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      Spatial coordination between chromosomes and cell division proteins in Escherichia coli

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          Abstract

          To successfully propagate, cells need to coordinate chromosomal replication and segregation with cell division to prevent formation of DNA-less cells and cells with damaged DNA. Here, we review molecular systems in Escherichia coli that are known to be involved in positioning the divisome and chromosome relative to each other. Interestingly, this well-studied micro-organism has several partially redundant mechanisms to achieve this task; none of which are essential. Some of these systems determine the localization of the divisome relative to chromosomes such as SlmA-dependent nucleoid occlusion, some localize the chromosome relative to the divisome such as DNA translocation by FtsK, and some are likely to act on both systems such as the Min system and newly described Ter linkage. Moreover, there is evidence that E. coli harbors other divisome-chromosome coordination systems in addition to those known. The review also discusses the minimal requirements of coordination between chromosomes and cell division proteins needed for cell viability. Arguments are presented that cells can propagate without any dedicated coordination between their chromosomes and cell division machinery at the expense of lowered fitness.

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          Most cited references63

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          Bacterial cell division: assembly, maintenance and disassembly of the Z ring.

          Bacterial cell division is orchestrated by a tubulin homologue, FtsZ, which polymerizes to form a ring-like structure that is both a scaffold for the assembly of the bacterial cytokinetic machinery and, at least in part, a source of the energy for constriction. FtsZ assembly is tightly regulated, and a diverse repertoire of accessory proteins contributes to the formation of a functional division machine that is responsive to cell cycle status and environmental stress. In this Review, we describe the interaction of these proteins with FtsZ and discuss recent advances in our understanding of Z ring assembly.
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            SlmA, a nucleoid-associated, FtsZ binding protein required for blocking septal ring assembly over Chromosomes in E. coli.

            Cell division in Escherichia coli begins with assembly of the tubulin-like FtsZ protein into a ring structure just underneath the cell membrane. Spatial control over Z ring assembly is achieved by two partially redundant negative regulatory systems, the Min system and nucleoid occlusion (NO), which cooperate to position the division site at midcell. In contrast to the well-studied Min system, almost nothing is known about how Z ring assembly is blocked in the vicinity of nucleoids to effect NO. Reasoning that Min function might become essential in cells impaired for NO, we screened for mutations synthetically lethal with a defective Min system (slm mutants). By using this approach, we identified SlmA (Ttk) as the first NO factor in E. coli. Our combined genetic, cytological, and biochemical results suggest that SlmA is a DNA-associated division inhibitor that is directly involved in preventing Z ring assembly on portions of the membrane surrounding the nucleoid.
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              Assembly dynamics of the bacterial MinCDE system and spatial regulation of the Z ring.

              The positioning of a cytoskeletal element that dictates the division plane is a fundamental problem in biology. The assembly and positioning of this cytoskeletal element has to be coordinated with DNA segregation and cell growth to ensure that equal-sized progeny cells are produced, each with a copy of the chromosome. In most prokaryotes, cytokinesis involves positioning a Z ring assembled from FtsZ, the ancestral homologue of tubulin. The position of the Z ring is determined by a gradient of negative regulators of Z-ring assembly. In Escherichia coli, the Min system consists of three proteins that cooperate to position the Z ring through a fascinating oscillation, which inhibits the formation of the Z ring away from midcell. Additional gradients of negative regulators of FtsZ assembly are used by E. coli and other bacteria to achieve spatial control of Z-ring assembly.
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                Author and article information

                Contributors
                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                14 April 2015
                2015
                : 6
                : 306
                Affiliations
                [1] 1Department of Physics and Astronomy, University of Tennessee , Knoxville, TN, USA
                [2] 2Department of Biochemistry and Molecular and Cellular Biology, University of Tennessee , Knoxville, TN, USA
                Author notes

                Edited by: Julie A. Maupin-Furlow, University of Florida, USA

                Reviewed by: Alex Dajkovic, Institut National de la Recherche Agronomique, France; Harold Erickson, Duke University, USA; Piet A. De Boer, Case Western Reserve University, USA

                *Correspondence: Jaan Männik, Department of Physics and Astronomy, University of Tennessee, 401 Nielsen Physics Building, Knoxville, TN 37996, USA jmannik@ 123456utk.edu

                This article was submitted to Microbial Physiology and Metabolism, a section of the journal Frontiers in Microbiology.

                Article
                10.3389/fmicb.2015.00306
                4396457
                25926826
                afcdb958-9588-4785-9aec-16da761e6f37
                Copyright © 2015 Männik and Bailey.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 27 January 2015
                : 27 March 2015
                Page count
                Figures: 3, Tables: 0, Equations: 0, References: 71, Pages: 8, Words: 7126
                Categories
                Microbiology
                Review

                Microbiology & Virology
                nucleoid,divisome,z-ring,cell division,escherichia coli,protocell,nucleoid occlusion

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