Defining a Centromere-like Element in Bacillus subtilis by Identifying the Binding Sites for the Chromosome-Anchoring Protein RacA

Ben-Yehuda, Sigal; Fujita, Masaya; Liu, Xiaole Shirley; Gorbatyuk, Boris; Skoko, Dunja; Yan, Jie; Marko, John F.; Liu, Jun S.; Eichenberger, Patrick; Rudner, David Z.; Losick, Richard

doi:10.1016/j.molcel.2005.02.023

Cited by 96 publications

(92 citation statements)

References 49 publications

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“…During sporulation in Bacillus subtilis, for example, the RacA and DivIVA proteins combine to anchor the chromosomal origin region to the cell pole (41). RacA binds to 25 sites spread over a 612-kb region of originproximal DNA (42), and DivIVA (which does not share sequence similarity with PopZ) is required for RacA-mediated localization of this region to the pole (41). The Escherichia coli chromosome, in turn, does not contain a parABS locus, but it has been shown that the migS cis-acting sequence affects bipolar localization of the origin region in this species (43).…”

Section: Discussionmentioning

confidence: 99%

Caulobacter requires a dedicated mechanism to initiate chromosome segregation

Toro

Hong

McAdams

et al. 2008

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

159

241

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Chromosome segregation in bacteria is rapid and directed, but the mechanisms responsible for this movement are still unclear. We show that Caulobacter crescentus makes use of and requires a dedicated mechanism to initiate chromosome segregation. Caulobacter has a single circular chromosome whose origin of replication is positioned at one cell pole. Upon initiation of replication, an 8-kb region of the chromosome containing both the origin and parS moves rapidly to the opposite pole. This movement requires the highly conserved ParABS locus that is essential in Caulobacter. We use chromosomal inversions and in vivo time-lapse imaging to show that parS is the Caulobacter site of force exertion, independent of its position in the chromosome. When parS is moved farther from the origin, the cell waits for parS to be replicated before segregation can begin. Also, a mutation in the ATPase domain of ParA halts segregation without affecting replication initiation. Chromosome segregation in Caulobacter cannot occur unless a dedicated parS guiding mechanism initiates movement.centromere ͉ parS ͉ ParA

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Section: Discussionmentioning

confidence: 99%

Caulobacter requires a dedicated mechanism to initiate chromosome segregation

Toro

Hong

McAdams

et al. 2008

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

159

241

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“…Alternative mechanisms may involve forespore-specific DNA-protein complexes that could obstruct DNA translocation by the forespore SpoIIIE exporter by creating DNA roadblocks or membrane anchors. These complexes could include the ParB homolog Spo0J, which compacts the originproximal region into filamentous protein-DNA architectures 1,39,40 , and RacA, which tightly tethers the chromosomal origin to the cell pole [40][41][42] . The late appearance of translocation reversal events could be related to the release of oriC tethering later in the process of sporulation.…”

Section: Discussionmentioning

confidence: 99%

Sequence-directed DNA export guides chromosome translocation during sporulation in Bacillus subtilis

Ptacin

Nollmann

Becker

et al. 2008

Nat Struct Mol Biol

165

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In prokaryotes, the transfer of DNA between cellular compartments is essential for the segregation and exchange of genetic material. SpoIIIE and FtsK are AAA+ ATPases responsible for intercompartmental chromosome translocation in bacteria. Despite functional and sequence similarities, these motors were proposed to use drastically different mechanisms: SpoIIIE was suggested to be a unidirectional DNA transporter that exports DNA from the compartment in which it assembles, whereas FtsK was shown to establish translocation directionality by interacting with highly skewed chromosomal sequences. Here we use a combination of single-molecule, bioinformatics and in vivo fluorescence methodologies to study the properties of DNA translocation by SpoIIIE in vitro and in vivo. These data allow us to propose a sequence-directed DNA exporter model that reconciles previously proposed models for SpoIIIE and FtsK, constituting a unified model for directional DNA transport by the SpoIIIE/FtsK family of AAA+ ring ATPases.The segregation and exchange of genetic material are central to the processes of cell division and evolution. Although mechanisms of genetic transfer between cellular compartments are diverse, all require the movement of DNA across cellular membranes. A dramatic example of intercellular transmembrane DNA transport is the segregation of chromosomes during sporulation in Bacillus subtilis. During this process, newly replicated chromosomes are rearranged into an elongated structure, or axial filament, in which the origin of replication of each chromosome is tethered to opposite cell poles 1,2 . Next, the division plane is relocated to one pole, creating two asymmetric cellular compartments (the forespore and the mother cell) and trapping the origin-proximal 30% of one chromosome within the forespore 3,4 . The septally

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“…Other bacteria have more complex segregation scenarios: B. subtilis and Caulobacter crescentus use asymmetric septum formation in differentiation, initiating endospores in the former and in the latter generating swarmer and stalked cells with different developmental prospects. These two bacteria have a centromere-like element represented by sequences extending for several hundred base pairs around oriC, together with proteinsRacA in B. subtilis and MreB in C. crescentusthat bind to it and help anchor chromosome copies to the cell poles (11,12,35).…”

Section: Chromosome Movement During Colony Growth and Developmentmentioning

confidence: 99%

Soil To Genomics: The Streptomyces Chromosome

2006

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The 8-9-Mb Streptomyces chromosome is linear, with a "core" containing essential genes and "arms" carrying conditionally adaptive genes that can sustain large deletions in the laboratory. Bidirectional chromosome replication from a central oriC is completed by "endpatching," primed from terminal proteins covalently bound to the free 5 -ends. Plasmid-mediated conjugation involves movement of double-stranded DNA by proteins resembling other bacterial motor proteins, probably via hyphal tip fusion, mediated by these transfer proteins. Circular plasmids probably transfer chromosomes by transient integration, but linear plasmids may lead the donor chromosome end-first into the recipient by noncovalent association of ends. Transfer of complete chromosomes may be the rule. The recipient mycelium is colonized by intramycelial spreading of plasmid copies, under the control of plasmid-borne "spread" genes. Chromosome partition into prespore compartments of the aerial mycelium is controlled in part by actin-and tubulin-like proteins, resembling MreB and FtsZ of other bacteria.

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Defining a Centromere-like Element in Bacillus subtilis by Identifying the Binding Sites for the Chromosome-Anchoring Protein RacA

Cited by 96 publications

References 49 publications

Caulobacter requires a dedicated mechanism to initiate chromosome segregation

Caulobacter requires a dedicated mechanism to initiate chromosome segregation

Sequence-directed DNA export guides chromosome translocation during sporulation in Bacillus subtilis

Soil To Genomics: The Streptomyces Chromosome

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