Polarization of the Escherichia coli chromosome. A view from the terminus

Capiaux, Hervé; Cornet, François; Corre, Jacqueline; Guijo, Maia-Isabel; Pérals, Koryn; Rebollo, José Emilio; Louarn, Jean-Michel

doi:10.1016/s0300-9084(00)01202-5

Cited by 28 publications

(16 citation statements)

References 34 publications

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“…Massey et al (2004) show that the previously proposed RAG polarized motifs (Capiaux et al, 2001;Lobry & Louarn, 2003) are not implicated in the mobilization of DNA by FtsZ. It is yet uncertain if another of these polarized motifs plays a role in chromosome segregation.…”

Section: Note Added In Proofmentioning

confidence: 82%

“…Site-specific recombination for chromosome dimer resolution is coupled to cell division by the presence of the FtsK protein at the dif site (Perals et al, 2001). FtsK forms a ring-like structure at the cell centre, and may be involved in guiding the regions flanking the dif sites in dimeric chromosomes towards the septum, so that synapsis and recombination can occur (Corre & Louarn, 2002;Li et al, 2003).…”

Section: Open Questions For Researchmentioning

confidence: 99%

“…When the septum is closing, the FtsK rings around the DNA threads mobilize them to place the dif site exactly under the septum. The recognition of the direction in which DNA should be pumped by the translocase would be made by the asymmetric distribution of polar motifs in the chromosome (Capiaux et al, 2001). Recent results suggest that such motifs could be widespread in bacterial genomes, thus connecting the opposing composition of leading and lagging strands with signals that are increasingly biased between the strands near the terminus of replication (Lobry & Louarn, 2003).…”

Section: Open Questions For Researchmentioning

confidence: 99%

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The replication-related organization of bacterial genomes

2004

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The replication of the chromosome is among the most essential functions of the bacterial cell and influences many other cellular mechanisms, from gene expression to cell division. Yet the way it impacts on the bacterial chromosome was not fully acknowledged until the availability of complete genomes allowed one to look upon genomes as more than bags of genes. Chromosomal replication includes a set of asymmetric mechanisms, among which are a division in a lagging and a leading strand and a gradient between early and late replicating regions. These differences are the causes of many of the organizational features observed in bacterial genomes, in terms of both gene distribution and sequence composition along the chromosome. When asymmetries or gradients increase in some genomes, e.g. due to a different composition of the DNA polymerase or to a higher growth rate, so do the corresponding biases. As some of the features of the chromosome structure seem to be under strong selection, understanding such biases is important for the understanding of chromosome organization and adaptation. Inversely, understanding chromosome organization may shed further light on questions relating to replication and cell division. Ultimately, the understanding of the interplay between these different elements will allow a better understanding of bacterial genetics and evolution.

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Section: Note Added In Proofmentioning

confidence: 82%

Section: Open Questions For Researchmentioning

confidence: 99%

Section: Open Questions For Researchmentioning

confidence: 99%

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The replication-related organization of bacterial genomes

2004

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“…These rearrangements can alter gene order and change replichore length. Replichores are defined as the halves of the chromosome between the origin of replication and the terminus region in the vicinity of the dif site (4,6,10,15). In most bacteria, both replichores are approximately the same length, with each comprising 180°around the circular chromosome.…”

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confidence: 99%

Fitness Effects of Replichore Imbalance in Salmonella enterica

Matthews

Maloy

2010

J Bacteriol

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A fitness cost due to imbalanced replichores has been proposed to provoke chromosome rearrangements in Salmonella enterica serovars. To determine the impact of replichore imbalance on fitness, the relative fitness of isogenic Salmonella strains containing transposon-held duplications of various sizes and at various chromosomal locations was determined. Although duplication of certain genes influenced fitness, a replichore imbalance of up to 16°did not affect fitness.The bacterial chromosome is a dynamic molecule that can undergo various types of rearrangements, including inversions, translocations, and duplications. These rearrangements can alter gene order and change replichore length. Replichores are defined as the halves of the chromosome between the origin of replication and the terminus region in the vicinity of the dif site (4, 6, 10, 15). In most bacteria, both replichores are approximately the same length, with each comprising 180°around the circular chromosome. In this state, the replichores and DNA replication are balanced. Imbalance is introduced when one replichore becomes longer than the other. For example, if the replichores comprise 200°and 160°around the circular chromosome, the replichores are 20°imbalanced. Various studies over the years have investigated the effect of imbalanced DNA replication on fitness in Escherichia coli (8,9,16,17). In a recent analysis, E. coli strains that contained asymmetrical interreplichore inversions were found to have growth defects when the imbalance was at least 50°(8). While these studies have demonstrated that imbalanced replichores can affect fitness, the approaches used to introduce the imbalance either do not occur or are extremely rare in nature.Duplications play important evolutionary roles because the increase in gene copy number can facilitate adaptation to certain growth conditions (20), as well as being a source for the evolution of new genes (3). Typically duplications occur at frequencies between 10 Ϫ3 and 10 Ϫ5 in unselected cultures (2) but are lost at rates of up to 1,000-fold more often if they do not provide a selective advantage (19). Duplications also result in replichore imbalance. However, the effect of duplications on fitness in relation to replichore balance has not been investigated.A major hurdle in studying the effects of duplications on fitness is that if the duplication is detrimental, haploid revertants will outgrow the parental strain containing the duplication. To circumvent this problem, we used a set of 11 isogenic Salmonella enterica strains with transposon-held duplications (5) ( Fig. 1 and Table 1). Culturing these strains in the presence of chloramphenicol selects for the duplication because if the duplication collapses, the transposon is lost and the cells become chloramphenicol sensitive. As the size of the duplications in these strains varies, so does the amount of introduced replichore imbalance, ranging from 5°to 23°. In addition, fitness effects due to the location of the duplication versus the size of the duplication ...

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“…Second, the presence near dif of the prophage in a certain orientation (which inverts on either sides of the site) inhibits the resolution process (12). The dif site maps in the region where the polarity of replichores generated by certain skewed oligonucleotides changes sign (8,12). The skew of RGNAGGGS (or Rag) motifs is especially spectacular: these motifs are skewed everywhere on the chromosome (Table 1), but their skew is accentuated near dif since, along 360 kb to the left and 280 kb to the right of the site, 97% of these sequences are located on strands running 5Ј to 3Ј from oriC to dif (Table 1 and Fig.…”

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confidence: 99%

Evidence from Terminal Recombination Gradients that FtsK Uses Replichore Polarity To Control Chromosome Terminus Positioning at Division inEscherichia coli

Corre

Louarn

2002

J Bacteriol

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Chromosome dimers in Escherichia coli are resolved at the dif locus by two recombinases, XerC and XerD, and the septum-anchored FtsK protein. Chromosome dimer resolution (CDR) is subject to strong spatiotemporal control: it takes place at the time of cell division, and it requires the dif resolution site to be located at the junction between the two polarized chromosome arms or replichores. Failure of CDR results in trapping of DNA by the septum and RecABCD recombination (terminal recombination). We had proposed that dif sites of a dimer are first moved to the septum by mechanisms based on local polarity and that normally CDR then occurs as the septum closes. To determine whether FtsK plays a role in the mobilization process, as well as in the recombination reaction, we characterized terminal recombination in an ftsK mutant. The frequency of recombination at various points in the terminus region of the chromosome was measured and compared with the recombination frequency on a xerC mutant chromosome with respect to intensity, the region affected, and response to polarity distortion. The use of a prophage excision assay, which allows variation of the site of recombination and interference with local polarity, allowed us to find that cooperating FtsK-dependent and -independent processes localize dif at the septum and that DNA mobilization by FtsK is oriented by the polarity probably due to skewed sequence motifs of the mobilized material.Though the architecture of the bacterial chromosome remains mysterious, the early proposal that it is established symmetrically on each replichore (31) has been supported recently by studies on the repair of the most frequent accident to befall circular chromosomes: the formation of a chromosome dimer by an odd number of recombinational exchanges between nascent chromosomes. Chromosome dimer resolution (CDR) takes place through the action of three proteins, the recombinases XerC and XerD and the septum-associated protein FtsK, on the resolution site dif (28 bp), located in the chromosome terminus (5,6,21,35). Resolution takes place at the time of division and requires septum formation (34). It also requires that dif be located within a small zone of the terminus region, the DAZ (for dif activity zone [10,22]).Failure of CDR gives rise to several phenotypes, including an increase of 50-to 100-fold in recombination in the terminus region (11,12,25,26). This terminal recombination reflects the extreme fragility of the dif region after inhibition of CDR, presumably a result of engulfment of the localized dif region by the closing septum. The recombination-stimulating events are, or culminate in, double-strand breaks, since terminal recombination is largely RecBCD dependent. Consistent with this scenario, trapping by septum of DNA joining sister nucleoids and DNA degradation near dif have been detected in CDR Ϫ mutants (18,24,30).Genetic studies of the DAZ have revealed the role played by the polarity of the regions that flank dif in generating this domain. First, the "natural" orientat...

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Polarization of the Escherichia coli chromosome. A view from the terminus

Cited by 28 publications

References 34 publications

The replication-related organization of bacterial genomes

The replication-related organization of bacterial genomes

Fitness Effects of Replichore Imbalance in Salmonella enterica

Evidence from Terminal Recombination Gradients that FtsK Uses Replichore Polarity To Control Chromosome Terminus Positioning at Division inEscherichia coli

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