Literature DB >> 31397672

Self-organised segregation of bacterial chromosomal origins.

Andreas Hofmann1, Jarno Mäkelä2, David J Sherratt2, Dieter Heermann1, Seán M Murray3.   

Abstract

The chromosomal replication origin region (ori) of characterised bacteria is dynamically positioned throughout the cell cycle. In slowly growing Escherichia coli, ori is maintained at mid-cell from birth until its replication, after which newly replicated sister oris move to opposite quarter positions. Here, we provide an explanation for ori positioning based on the self-organisation of the Structural Maintenance of Chromosomes complex, MukBEF, which forms dynamically positioned clusters on the chromosome. We propose that a non-trivial feedback between the self-organising gradient of MukBEF complexes and the oris leads to accurate ori positioning. We find excellent agreement with quantitative experimental measurements and confirm key predictions. Specifically, we show that oris exhibit biased motion towards MukBEF clusters, rather than mid-cell. Our findings suggest that MukBEF and oris act together as a self-organising system in chromosome organisation-segregation and introduces protein self-organisation as an important consideration for future studies of chromosome dynamics.
© 2019, Hofmann et al.

Entities:  

Keywords:  E. coli; SMC; Turing patterning; chromosome organisation; computational biology; physics of living systems; self-organisation; systems biology

Mesh:

Substances:

Year:  2019        PMID: 31397672      PMCID: PMC6701925          DOI: 10.7554/eLife.46564

Source DB:  PubMed          Journal:  Elife        ISSN: 2050-084X            Impact factor:   8.140


  62 in total

1.  Progressive segregation of the Escherichia coli chromosome.

Authors:  Henrik J Nielsen; Yongfang Li; Brenda Youngren; Flemming G Hansen; Stuart Austin
Journal:  Mol Microbiol       Date:  2006-06-12       Impact factor: 3.501

2.  The Escherichia coli chromosome is organized with the left and right chromosome arms in separate cell halves.

Authors:  Henrik J Nielsen; Jesper R Ottesen; Brenda Youngren; Stuart J Austin; Flemming G Hansen
Journal:  Mol Microbiol       Date:  2006-10       Impact factor: 3.501

3.  Distribution of centromere-like parS sites in bacteria: insights from comparative genomics.

Authors:  Jonathan Livny; Yoshiharu Yamaichi; Matthew K Waldor
Journal:  J Bacteriol       Date:  2007-09-28       Impact factor: 3.490

4.  Mechanics of DNA bridging by bacterial condensin MukBEF in vitro and in singulo.

Authors:  Zoya M Petrushenko; Yuanbo Cui; Weifeng She; Valentin V Rybenkov
Journal:  EMBO J       Date:  2010-01-14       Impact factor: 11.598

5.  Quantifying absolute protein synthesis rates reveals principles underlying allocation of cellular resources.

Authors:  Gene-Wei Li; David Burkhardt; Carol Gross; Jonathan S Weissman
Journal:  Cell       Date:  2014-04-24       Impact factor: 41.582

6.  Stochastic Turing patterns: analysis of compartment-based approaches.

Authors:  Yang Cao; Radek Erban
Journal:  Bull Math Biol       Date:  2014-11-25       Impact factor: 1.758

7.  DNA-relay mechanism is sufficient to explain ParA-dependent intracellular transport and patterning of single and multiple cargos.

Authors:  Ivan V Surovtsev; Manuel Campos; Christine Jacobs-Wagner
Journal:  Proc Natl Acad Sci U S A       Date:  2016-10-31       Impact factor: 11.205

8.  Perspective: Stochastic algorithms for chemical kinetics.

Authors:  Daniel T Gillespie; Andreas Hellander; Linda R Petzold
Journal:  J Chem Phys       Date:  2013-05-07       Impact factor: 3.488

9.  Topological interactions between ring polymers: Implications for chromatin loops.

Authors:  Manfred Bohn; Dieter W Heermann
Journal:  J Chem Phys       Date:  2010-01-28       Impact factor: 3.488

Review 10.  The bacterial chromosome: architecture and action of bacterial SMC and SMC-like complexes.

Authors:  Sophie Nolivos; David Sherratt
Journal:  FEMS Microbiol Rev       Date:  2013-11-18       Impact factor: 16.408

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  6 in total

1.  Machine learning classification of trajectories from molecular dynamics simulations of chromosome segregation.

Authors:  David Geisel; Peter Lenz
Journal:  PLoS One       Date:  2022-01-21       Impact factor: 3.240

2.  Chromosome Segregation in Bacillus subtilis Follows an Overall Pattern of Linear Movement and Is Highly Robust against Cell Cycle Perturbations.

Authors:  Nina El Najjar; David Geisel; Felix Schmidt; Simon Dersch; Benjamin Mayer; Raimo Hartmann; Bruno Eckhardt; Peter Lenz; Peter L Graumann
Journal:  mSphere       Date:  2020-06-17       Impact factor: 4.389

3.  Alternating Dynamics of oriC, SMC, and MksBEF in Segregation of Pseudomonas aeruginosa Chromosome.

Authors:  Hang Zhao; Bijit K Bhowmik; Zoya M Petrushenko; Valentin V Rybenkov
Journal:  mSphere       Date:  2020-09-09       Impact factor: 4.389

Review 4.  Mechanisms for Chromosome Segregation in Bacteria.

Authors:  Christos Gogou; Aleksandre Japaridze; Cees Dekker
Journal:  Front Microbiol       Date:  2021-06-16       Impact factor: 5.640

5.  Competitive binding of MatP and topoisomerase IV to the MukB hinge domain.

Authors:  Gemma Lm Fisher; Jani R Bolla; Karthik V Rajasekar; Jarno Mäkelä; Rachel Baker; Man Zhou; Josh P Prince; Mathew Stracy; Carol V Robinson; Lidia K Arciszewska; David J Sherratt
Journal:  Elife       Date:  2021-09-29       Impact factor: 8.140

6.  Organization of the Escherichia coli Chromosome by a MukBEF Axial Core.

Authors:  Jarno Mäkelä; David J Sherratt
Journal:  Mol Cell       Date:  2020-02-24       Impact factor: 17.970

  6 in total

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