The SMC Condensin Complex Is Required for Origin Segregation in Bacillus subtilis

Wang, Xindan; Tang, Olive W.; Riley, Eammon P.; Rudner, David Z.

doi:10.1016/j.cub.2013.11.050

Cited by 117 publications

(138 citation statements)

References 27 publications

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“…In this model, recruitment of SMC complexes to the origin by ParB (28, 38) sets up the left-ori-right pattern. SMC resolves the replicated origins (44,45), and by analogy to the stiffening of eukaryotic centromeres by condensin (46), we hypothesize that SMC rigidifies the origin region constraining the left and right arms on either side of the origin through lengthwise condensation (47). Because SMC complexes are present at the origin throughout the cell cycle, force must be applied to the chromosome to generate the ori-ter pattern.…”

Section: Discussionmentioning

confidence: 94%

Bacillus subtilischromosome organization oscillates between two distinct patterns

Wang

Llopis

Rudner

2014

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

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Bacterial chromosomes have been found to possess one of two distinct patterns of spatial organization. In the first, called "ori-ter" and exemplified by Caulobacter crescentus, the chromosome arms lie side-by-side, with the replication origin and terminus at opposite cell poles. In the second, observed in slow-growing Escherichia coli ("left-ori-right"), the two chromosome arms reside in separate cell halves, on either side of a centrally located origin. These two patterns, rotated 90°relative to each other, appear to result from different segregation mechanisms. Here, we show that the Bacillus subtilis chromosome alternates between them. For most of the cell cycle, newly replicated origins are maintained at opposite poles with chromosome arms adjacent to each other, in an ori-ter configuration. Shortly after replication initiation, the duplicated origins move as a unit to midcell and the two unreplicated arms resolve into opposite cell halves, generating a left-ori-right pattern. The origins are then actively segregated toward opposite poles, resetting the cycle. Our data suggest that the condensin complex and the parABS partitioning system are the principal driving forces underlying this oscillatory cycle. We propose that the distinct organization patterns observed for bacterial chromosomes reflect a common organization-segregation mechanism, and that simple modifications to it underlie the unique patterns observed in different species.DNA replication | ParA | chromosome segregation | SMC condensin C entral to reproduction is the faithful segregation of replicated chromosomes to daughter cells. In eukaryotes, DNA replication, chromosome condensation, and sister chromatid segregation are separated into distinct steps in the cell cycle that are safeguarded by checkpoint pathways. In bacteria, these processes occur concurrently, posing unique challenges to genome integrity and inheritance (1, 2). In the absence of temporal control, bacteria take advantage of spatial organization to promote faithful and efficient chromosome segregation. The organization of the chromosome dictates where the chromosome is replicated, and the factors that organize and compact the newly replicated DNA play a central role in its segregation (1, 2).Studies in different bacteria have revealed strikingly distinct patterns of chromosome organization that appear to arise from different segregation mechanisms. In Caulobacter crescentus and Vibrio cholerae chromosome I, the origin and terminus are located at opposite cell poles, with the two replication arms between them, in a pattern referred to as "ori-ter" (3-5). After replication initiation, one of the sister origins is held in place and the other is actively translocated to the opposite cell pole, regenerating the oriter organization in both daughter cells (5-11). By contrast, in slowgrowing Escherichia coli, the origin is located in the middle of the nucleoid and the two replication arms reside in opposite cell halves, in a "left-ori-right" pattern (12, 13). Replication initiates at mid...

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Section: Discussionmentioning

confidence: 94%

Bacillus subtilischromosome organization oscillates between two distinct patterns

Wang

Llopis

Rudner

2014

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

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119

146

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“…An SMC homodimer and ScpA form a tripartite ring that is similar in size, architecture, and intersubunit contacts to eukaryotic condensins (Hirano et al 2001;Burmann et al 2013;Kamada et al 2013). In bacteria, chromosome segregation occurs concomitant with DNA replication, and B. subtilis condensin plays a central role in the earliest step in this process: the compaction and resolution (or individualization) of newly replicated sister origins Wang et al 2014b). Inactivation of SMC during growth in rich medium leads to the accumulation of unresolved origins and a lethal defect in chromosome segregation.…”

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confidence: 99%

“…Inactivation of SMC during growth in rich medium leads to the accumulation of unresolved origins and a lethal defect in chromosome segregation. In slow growth conditions, cells lacking condensin subunits are viable but inefficiently individualize their origins and produce a high frequency of anucleated cells (Britton et al 1998;Gruber et al 2014;Wang et al 2014b). These defects are significantly enhanced by mutations in the parABS partitioning system that actively segregates replicated origins toward opposite cell poles (Lee and Grossman 2006;Wang et al 2014a,b).…”

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confidence: 99%

“…Despite ParB's role in recruiting condensin to the origin, cells lacking ParB have a modest (fivefold to 80-fold) increase in anucleated cells (Ireton et al 1994; Lee and Grossman 2006), suggesting that the limited number of condensin complexes loaded in the absence of ParB (Wilhelm et al 2015) is sufficient to resolve replicated origins. However, when combined with hypomorphic alleles of SMC, ParB mutants have severe defects in origin resolution and chromosome segregation (Gruber and Errington 2009;Wang et al 2014b). Thus, the current thinking is that ParB loads condensin at parS sites, where it individualizes newly replicated origins (Gruber and Errington 2009;Wang et al 2014b).…”

mentioning

confidence: 99%

“…However, when combined with hypomorphic alleles of SMC, ParB mutants have severe defects in origin resolution and chromosome segregation (Gruber and Errington 2009;Wang et al 2014b). Thus, the current thinking is that ParB loads condensin at parS sites, where it individualizes newly replicated origins (Gruber and Errington 2009;Wang et al 2014b). Once resolved, they are actively segregated by ParA acting on ParB/parS.…”

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confidence: 99%

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Condensin promotes the juxtaposition of DNA flanking its loading site in Bacillus subtilis

et al. 2015

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SMC condensin complexes play a central role in compacting and resolving replicated chromosomes in virtually all organisms, yet how they accomplish this remains elusive. In Bacillus subtilis, condensin is loaded at centromeric parS sites, where it encircles DNA and individualizes newly replicated origins. Using chromosome conformation capture and cytological assays, we show that condensin recruitment to origin-proximal parS sites is required for the juxtaposition of the two chromosome arms. Recruitment to ectopic parS sites promotes alignment of large tracks of DNA flanking these sites. Importantly, insertion of parS sites on opposing arms indicates that these "zip-up" interactions only occur between adjacent DNA segments. Collectively, our data suggest that condensin resolves replicated origins by promoting the juxtaposition of DNA flanking parS sites, drawing sister origins in on themselves and away from each other. These results are consistent with a model in which condensin encircles the DNA flanking its loading site and then slides down, tethering the two arms together. Lengthwise condensation via loop extrusion could provide a generalizable mechanism by which condensin complexes act dynamically to individualize origins in B. subtilis and, when loaded along eukaryotic chromosomes, resolve them during mitosis.

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Lysis‐lysogeny coexistence: prophage integration during lytic development

et al. 2016

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The infection of Escherichia coli cells by bacteriophage lambda results in bifurcated means of propagation, where the phage decides between the lytic and lysogenic pathways. Although traditionally thought to be mutually exclusive, increasing evidence suggests that this lysis‐lysogeny decision is more complex than once believed, but exploring its intricacies requires an improved resolution of study. Here, with a newly developed fluorescent reporter system labeling single phage and E. coli DNAs, these two distinct pathways can be visualized by following the DNA movements in vivo. Surprisingly, we frequently observed an interesting “lyso‐lysis” phenomenon in lytic cells, where phage integrates its DNA into the host, a characteristic event of the lysogenic pathway, followed by cell lysis. Furthermore, the frequency of lyso‐lysis increases with the number of infecting phages, and specifically, with CII activity. Moreover, in lytic cells, the integration site attB on the E. coli genome migrates toward the polar region over time, leading to more spatial overlap with the phage DNA and frequent colocalization/collision of attB and phage DNA, possibly contributing to a higher chance for DNA integration.

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The SMC Condensin Complex Is Required for Origin Segregation in Bacillus subtilis

Cited by 117 publications

References 27 publications

Bacillus subtilischromosome organization oscillates between two distinct patterns

Bacillus subtilischromosome organization oscillates between two distinct patterns

Condensin promotes the juxtaposition of DNA flanking its loading site in Bacillus subtilis

Lysis‐lysogeny coexistence: prophage integration during lytic development

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