Linear ordering and dynamic segregation of the bacterial chromosome

Breier, Adam M.; Cozzarelli, Nicholas R.

doi:10.1073/pnas.0403722101

Cited by 27 publications

(32 citation statements)

References 24 publications

(24 reference statements)

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“…In the ter region at least, any cohesion that there is must be broken in small stretches as segregation proceeds, because the ter2-ter3 markers 150 kb apart segregate independently over time as well as in space. This observation is consistent with the demonstration that pairs of fluorescent E. coli ori markers 233 kb apart position and duplicate independently (Fekete and Chattoraj 2005), while in C. crescentus a series of genome-wide fluorescent markers 125-250 kb apart segregate sequentially and independently after replication (discussed in Breier and Cozzarelli 2004;. Also consistent with our observations is the report that E. coli oriC and ter remain cohesed for 15-20 min after replication, although two other markers, one just to the right of oriC and the other midway between oriC and ter, appear to remain cohesed Figure 3.…”

Section: Independent Positioning and Separation Of Pairs Of Loci In Tsupporting

confidence: 77%

Dancing around the divisome: asymmetric chromosome segregation in Escherichia coli

Wang

Possoz²,

Sherratt³

2005

Genes Dev.

153

193

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By simultaneously tracking pairs of specific genetic regions and divisome proteins in live Escherichia coli, we develop a new scheme for the relationship between DNA replication-segregation, chromosome organization, and cell division. A remarkable asymmetric pattern of segregation of different loci in the replication termination region (ter) suggests that individual replichores segregate to distinct nucleoid positions, consistent with an asymmetric segregation of leading and lagging strand templates after replication. Cells growing with a generation time of 100 min are born with a nonreplicating chromosome and have their origin region close to mid-cell and their ter polar. After replication initiation, the two newly replicated origin regions move away from mid-cell to opposite cell halves. By mid-S phase, FtsZ forms a ring at mid-cell at the time of initiation of nucleoid separation; ter remains polar. In the latter half of S phase, ter moves quickly toward mid-cell. FtsK, which coordinates the late stages of chromosome segregation with cell division, forms a ring coincident with the FtsZ ring as S phase completes, ∼50 min after its initiation. As ter duplicates at mid-cell, sister nucleoid separation appears complete. After initiation of invagination, the FtsZ ring disassembles, leaving FtsK to complete chromosome segregation and cytokinesis. Understanding of how bacterial chromosomes are organized and how this organization relates to replication, recombination, chromosome segregation, and cell division has emerged in recent years (for review, see Harry 2001;Margolin 2001;Draper and Gober 2002;Sherratt 2003;Espeli and Marians 2004;Lesterlin et al. 2004;Bates and Kleckner 2005). Importantly, this understanding has been informed by the exploitation of microscopic imaging of specific genetic regions, and of divisome and cytoskeletal structures using fluorescent fusion proteins, FISH (fluorescent in situ hybridization), and immunocytochemistry. However, the interpretation of many of these studies has been complicated by the fact that fastgrowing cells in which multiple rounds of replication are ongoing at the same time, and which therefore have overlapping S and G2/M phases, have been analysed. Furthermore, in most studies, a single genetic locus or protein was examined at any one time, and integration of data for multiple loci required combining results from different genetic backgrounds, growth conditions, and methodologies. Finally, genetic studies have been hampered because mutants with defects in either chromosome organization or segregation all have pleiotropic phenotypes that influence many aspects of DNA metabolism and growth. A current challenge is to use a combination of reagents and techniques that interfere minimally with cellular processes in order to gain a comprehensive and consistent picture of how chromosome organization relates to replication-recombination, and how these relate to chromosome segregation and cell division.The 4.6-Mbp Escherichia coli circular chromosome is compacted >1000-fold int...

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Section: Independent Positioning and Separation Of Pairs Of Loci In Tsupporting

confidence: 77%

Dancing around the divisome: asymmetric chromosome segregation in Escherichia coli

Wang

Possoz²,

Sherratt³

2005

Genes Dev.

153

193

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“…But there is also evidence for the participation of some kind of mitotic machinery that exerts mechanical force and pulls the nascent chromosomes apart (46); the nature of this machinery is still quite uncertain. In the end, the chromosome comes to be organized into loops perpendicular to the cell axis, with individual genes occupying fixed positions in linear order between origin and terminus (14,156). The compulsive neatness of the arrangements is a far cry from the historical image of DNA tangled up in midcell like spaghetti in a bowl!…”

Section: Escherichia Coli: Bisecting the Cylindermentioning

confidence: 99%

Molecules into Cells: Specifying Spatial Architecture

Harold

2005

Microbiol Mol Biol Rev

148

157

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SUMMARY A living cell is not an aggregate of molecules but an organized pattern, structured in space and in time. This article addresses some conceptual issues in the genesis of spatial architecture, including how molecules find their proper location in cell space, the origins of supramolecular order, the role of the genes, cell morphology, the continuity of cells, and the inheritance of order. The discussion is framed around a hierarchy of physiological processes that bridge the gap between nanometer-sized molecules and cells three to six orders of magnitude larger. Stepping stones include molecular self-organization, directional physiology, spatial markers, gradients, fields, and physical forces. The knowledge at hand leads to an unconventional interpretation of biological order. I have come to think of cells as self-organized systems composed of genetically specified elements plus heritable structures. The smallest self that can be fairly said to organize itself is the whole cell. If structure, form, and function are ever to be computed from data at a lower level, the starting point will be not the genome, but a spatially organized system of molecules. This conclusion invites us to reconsider our understanding of what genes do, what organisms are, and how living systems could have arisen on the early Earth.

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“…3C). Nevertheless, if specific loci along the chromosome, in particular the ori regions, are tethered to the opposite cell poles after release from the replication factory as hypothesized in the ''extrusion-capture'' model (41), such fluctuations could be reduced (42).…”

Section: Principal Linear Ordering Of Circular Chromosomes In Bacteriamentioning

confidence: 99%

Entropy-driven spatial organization of highly confined polymers: Lessons for the bacterial chromosome

Jun

Mulder

2006

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

371

442

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Despite recent progress in visualization experiments, the mechanism underlying chromosome segregation in bacteria still remains elusive. Here we address a basic physical issue associated with bacterial chromosome segregation, namely the spatial organization of highly confined, self-avoiding polymers (of nontrivial topology) in a rod-shaped cell-like geometry. Through computer simulations, we present evidence that, under strong confinement conditions, topologically distinct domains of a polymer complex effectively repel each other to maximize their conformational entropy, suggesting that duplicated circular chromosomes could partition spontaneously. This mechanism not only is able to account for the spatial separation per se but also captures the major features of the spatiotemporal organization of the duplicating chromosomes observed in Escherichia coli and Caulobacter crescentus.bacterial chromosome segregation ͉ Caulobacter crescentus ͉ Escherichia coli ͉ polymer physics B acteria are arguably the simplest living organisms that are able to reproduce independently. The key step in cellular reproduction consists of the duplication of the genetic material and its subsequent distribution over the offspring. Successful as they are from an evolutionary perspective, bacteria are indeed considered to be highly efficient and accurate in these processes.What then is the mechanism underlying bacterial chromosome segregation? Perhaps the most influential model so far was proposed by Jacob et al. in 1963 (1) in their seminal paper on the replicon model of Escherichia coli; if replicating chromosomes are attached to the elongating cell-wall membrane, they can be segregated passively by insertion of membrane material between the attachment points. Although the hypothesis by Jacob et al.(1) is intuitive and elegant, it has been undermined by a series of recent visualization experiments. In Bacillus subtilis (2) and Caulobacter crescentus (3), for example, the measured rate of movement of the replication origin ranges from 0.1 to 0.3 m͞min, almost 10 times larger than the cell elongation rate. In E. coli, on the other hand, the movement rate of DNA segments is still a matter of debate [see, for example, Elmore et al. (4)]. Nevertheless, all three species, including E. coli, show striking dynamics and directed longitudinal movements of chromosome loci during replication; although details vary from organism to organism, typically the duplicated replication origins (ori) move toward opposite poles in the cell, and the terminus (ter) moves toward the cell center (3, 5-7).A number of alternative models have been proposed recently to explain the driving force for DNA segregation in bacteria [for recent reviews, see Woldringh (8), Errington et al. (9), and Gitai et al. (10) and references therein]. A consensus view that seems to emerge from this more recent literature, at least in case of C. crescentus, favors the existence of putative ''eukaryotic-like'' mechanisms (11-13), which would actively push͞pull the duplicating bacterial c...

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Linear ordering and dynamic segregation of the bacterial chromosome

Cited by 27 publications

References 24 publications

Dancing around the divisome: asymmetric chromosome segregation in Escherichia coli

Dancing around the divisome: asymmetric chromosome segregation in Escherichia coli

Molecules into Cells: Specifying Spatial Architecture

Entropy-driven spatial organization of highly confined polymers: Lessons for the bacterial chromosome

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