Brownian ratchet mechanisms of ParA-mediated partitioning

Hu, Longhua; Vecchiarelli, Anthony G.; Mizuuchi, Kiyoshi; Neuman, Keir C.; Liu, Jian

doi:10.1016/j.plasmid.2017.05.002

Cited by 32 publications

(21 citation statements)

References 25 publications

(77 reference statements)

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“…The first consequence of this assumption is that the self-organised MukBEF gradient can act as a potential energy surface for ori, with the result that ori climb the MukBEF gradient in a directed manner. This is similar to the DNA relay model [34,45] of ParABS-based positioning and to Brownian ratchet models [46,47] in general. However, the situation here is simpler in that the protein gradient is already and spontaneously established and so ori positioning requires no further energy input, similar to the proposed bulk segregation of chromosomes by membrane-based protein gradients [48].…”

Section: Accurate Partitioning During Growthsupporting

confidence: 62%

Self-organised segregation of bacterial chromosomal origins

Murray

Sourjik

2018

Preprint

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In spite of much effort, many aspects of chromosome organisation and segregation in bacteria remain unclear. Even for Escherichia coli, the most widely studied bacterial model organism, we still do not know the underlying mechanisms.Like many other bacteria, the chromosomal origin of replication in E. coli is dynamically positioned throughout the cell cycle. Initially maintained at mid-cell, where replication occurs, origins are subsequently partitioned to opposite quarter positions. The Structural Maintenance of Chromosomes (SMC) complex, MukBEF, which is required for correct chromosome compaction and organisation, has been implicated in this behaviour but the mode of action is unknown.Here, we build on a recent self-organising model for the positioning of E. coli MukBEF, to propose an explanation for the positioning and partitioning of origins. We propose that a specific association of MukBEF with the origin region, results in a non-trivial feedback between the self-organising MukBEF gradient and the origins, leading to accurate positioning and partitioning as an emergent property. We compare the model to quantitative experimental data of origin dynamics and their colocalisation with MukBEF clusters and find excellent agreement. Overall, the model suggests thatMukBEF and origins act together as a self-organising system for chromosome segregation and introduces protein selforganisation as an important consideration for future studies of chromosome dynamics.The faithful and timely segregation of genetic material is essential for all cellular life. In eukaryotes the responsibility for chromosome segregation lies with a well-understood macromolecular machine, the mitotic spindle. In contrast, the mechanisms underlying bacterial chromosome segregation are much less understood but are just as critical for cellular proliferation. Nevertheless, a lot has been learned in recent years (see [1] for a review). In particular, the starting point for (bidirectional) chromosomal replication, the origin, has been found to have a crucial role in chromosome organisation and segregation. Not only is it duplicated and segregated first but its genomic position defines other macrodomains [2] and its spatial position may determine the overall organisation of the chromosome [3].The positions of genomic loci, including the origin, change as replication and segregation progress. Initiated at the chromosomal origin, replication proceeds bi-directionally down each arm of the chromosome. In slowly to moderately growing (1-2 hr generation time) Escherichia coli cells, the home positon of the origin, oriC (henceforth and in the model, ori), in new-born cells is at mid-cell [4][5][6]. After 10-15 min of 'cohesion', in at least part arising from interlinking of the two daughter chromosomes (precatenation) [7][8][9][10][11][12], duplicated origins separate and migrate, initially very rapidly, to opposite quarter positions, which become the new home positions for the remainder of the cell cycle [13,14]. Other genomic loci migrate sequentially to ...

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Section: Accurate Partitioning During Growthsupporting

confidence: 62%

Self-organised segregation of bacterial chromosomal origins

Murray

Sourjik

2018

Preprint

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“…It will be in our future work to interrogate whether and how the Brownian-ratchet mechanism plays out under these different contexts. In a broader scope, given the lack of linear stepper motors in prokaryotic world, Brownian-ratcheting appears to be an ancient mechanism for directed cargo transportation in bacteria – another salient example is ParA-mediated DNA partitioning 39–41 . Interestingly, a similar Brownian-ratchet mechanism also underlies directional movements of mitotic chromosomes by end-tracking spindle microtubule in eukaryotes 42 .…”

Section: Discussionmentioning

confidence: 99%

Treadmilling FtsZ polymers drive the directional movement of sPG-synthesis enzymes via a Brownian ratchet mechanism

McCausland¹,

Yang²,

Lyu³

et al. 2019

Preprint

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15FtsZ, a highly conserved bacterial tubulin GTPase homolog, is a central component of 16 the cell division machinery in nearly all walled bacteria. FtsZ polymerizes at the future 17 division site and recruits > 30 proteins that assemble into a macromolecular complex 18 termed divisome. Many of these divisome proteins are involved in septal cell wall 19 peptidoglycan (sPG) synthesis. Recent studies found that FtsZ polymers undergo GTP 20 hydrolysis-coupled treadmilling dynamics along the septum circumference of dividing 21 cells, which drives processive movements of sPG synthesis enzymes. The mechanism 22

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“…MacCready et al observe that this model fits a Brownian ratchet model (in which random motion can be used to move a cargo in one direction). A similar model has been proposed for the ParA–ParB segregation system that partitions chromosomes and plasmids (Vecchiarelli et al, 2014; Hu et al, 2017). Indeed, McdA is a ParA-like protein.…”

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confidence: 87%