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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    • "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.
    The EMBO Journal 01/2015; 34(4). DOI:10.15252/embj.201490177 · 10.43 Impact Factor
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    • "Nucleoid occlusion systems, such as Noc [23] and SlmA [24] are absent in both Mycobacteria [1] and Corynebacteria [25], which are closely related Actinobacteria. However, TEM and DAPI-stained images showed that the positioning of the septum in the asymmetric and symmetric division was found in the space between the already asymmetrically or symmetrically segregated nucleoids, respectively. "
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    ABSTRACT: In this study, we show that about 20% of the septating Mycobacterium smegmatis and Mycobacterium xenopi cells in the exponential phase populationdivideasymmetrically, with an unusually high deviation (17 ± 4%) in the division site from the median, to generate short cells and long cells, thereby generating population heterogeneity. This mode of division is very different from the symmetric division of themajority (about 80%) of the septating cells in the Mycobacterium smegmatis, Mycobacterium marinum, and Mycobacterium bovis BCG exponential phase population, with 5-10% deviation in the division site from the mid-cell site, as reported by recent studies. The short cells and the long cells further grew and divided to generate a population. We speculate that the generation of the short cells and the long cells through the highly deviated asymmetric divisionin the low proportions of mycobacterial population may have a role in stress tolerance.
    The Open Microbiology Journal 05/2014; 8(1):40-50. DOI:10.2174/1874285801408010040
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    • "? b3641 (slmA) BSU40990 (noc) Nucleoid occlusion effector proteins, inhibit Z-ring assembly over the nucleoid Wu and Errington, 2004; Bernhardt and De Boer, 2005 pldP cg1610 rv1708 – – Putative spatial regulator of cell division, member of the ParA/MinD protein family Donovan et al., 2010 mciZ – – – BL02920 § Small peptide, inhibits Z-ring assembly during sporulation in B. subtilis Handler et al., 2008 clpX cg2620 rv2457c b0438 BSU28220 Putative negative regulator of cell division, inhibits Z-ring formation under stress conditions Weart et al., 2005; Camberg et al., 2009; Haeusser et al., 2009; Dziedzic et al., 2010; Sugimoto et al., 2010 divS § § cgR_1759*** (cg2113, C. glutamicum ATCC 13032) rv2719c (chiZ ) b0958 (sulA) BSU17860 (yneA) Induced upon DNA damage, inhibits Z-ring formation, ChiZ is a cell wall hydrolase and interacts with FtsI and FtsQ Huisman et al., 1984; Bi and Lutkenhaus, 1993; Kawai et al., 2003; Chauhan et al., 2006; Ogino et al., 2008 ugtP ? ? "
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    ABSTRACT: Bacterial cells must coordinate a number of events during the cell cycle. Spatio-temporal regulation of bacterial cytokinesis is indispensable for the production of viable, genetically identical offspring. In many rod-shaped bacteria, precise midcell assembly of the division machinery relies on inhibitory systems such as Min and Noc. In rod-shaped Actinobacteria, for example Corynebacterium glutamicum and Mycobacterium tuberculosis, the divisome assembles in the proximity of the midcell region, however more spatial flexibility is observed compared to Escherichia coli and Bacillus subtilis. Actinobacteria represent a group of bacteria that spatially regulate cytokinesis in the absence of recognizable Min and Noc homologs. The key cell division steps in E. coli and B. subtilis have been subject to intensive study and are well-understood. In comparison, only a minimal set of positive and negative regulators of cytokinesis are known in Actinobacteria. Nonetheless, the timing of cytokinesis and the placement of the division septum is coordinated with growth as well as initiation of chromosome replication and segregation. We summarize here the current knowledge on cytokinesis and division site selection in the Actinobacteria suborder Corynebacterineae.
    Frontiers in Microbiology 04/2014; 5:132. DOI:10.3389/fmicb.2014.00132 · 3.99 Impact Factor
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