These methods include recent super-resolution microscopy, cryo-electron tomography and synthetic reconstitution.

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3D-SIM Super Resolution Microscopy Reveals a Bead-Like Arrangement for FtsZ and the Division Machinery: Implications for Triggering Cytokinesis

Abstract: Super resolution three-dimensional imaging reveals a new picture of how bacterial cell division proteins localize to the division site, including the formation of dynamic bead-like patterns, and explains how the division ring constricts.

Cited by 196 publications

References 65 publications

Defining the rate-limiting processes of bacterial cytokinesis

Defining the rate-limiting processes of bacterial cytokinesis

Lessons from bacterial homolog of tubulin, FtsZ for microtubule dynamics

The bacterial divisome: ready for its close-up

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