A dual role for the FtsK protein in <i>Escherichia coli</i> chromosome segregation

Capiaux, Hervé; Lesterlin, Christian; Pérals, Koryn; Louarn, Jean-Michel; Cornet, François

doi:10.1093/embo-reports/kvf116

Cited by 59 publications

(74 citation statements)

References 32 publications

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“…This latter hypothesis is supported by the RecAdependency of recombination between plasmid-borne dif sites (29). A role for FtsK in the segregation of monomers also may contrast with the growth defect of translocation-deficient FtsK mutants, mainly because of their inability to resolve dimers (30). However, these mutations provoke many more cells of abnormal size or shape than seen with Xer inactivation (i.e., see Fig.…”

Section: Discussionmentioning

confidence: 94%

FtsK actively segregates sister chromosomes in Escherichia coli

Stouf

Meile

Cornet

2013

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

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109

131

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Bacteria use the replication origin-to-terminus polarity of their circular chromosomes to control DNA transactions during the cell cycle. Segregation starts by active migration of the region of origin followed by progressive movement of the rest of the chromosomes. The last steps of segregation have been studied extensively in the case of dimeric sister chromosomes and when chromosome organization is impaired by mutations. In these special cases, the divisome-associated DNA translocase FtsK is required. FtsK pumps chromosomes toward the dif chromosome dimer resolution site using polarity of the FtsK-orienting polar sequence (KOPS) DNA motifs. Assays based on monitoring dif recombination have suggested that FtsK acts only in these special cases and does not act on monomeric chromosomes. Using a two-color system to visualize pairs of chromosome loci in living cells, we show that the spatial resolution of sister loci is accurately ordered from the point of origin to the dif site. Furthermore, ordered segregation in a region ∼200 kb long surrounding dif depended on the oriented translocation activity of FtsK but not on the formation of dimers or their resolution. FtsK-mediated segregation required the MatP protein, which delays segregation of the dif-surrounding region until cell division. We conclude that FtsK segregates the terminus region of sister chromosomes whether they are monomeric or dimeric and does so in an accurate and ordered manner. Our data are consistent with a model in which FtsK acts to release the MatP-mediated cohesion and/or interaction with the division apparatus of the terminus region in a KOPS-oriented manner.

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Section: Discussionmentioning

confidence: 94%

FtsK actively segregates sister chromosomes in Escherichia coli

Stouf

Meile

Cornet

2013

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

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109

131

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“…It is not only involved in chromosome decatenation by stimulating the activity of topoisomerase IV [Espeli et al, 2003a,b] but also promotes dimer resolution by catalyzing synopsis of the terminal dif sites [Capiaux et al, 2002] and activating the XerCD recombination system [Aussel et al, 2002;Massey et al, 2004]. This elegant interplay between different systems at the septal region ascertains that DNA partitioning and cell septation occur at the right place and precisely at the right time in the replication process, thereby ensuring unhindered progression of the cell cycle.…”

Section: The Last Stages Of Dna Replicationmentioning

confidence: 99%

The bacterial nucleoid: A highly organized and dynamic structure

Thanbichler

Wang

Shapiro

2005

J of Cellular Biochemistry

122

101

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Recent advances in bacterial cell biology have revealed unanticipated structural and functional complexity, reminiscent of eukaryotic cells. Particular progress has been made in understanding the structure, replication, and segregation of the bacterial chromosome. It emerged that multiple mechanisms cooperate to establish a dynamic assembly of supercoiled domains, which are stacked in consecutive order to adopt a defined higher-level organization. The position of genetic loci on the chromosome is thereby linearly correlated with their position in the cell. SMC complexes and histone-like proteins continuously remodel the nucleoid to reconcile chromatin compaction with DNA replication and gene regulation. Moreover, active transport processes ensure the efficient segregation of sister chromosomes and the faithful restoration of nucleoid organization while DNA replication and condensation are in progress.

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“…FtsK brings the sites of chromosome dimer resolution (dif sites) into close proximity by translocating DNA directionally 13 . SpoIIIE and FtsK are composed of an N-terminal transmembrane domain involved in septal localization [14][15][16] , a putatively unstructured linker and a C-terminal motor domain involved in DNA translocation (Fig.…”

mentioning

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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A dual role for the FtsK protein in Escherichia coli chromosome segregation

Cited by 59 publications

References 32 publications

FtsK actively segregates sister chromosomes in Escherichia coli

FtsK actively segregates sister chromosomes in Escherichia coli

The bacterial nucleoid: A highly organized and dynamic structure

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

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