Direct interaction of FtsZ and MreB is required for septum synthesis and cell division in Escherichia coli

Fenton, Andrew K.; Gerdes, Kenn

doi:10.1038/emboj.2013.129

Cited by 122 publications

(135 citation statements)

References 67 publications

(123 reference statements)

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“…Additional support for this hypothesis is lent by an ftsZ-mamK fusion gene which was found in a metagenomic clone library from enriched magnetotactic bacteria (48). Direct interactions of bacterial actin and tubulin homologs during cell growth and division are also known from other studies (16,32,49,50).…”

Section: Discussionmentioning

confidence: 75%

The FtsZ-Like Protein FtsZm of Magnetospirillum gryphiswaldense Likely Interacts with Its Generic Homolog and Is Required for Biomineralization under Nitrate Deprivation

et al. 2014

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dMidcell selection, septum formation, and cytokinesis in most bacteria are orchestrated by the eukaryotic tubulin homolog FtsZ. The alphaproteobacterium Magnetospirillum gryphiswaldense (MSR-1) septates asymmetrically, and cytokinesis is linked to splitting and segregation of an intracellular chain of membrane-enveloped magnetite crystals (magnetosomes). In addition to a generic, full-length ftsZ gene, MSR-1 contains a truncated ftsZ homolog (ftsZm) which is located adjacent to genes controlling biomineralization and magnetosome chain formation. We analyzed the role of FtsZm in cell division and biomineralization together with the full-length MSR-1 FtsZ protein. Our results indicate that loss of FtsZm has a strong effect on microoxic magnetite biomineralization which, however, could be rescued by the presence of nitrate in the medium. Fluorescence microscopy revealed that FtsZm-mCherry does not colocalize with the magnetosome-related proteins MamC and MamK but is confined to asymmetric spots at midcell and at the cell pole, coinciding with the FtsZ protein position. In Escherichia coli, both FtsZ homologs form distinct structures but colocalize when coexpressed, suggesting an FtsZdependent recruitment of FtsZm. In vitro analyses indicate that FtsZm is able to interact with the FtsZ protein. Together, our data suggest that FtsZm shares key features with its full-length homolog but is involved in redox control for magnetite crystallization. Magnetotactic bacteria (MTB) produce magnetosomes to navigate along Earth's magnetic field lines toward growth-favoring microoxic environments. Magnetosomes consist of nanometer-sized membrane-enveloped magnetite crystals and have recently emerged as a model system to study formation of prokaryotic organelles (1). In the alphaproteobacterium Magnetospirillum gryphiswaldense MSR-1 (in the following, referred to as MSR-1) and related magnetospirilla, the intracellular organelles are attached to a filamentous cytoskeletal structure formed by the actinlike MamK protein (2, 3, 4) which assembles magnetosomes into a cohesive chain (5). This magnetosome chain generates a magnetic moment which aligns the cell in external magnetic fields. In order to be cleaved evenly during cytokinesis and to be equipartitioned to daughter cells, the magnetosome chain is positioned at midcell. After cytokinesis, daughter chains are translocated to midcell again, suggesting that chain separation and relocalization are coordinated with the cell cycle.A crucial factor for midcell determination and septum formation in most bacteria is the conserved tubulin homolog FtsZ. FtsZ monomers assemble in a GTP-dependent manner to form protofilaments that align into higher-ordered structures by lateral selfinteraction assisted by accessory proteins. The FtsZ polymers are membrane tethered by C-terminal interaction with FtsA and build ring-or arc-like structures at future division sites (6). These FtsZ assemblies recruit further cell division proteins to finally build the divisome complex (7,8). Several factors have ...

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Section: Discussionmentioning

confidence: 75%

The FtsZ-Like Protein FtsZm of Magnetospirillum gryphiswaldense Likely Interacts with Its Generic Homolog and Is Required for Biomineralization under Nitrate Deprivation

et al. 2014

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“…Moreover, FtsA and MreB have been proposed to share an evolutionary origin that subsequently diverged to perform parallel functions within the divisome and the elongasome, respectively (72). It is therefore tempting to speculate that in S. pneumoniae, which compared to bacilli has a different and less sophisticated elongation scheme, a single actin-like protein, FtsA, could perform both roles, taking over the functions of MreB, as seems to occur in preseptal PG synthesis in E. coli (71,(73)(74)(75). Some features of FtsA in S. pneumoniae, such as its higher concentration and FtsA-to-FtsZ ratio (20), are consistent with this replacement role.…”

Section: Discussionmentioning

confidence: 99%

Roles of the Essential Protein FtsA in Cell Growth and Division in Streptococcus pneumoniae

et al. 2017

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Streptococcus pneumoniae is an ovoid-shaped Gram-positive bacterium that grows by carrying out peripheral and septal peptidoglycan (PG) synthesis, analogous to model bacilli, such as Escherichia coli and Bacillus subtilis. In the model bacilli, FtsZ and FtsA proteins assemble into a ring at midcell and are dedicated to septal PG synthesis but not peripheral PG synthesis; hence, inactivation of FtsZ or FtsA results in long filamentous cells unable to divide. Here, we demonstrate that FtsA and FtsZ colocalize at midcell in S. pneumoniae and that partial depletion of FtsA perturbs septum synthesis, resulting in elongated cells with multiple FtsZ rings that fail to complete septation. Unexpectedly, complete depletion of FtsA resulted in the delocalization of FtsZ rings and ultimately cell ballooning and lysis. In contrast, depletion or deletion of gpsB and sepF, which in B. subtilis are synthetically lethal with ftsA, resulted in enlarged and elongated cells with multiple FtsZ rings, with deletion of sepF mimicking partial depletion of FtsA. Notably, cell ballooning was not observed, consistent with later recruitment of these proteins to midcell after Z-ring assembly. The overproduction of FtsA stimulates septation and suppresses the cell division defects caused by the deletion of sepF and gpsB under some conditions, supporting the notion that FtsA shares overlapping functions with GpsB and SepF at later steps in the division process. Our results indicate that, in S. pneumoniae, both GpsB and SepF are involved in septal PG synthesis, whereas FtsA and FtsZ coordinate both peripheral and septal PG synthesis and are codependent for localization at midcell.IMPORTANCE Streptococcus pneumoniae (pneumococcus) is a clinically important human pathogen for which more therapies against unexploited essential targets, like cell growth and division proteins, are needed. Pneumococcus is an ovoid-shaped Gram-positive bacterium with cell growth and division properties that have important distinctions from those of rod-shaped bacteria. Gaining insights into these processes can thus provide valuable information to develop novel antimicrobials. Whereas rods use distinctly localized protein machines at different cellular locations to synthesize peripheral and septal peptidoglycans, we present evidence that S. pneumoniae organizes these two machines at a single location in the middle of dividing cells. Here, we focus on the properties of the actin-like protein FtsA as an essential orchestrator of peripheral and septal growth in this bacterium.KEYWORDS FtsA, Gram-positive cocci, Streptococcus pneumoniae, cell division

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“…Septal cell wall synthesis is directed by the divisome, and lateral cell wall synthesis is directed by the 'elongasome' (91). These two systems may compete with each other, because they share the same precursors (92,93) and/or coordinate with each other during both cell wall elongation and constriction (94)(95)(96)(97)(98).…”

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

confidence: 99%

Defining the rate-limiting processes of bacterial cytokinesis

Coltharp

Buss

Plumer

et al. 2016

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

154

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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Direct interaction of FtsZ and MreB is required for septum synthesis and cell division in Escherichia coli

Cited by 122 publications

References 67 publications

The FtsZ-Like Protein FtsZm of Magnetospirillum gryphiswaldense Likely Interacts with Its Generic Homolog and Is Required for Biomineralization under Nitrate Deprivation

The FtsZ-Like Protein FtsZm of Magnetospirillum gryphiswaldense Likely Interacts with Its Generic Homolog and Is Required for Biomineralization under Nitrate Deprivation

Roles of the Essential Protein FtsA in Cell Growth and Division in Streptococcus pneumoniae

Defining the rate-limiting processes of bacterial cytokinesis

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