Filament depolymerization can explain chromosome pulling during bacterial mitosis.

Chromosome segregation is fundamental to all cells, but the force-generating mechanisms underlying chromosome translocation in bacteria remain mysterious. Caulobacter crescentus utilizes a depolymerization-driven process in which a ParA protein structure elongates from the new cell pole, binds to a...

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Main Authors: Edward J Banigan, Michael A Gelbart, Zemer Gitai, Ned S Wingreen, Andrea J Liu
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2011-09-01
Series:PLoS Computational Biology
Online Access:http://europepmc.org/articles/PMC3178632?pdf=render
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spelling doaj-221e2cceb71e4506b0d27e02bd8dc2662020-11-25T01:44:39ZengPublic Library of Science (PLoS)PLoS Computational Biology1553-734X1553-73582011-09-0179e100214510.1371/journal.pcbi.1002145Filament depolymerization can explain chromosome pulling during bacterial mitosis.Edward J BaniganMichael A GelbartZemer GitaiNed S WingreenAndrea J LiuChromosome segregation is fundamental to all cells, but the force-generating mechanisms underlying chromosome translocation in bacteria remain mysterious. Caulobacter crescentus utilizes a depolymerization-driven process in which a ParA protein structure elongates from the new cell pole, binds to a ParB-decorated chromosome, and then retracts via disassembly, pulling the chromosome across the cell. This poses the question of how a depolymerizing structure can robustly pull the chromosome that disassembles it. We perform Brownian dynamics simulations with a simple, physically consistent model of the ParABS system. The simulations suggest that the mechanism of translocation is "self-diffusiophoretic": by disassembling ParA, ParB generates a ParA concentration gradient so that the ParA concentration is higher in front of the chromosome than behind it. Since the chromosome is attracted to ParA via ParB, it moves up the ParA gradient and across the cell. We find that translocation is most robust when ParB binds side-on to ParA filaments. In this case, robust translocation occurs over a wide parameter range and is controlled by a single dimensionless quantity: the product of the rate of ParA disassembly and a characteristic relaxation time of the chromosome. This time scale measures the time it takes for the chromosome to recover its average shape after it is has been pulled. Our results suggest explanations for observed phenomena such as segregation failure, filament-length-dependent translocation velocity, and chromosomal compaction.http://europepmc.org/articles/PMC3178632?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Edward J Banigan
Michael A Gelbart
Zemer Gitai
Ned S Wingreen
Andrea J Liu
spellingShingle Edward J Banigan
Michael A Gelbart
Zemer Gitai
Ned S Wingreen
Andrea J Liu
Filament depolymerization can explain chromosome pulling during bacterial mitosis.
PLoS Computational Biology
author_facet Edward J Banigan
Michael A Gelbart
Zemer Gitai
Ned S Wingreen
Andrea J Liu
author_sort Edward J Banigan
title Filament depolymerization can explain chromosome pulling during bacterial mitosis.
title_short Filament depolymerization can explain chromosome pulling during bacterial mitosis.
title_full Filament depolymerization can explain chromosome pulling during bacterial mitosis.
title_fullStr Filament depolymerization can explain chromosome pulling during bacterial mitosis.
title_full_unstemmed Filament depolymerization can explain chromosome pulling during bacterial mitosis.
title_sort filament depolymerization can explain chromosome pulling during bacterial mitosis.
publisher Public Library of Science (PLoS)
series PLoS Computational Biology
issn 1553-734X
1553-7358
publishDate 2011-09-01
description Chromosome segregation is fundamental to all cells, but the force-generating mechanisms underlying chromosome translocation in bacteria remain mysterious. Caulobacter crescentus utilizes a depolymerization-driven process in which a ParA protein structure elongates from the new cell pole, binds to a ParB-decorated chromosome, and then retracts via disassembly, pulling the chromosome across the cell. This poses the question of how a depolymerizing structure can robustly pull the chromosome that disassembles it. We perform Brownian dynamics simulations with a simple, physically consistent model of the ParABS system. The simulations suggest that the mechanism of translocation is "self-diffusiophoretic": by disassembling ParA, ParB generates a ParA concentration gradient so that the ParA concentration is higher in front of the chromosome than behind it. Since the chromosome is attracted to ParA via ParB, it moves up the ParA gradient and across the cell. We find that translocation is most robust when ParB binds side-on to ParA filaments. In this case, robust translocation occurs over a wide parameter range and is controlled by a single dimensionless quantity: the product of the rate of ParA disassembly and a characteristic relaxation time of the chromosome. This time scale measures the time it takes for the chromosome to recover its average shape after it is has been pulled. Our results suggest explanations for observed phenomena such as segregation failure, filament-length-dependent translocation velocity, and chromosomal compaction.
url http://europepmc.org/articles/PMC3178632?pdf=render
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