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...
| Main Authors: | , , , , |
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| Format: | Article |
| Language: | English |
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Public Library of Science (PLoS)
2011-09-01
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| Series: | PLoS Computational Biology |
| Online Access: | https://journals.plos.org/ploscompbiol/article/file?id=10.1371/journal.pcbi.1002145&type=printable |
| _version_ | 1826799385126633472 |
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| author | Edward J Banigan Michael A Gelbart Zemer Gitai Ned S Wingreen Andrea J Liu |
| author_facet | Edward J Banigan Michael A Gelbart Zemer Gitai Ned S Wingreen Andrea J Liu |
| author_sort | Edward J Banigan |
| collection | DOAJ |
| 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. |
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| id | doaj.art-221e2cceb71e4506b0d27e02bd8dc266 |
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| issn | 1553-734X 1553-7358 |
| language | English |
| last_indexed | 2025-03-17T00:34:14Z |
| publishDate | 2011-09-01 |
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| series | PLoS Computational Biology |
| spelling | doaj.art-221e2cceb71e4506b0d27e02bd8dc2662025-02-21T05:31:56ZengPublic 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.https://journals.plos.org/ploscompbiol/article/file?id=10.1371/journal.pcbi.1002145&type=printable |
| 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 |
| title | 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_short | Filament depolymerization can explain chromosome pulling during bacterial mitosis. |
| title_sort | filament depolymerization can explain chromosome pulling during bacterial mitosis |
| url | https://journals.plos.org/ploscompbiol/article/file?id=10.1371/journal.pcbi.1002145&type=printable |
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