Interlinked Sister Chromosomes Arise in the Absence of Condensin during Fast Replication in B. subtilis

Gruber, Stephan; Veening, Jan‐Willem; Bach, Juri Niño; Blettinger, Martin; Bramkamp, Marc; Errington, Jeff

doi:10.1016/j.cub.2013.12.049

Cited by 82 publications

(103 citation statements)

References 34 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: 99%

Bacillus subtilischromosome organization oscillates between two distinct patterns

Wang

Llopis

Rudner

2014

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

118

146

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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: 99%

Bacillus subtilischromosome organization oscillates between two distinct patterns

Wang

Llopis

Rudner

2014

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

118

146

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“…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%

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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“…); the daugther proto-cells deriving from the division of the same coacervate did not share all the components of the mother proto-cell with a precision similar to the one that will appear later in the reproduction of chromosomes. Errington recently observed (2014) and established the morphological comparison of the fusion/fission process of the L-Bacillus subtilis (bacteria devoid of cell wall) with coacervates [4]. Both produce offsprings in the form of "buds", kinds of blebs perfectly observable by electron microscopy.…”

Section: Competition and Community Of Origin Define The Bases Of A Damentioning

confidence: 99%

“…The compounds dissolved in oceans would have constituted the "prebiotic soup" in which organic molecules possibly capable of self-assembly would have appeared. Proto-cells 00014-p. 4 ORIGINS or coacervates would then have concentrated from this primitive "broth" the molecules capable of developing a proto-metabolism, a true bridge between the chemical world and the living world. The construction of the first cells would thus have occurred in parallel with the birth of heterotrophic metabolism.…”

Section: A Brief Historical Backgroundmentioning

confidence: 99%

Fromneontstofiliontsand their progenies...

Maurel

2015

BIO Web of Conferences

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"Should the question of the priority of the egg over the chicken, or of the chicken over the egg disturb you, it is because you assume that animals were originally what they are to-day; what madness!" The dream of d'Alembert, 1760, Denis DiderotAbstract. Since the origins, different modes of life exist. Indeed it is difficult to imagine how things could have been constructed by a single event that would have marked the birth of life. A brief historical background of the subject will be presented here. Then, we shall wander through the history of the discoveries that have led the way of experimental science over the last 150 years and shall dwell on one of the major paradigms, that of the RNA World. This paradigm illustrates the path followed by the living that tries all possible means when expressed at the molecular level as simple free molecule leading to RNA fragments and to modern subviral particles such as viroids then to ramifications and compartments. Between the ancient and the modern RNA world we underline how environment talks to molecules leading to the global living tissus which establish the ground of biodiversity.

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Interlinked Sister Chromosomes Arise in the Absence of Condensin during Fast Replication in B. subtilis

Cited by 82 publications

References 34 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

Fromneontstofiliontsand their progenies...

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