The extrusion-capture model for chromosome partitioning in bacteria

Lemon, Katherine P.; Grossman, Alan D.

doi:10.1101/gad.913301

Cited by 142 publications

(133 citation statements)

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“…These data, in part, provided support for an "extrusion-capture" model for chromosome segregation in which a DNA replication factory located at a fixed cellular position pulls in the DNA to replicate and then expels the newly replicated sisters outward (34). However, the demonstration that sister replisomes track independently along the DNA in slow-growing E. coli argues against this model (47).…”

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confidence: 93%

Independent Segregation of the Two Arms of theEscherichia coli oriRegion Requires neither RNA Synthesis nor MreB Dynamics

Wang

Sherratt

2010

J Bacteriol

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The mechanism of Escherichia coli chromosome segregation remains elusive. We present results on the simultaneous tracking of segregation of multiple loci in the ori region of the chromosome in cells growing under conditions in which a single round of replication is initiated and completed in the same generation. Loci segregated as expected for progressive replication-segregation from oriC, with markers placed symmetrically on either side of oriC segregating to opposite cell halves at the same time, showing that sister locus cohesion in the origin region is local rather than extensive. We were unable to observe any influence on segregation of the proposed centromeric site, migS, or indeed any other potential cis-acting element on either replication arm (replichore) in the AB1157 genetic background. Site-specific inhibition of replication close to oriC on one replichore did not prevent segregation of loci on the other replichore. Inhibition of RNA synthesis and inhibition of the dynamic polymerization of the actin homolog MreB did not affect ori and bulk chromosome segregation.The chromosome of the extensively studied bacterium Escherichia coli undergoes simultaneous replication and segregation and has no apparent mitotic apparatus for chromosome segregation, a situation very different from that of eukaryotes, where replication and segregation occur in temporally separate periods of the cell cycle. An unsolved mystery of the bacterial cell cycle is how chromosome segregation takes place. Several mechanisms have been proposed to drive the segregation of origin and bulk DNA after replication. In one model, cell elongation is proposed to be a crucial factor, in which the two newly replicated origins are attached to the inner membrane and separated by cell growth between them along the long axis of the cell (25). However, it is now clear that elongation occurs throughout the cell and the movement of the origins is much faster than the rate of cell elongation, indicating that cell elongation alone is not responsible for segregation (55,60).Active partitioning systems were first found in low-copynumber plasmids, where they are required for stable inheritance by distributing the daughter plasmids to both daughter cells (reviewed in reference 14). These systems fall into two families; one uses the ParM actin and its associated protein and binding sites to drive newly replicated sister plasmids apart during cycles of actin polymerization and depolymerization (4, 19). The second parABS family is less well understood mechanistically, although ATP hydrolysis-dependent cycles of ParA movement appear to play a key role in the segregation process (48).Later, it was found that many bacterial chromosomes also utilize parABS systems for their segregation, for example, Bacillus subtilis (23, 37), Caulobacter crescentus (41), and both chromosomes of Vibrio cholerae (22). The typical chromosomal par locus consists of two genes, parA and parB (soj and spo0J in B. subtilis), and a cis-acting parS DNA element. ParB is a DNA-binding prote...

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confidence: 93%

Independent Segregation of the Two Arms of theEscherichia coli oriRegion Requires neither RNA Synthesis nor MreB Dynamics

Wang

Sherratt

2010

J Bacteriol

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“…Inhibiting replication initiation in B. subtilis also inhibits spore formation by a RecA-independent pathway (12)(13)(14). This inhibition of spore formation is mediated by the transcriptional activation of sda, which indirectly reduces the expression of many genes needed for sporulation (12,15).…”

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confidence: 99%

A transcriptional response to replication status mediated by the conserved bacterial replication protein DnaA

Goranov

Katz

Breier

et al. 2005

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

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263

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Organisms respond to perturbations in DNA replication. We characterized the global transcriptional response to inhibition of DNA replication in Bacillus subtilis. We focused on changes that were independent of the known recA-dependent global DNA damage (SOS) response. We found that overlapping sets of genes are affected by perturbations in replication elongation or initiation and that this transcriptional response serves to inhibit cell division and maintain cell viability. Approximately 20 of the operons (>50 genes) affected have potential DnaA-binding sites and are probably regulated directly by DnaA, the highly conserved replication initiation protein and transcription factor. Many of these genes have homologues and recognizable DnaA-binding sites in other bacteria, indicating that a DnaA-mediated response, elicited by changes in DNA replication status, may be conserved.DNA replication ͉ transcription ͉ DNA microarrays ͉ Bacillus subtilis

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“…This model organizes replication to the cell's advantage (8,9). Extruding the two daughter chromosomes in opposite directions should greatly facilitate chromosome partitioning (10)(11)(12). Furthermore, resources such as dNTPs, Ssb protein, and ␤-clamps can be concentrated in one place, improving the speed and efficiency of replication.…”

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Independence of replisomes in Escherichia coli chromosomal replication

Breier

Cozzarelli

2005

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

103

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In Escherichia coli DNA replication is carried out by the coordinated action of the proteins within a replisome. After replication initiation, the two bidirectionally oriented replisomes from a single origin are colocalized into higher-order structures termed replication factories. The factory model postulated that the two replisomes are also functionally coupled. We tested this hypothesis by using DNA combing and whole-genome microarrays. Nascent DNA surrounding oriC in single, combed chromosomes showed instead that one replisome, usually the leftward one, was significantly ahead of the other 70% of the time. We next used microarrays to follow replication throughout the genome by measuring DNA copy number. We found in multiple E. coli strains that the replisomes are independent, with the leftward replisome ahead of the rightward one. The size of the bias was strain-specific, varying from 50 to 130 kb in the array results. When we artificially blocked one replisome, the other continued unabated, again demonstrating independence. We suggest an improved version of the factory model that retains the advantages of threading DNA through colocalized replisomes at about equal rates, but allows the cell flexibility to overcome obstacles encountered during elongation.DNA combing ͉ microarrays ͉ initiation ͉ replication origin ͉ factory model C ellular DNA replication is almost always initiated in a bidirectional manner. Therefore, initiation of replication requires the recruitment of four polymerases and assorted auxiliary proteins at a replication origin (1). Before 1983, the dominant model was that the leading and lagging polymerases continually and repeatedly sped past each other (Fig. 1A) because of the antiparallel nature of duplex DNA. It was difficult to see how the polymerases could be coordinated to achieve synthesis of both DNA strands at about the same time. Alberts et al. (2) suggested an elegant solution, the trombone model, in which one strand is looped so that the two polymerases are colocalized and point in the same direction (Fig. 1B), forming a replisome that additionally contains the auxiliary proteins. Subsequent work confirmed that sister polymerases are physically attached to one another (1). This colocalization is accompanied by coordination; blocking leading-strand replication stops the whole replisome (3-5).A colocalization of the replisomes themselves was proposed in the factory model of DNA replication (6) and demonstrated cytologically (7). Instead of the left and right replisomes racing away from each other until they meet at the terminus (Fig. 1C), this model proposed that the replisomes have stationary positions in the center of the cell (7). Much as in the trombone model, colocalization is facilitated through looping of the DNA, which is fed through the factory (Fig. 1D). This model organizes replication to the cell's advantage (8,9). Extruding the two daughter chromosomes in opposite directions should greatly facilitate chromosome partitioning (10-12). Furthermore, resources such as dNT...

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The extrusion-capture model for chromosome partitioning in bacteria

Cited by 142 publications

References 118 publications

Independent Segregation of the Two Arms of theEscherichia coli oriRegion Requires neither RNA Synthesis nor MreB Dynamics

Independent Segregation of the Two Arms of theEscherichia coli oriRegion Requires neither RNA Synthesis nor MreB Dynamics

A transcriptional response to replication status mediated by the conserved bacterial replication protein DnaA

Independence of replisomes in Escherichia coli chromosomal replication

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