Cell Boundary Confinement Sets the Size and Position of the E. coli Chromosome

Fabai Wu, Pinaki Swain, Louis Kuijpers, Xuan Zheng, Kevin Felter, Margot Guurink, Jacopo Solari, Suckjoon Jun, Thomas S. Shimizu, Debasish Chaudhuri, Bela Mulder*, Cees Dekker

*Corresponding author for this work

Research output: Contribution to journalArticleAcademicpeer-review

6 Citations (Scopus)

Abstract

Although the spatiotemporal structure of the genome is crucial to its biological function, many basic questions remain unanswered on the morphology and segregation of chromosomes. Here, we experimentally show in Escherichia coli that spatial confinement plays a dominant role in determining both the chromosome size and position. In non-dividing cells with lengths increased to 10 times normal, single chromosomes are observed to expand > 4-fold in size. Chromosomes show pronounced internal dynamics but exhibit a robust positioning where single nucleoids reside robustly at mid-cell, whereas two nucleoids self-organize at 1/4 and 3/4 positions. The cell-size-dependent expansion of the nucleoid is only modestly influenced by deletions of nucleoid-associated proteins, whereas osmotic manipulation experiments reveal a prominent role of molecular crowding. Molecular dynamics simulations with model chromosomes and crowders recapitulate the observed phenomena and highlight the role of entropic effects caused by confinement and molecular crowding in the spatial organization of the chromosome

Original languageEnglish
Pages (from-to)2131-2144.e4
JournalCurrent Biology
Volume29
Issue number13
DOIs
Publication statusPublished - 8 Jul 2019

Fingerprint

Chromosomes
Escherichia coli
chromosomes
cells
chromosome morphology
Chromosome Segregation
chromosome segregation
molecular dynamics
Molecular Dynamics Simulation
Cell Size
Molecular dynamics
Genome
Genes
genome
Computer simulation
Proteins
proteins
Experiments

Keywords

  • bacterial nucleoid
  • cell boundary confinement
  • chromosome segregation
  • chromosome size
  • crowders

Cite this

Wu, F., Swain, P., Kuijpers, L., Zheng, X., Felter, K., Guurink, M., ... Dekker, C. (2019). Cell Boundary Confinement Sets the Size and Position of the E. coli Chromosome. Current Biology, 29(13), 2131-2144.e4. https://doi.org/10.1016/j.cub.2019.05.015
Wu, Fabai ; Swain, Pinaki ; Kuijpers, Louis ; Zheng, Xuan ; Felter, Kevin ; Guurink, Margot ; Solari, Jacopo ; Jun, Suckjoon ; Shimizu, Thomas S. ; Chaudhuri, Debasish ; Mulder, Bela ; Dekker, Cees. / Cell Boundary Confinement Sets the Size and Position of the E. coli Chromosome. In: Current Biology. 2019 ; Vol. 29, No. 13. pp. 2131-2144.e4.
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abstract = "Although the spatiotemporal structure of the genome is crucial to its biological function, many basic questions remain unanswered on the morphology and segregation of chromosomes. Here, we experimentally show in Escherichia coli that spatial confinement plays a dominant role in determining both the chromosome size and position. In non-dividing cells with lengths increased to 10 times normal, single chromosomes are observed to expand > 4-fold in size. Chromosomes show pronounced internal dynamics but exhibit a robust positioning where single nucleoids reside robustly at mid-cell, whereas two nucleoids self-organize at 1/4 and 3/4 positions. The cell-size-dependent expansion of the nucleoid is only modestly influenced by deletions of nucleoid-associated proteins, whereas osmotic manipulation experiments reveal a prominent role of molecular crowding. Molecular dynamics simulations with model chromosomes and crowders recapitulate the observed phenomena and highlight the role of entropic effects caused by confinement and molecular crowding in the spatial organization of the chromosome",
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author = "Fabai Wu and Pinaki Swain and Louis Kuijpers and Xuan Zheng and Kevin Felter and Margot Guurink and Jacopo Solari and Suckjoon Jun and Shimizu, {Thomas S.} and Debasish Chaudhuri and Bela Mulder and Cees Dekker",
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Wu, F, Swain, P, Kuijpers, L, Zheng, X, Felter, K, Guurink, M, Solari, J, Jun, S, Shimizu, TS, Chaudhuri, D, Mulder, B & Dekker, C 2019, 'Cell Boundary Confinement Sets the Size and Position of the E. coli Chromosome', Current Biology, vol. 29, no. 13, pp. 2131-2144.e4. https://doi.org/10.1016/j.cub.2019.05.015

Cell Boundary Confinement Sets the Size and Position of the E. coli Chromosome. / Wu, Fabai; Swain, Pinaki; Kuijpers, Louis; Zheng, Xuan; Felter, Kevin; Guurink, Margot; Solari, Jacopo; Jun, Suckjoon; Shimizu, Thomas S.; Chaudhuri, Debasish; Mulder, Bela; Dekker, Cees.

In: Current Biology, Vol. 29, No. 13, 08.07.2019, p. 2131-2144.e4.

Research output: Contribution to journalArticleAcademicpeer-review

TY - JOUR

T1 - Cell Boundary Confinement Sets the Size and Position of the E. coli Chromosome

AU - Wu, Fabai

AU - Swain, Pinaki

AU - Kuijpers, Louis

AU - Zheng, Xuan

AU - Felter, Kevin

AU - Guurink, Margot

AU - Solari, Jacopo

AU - Jun, Suckjoon

AU - Shimizu, Thomas S.

AU - Chaudhuri, Debasish

AU - Mulder, Bela

AU - Dekker, Cees

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N2 - Although the spatiotemporal structure of the genome is crucial to its biological function, many basic questions remain unanswered on the morphology and segregation of chromosomes. Here, we experimentally show in Escherichia coli that spatial confinement plays a dominant role in determining both the chromosome size and position. In non-dividing cells with lengths increased to 10 times normal, single chromosomes are observed to expand > 4-fold in size. Chromosomes show pronounced internal dynamics but exhibit a robust positioning where single nucleoids reside robustly at mid-cell, whereas two nucleoids self-organize at 1/4 and 3/4 positions. The cell-size-dependent expansion of the nucleoid is only modestly influenced by deletions of nucleoid-associated proteins, whereas osmotic manipulation experiments reveal a prominent role of molecular crowding. Molecular dynamics simulations with model chromosomes and crowders recapitulate the observed phenomena and highlight the role of entropic effects caused by confinement and molecular crowding in the spatial organization of the chromosome

AB - Although the spatiotemporal structure of the genome is crucial to its biological function, many basic questions remain unanswered on the morphology and segregation of chromosomes. Here, we experimentally show in Escherichia coli that spatial confinement plays a dominant role in determining both the chromosome size and position. In non-dividing cells with lengths increased to 10 times normal, single chromosomes are observed to expand > 4-fold in size. Chromosomes show pronounced internal dynamics but exhibit a robust positioning where single nucleoids reside robustly at mid-cell, whereas two nucleoids self-organize at 1/4 and 3/4 positions. The cell-size-dependent expansion of the nucleoid is only modestly influenced by deletions of nucleoid-associated proteins, whereas osmotic manipulation experiments reveal a prominent role of molecular crowding. Molecular dynamics simulations with model chromosomes and crowders recapitulate the observed phenomena and highlight the role of entropic effects caused by confinement and molecular crowding in the spatial organization of the chromosome

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KW - cell boundary confinement

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Wu F, Swain P, Kuijpers L, Zheng X, Felter K, Guurink M et al. Cell Boundary Confinement Sets the Size and Position of the E. coli Chromosome. Current Biology. 2019 Jul 8;29(13):2131-2144.e4. https://doi.org/10.1016/j.cub.2019.05.015