Coordination of Cell Division and Chromosome Segregation by a Nucleoid Occlusion Protein in Bacillus subtilis

Sir William Dunn School of Pathology, University of Oxford, Oxford OX1 3RE, United Kingdom.
Cell (Impact Factor: 32.24). 07/2004; 117(7):915-25. DOI: 10.1016/j.cell.2004.06.002
Source: PubMed


A range of genetical and physiological experiments have established that diverse bacterial cells possess a function called nucleoid occlusion, which acts to prevent cell division in the vicinity of the nucleoid. We have identified a specific effector of nucleoid occlusion in Bacillus subtilis, Noc (YyaA), as an inhibitor of division that is also a nonspecific DNA binding protein. Under various conditions in which the cell cycle is perturbed, Noc prevents the division machinery from assembling in the vicinity of the nucleoid. Unexpectedly, cells lacking both Noc and the Min system (which prevents division close to the cell poles) are blocked for division, apparently because they establish multiple nonproductive accumulations of division proteins. The results help to explain how B. subtilis specifies the division site under a range of conditions and how it avoids catastrophic breakage of the chromosome by division through the nucleoid.

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    • "This approach has a number of advantages over immunofluorescence, with the ability to perform live-cell microscopy being one of the main among them. This approach provided a lot of important information about bacterial division mechanisms (Ma et al. 1996; Hale and de Boer 1997; Hu and Lutkenhaus 1999; Wu and Errington 2004; Bernhardt and de Boer 2005; Goehring et al. 2005). Single-molecule localization microscopy (SMLM) of FtsZ-mEos2 yielded Z-ring images with a resolution of about 35 nm (Fu et al. 2010). "
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    ABSTRACT: FtsZ - a prokaryotic tubulin homolog - is one of the central components of bacterial division machinery. At the early stage of cytokinesis FtsZ forms the so-called Z-ring at mid-cell that guides septum formation. Many approaches were used to resolve the structure of the Z-ring, however, researchers are still far from consensus on this question. We utilized single-molecule localization microscopy (SMLM) in combination with immunofluorescence staining to visualize FtsZ in Esherichia coli fixed cells that were grown under slow and fast growth conditions. This approach allowed us to obtain images of FtsZ structures at different stages of cell division and accurately measure Z-ring dimensions. Analysis of these images demonstrated that Z-ring thickness increases during constriction, starting at about 70 nm at the beginning of division and increasing by approximately 25% half-way through constriction.
    Full-text · Article · Feb 2016 · MicrobiologyOpen
    • "Continued study of the Min system and nucleoid occlusion regulatory systems has shown that they cannot be the sole regulators of correct placement of the Z ring at midcell. Under normal growth conditions, when either the Min system or Noc/SlmA in B. subtilis or E. coli are deleted, cells continue to grow and divide without major changes to cell viability [52,53,70]. However, although division is significantly perturbed in B. subtilis and E. coli cells devoid of both the Min system and their respective nucleoid occlusion proteins, Z rings nonetheless preferentially form at midcell in internucleoid positions with high precision [53,71,72]. "
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    ABSTRACT: Proper division site selection is crucial for the survival of all organisms. What still eludes us is how bacteria position their division site with high precision, and in tight coordination with chromosome replication and segregation. Until recently, the general belief, at least in the model organisms Bacillus subtilis and Escherichia coli, was that spatial regulation of division comes about by the combined negative regulatory mechanisms of the Min system and nucleoid occlusion. However, as we review here, these two systems cannot be solely responsible for division site selection and we highlight additional regulatory mechanisms that are at play. In this review, we put forward evidence of how chromosome replication and segregation may have direct links with cell division in these bacteria and the benefit of recent advances in chromosome conformation capture techniques in providing important information about how these three processes mechanistically work together to achieve accurate generation of progenitor cells.
    No preview · Article · Dec 2015 · Seminars in Cell and Developmental Biology
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    • "Though neither gene is normally essential in their respective organisms, both are synthetic lethal with mutations in min. Simultaneous inactivation of both systems leads to chaotic FtsZ assembly such that it cannot reach a sufficiently high concentration for Z-ring assembly at any one point in the cell, rendering cells unable to divide (Wu & Errington, 2004; Bernhardt & de Boer, 2005). Nevertheless, under conditions that perturb DNA replication, the absence of noc (or slmA in E. coli) is itself sufficient to allow division through the nucleoid (Bernhardt & de Boer, 2005; Wu et al, 2009). "
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    ABSTRACT: To proliferate efficiently, cells must co-ordinate division with chromosome segregation. In Bacillus subtilis, the nucleoid occlusion protein Noc binds to specific DNA sequences (NBSs) scattered around the chromosome and helps to protect genomic integrity by coupling the initiation of division to the progression of chromosome replication and segregation. However, how it inhibits division has remained unclear. Here, we demonstrate that Noc associates with the cell membrane via an N-terminal amphipathic helix, which is necessary for function. Importantly, the membrane-binding affinity of this helix is weak and requires the assembly of nucleoprotein complexes, thus establishing a mechanism for DNA-dependent activation of Noc. Furthermore, division inhibition by Noc requires recruitment of NBS DNA to the cell membrane and is dependent on its ability to bind DNA and membrane simultaneously. Indeed, Noc production in a heterologous system is sufficient for recruitment of chromosomal DNA to the membrane. Our results suggest a simple model in which the formation of large membrane-associated nucleoprotein complexes physically occludes assembly of the division machinery.
    Full-text · Article · Jan 2015 · The EMBO Journal
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