Asymmetric Chromosome Segregation and Cell Division in DNA Damage-induced Bacterial Filaments

Overview

Journal Mol Biol Cell

Specialties Cell Biology
Molecular Biology

Date 2020 Oct 28

PMID 33112716

Citations 11

Authors

Suchitha Raghunathan

Afroze Chimthanawala

Sandeep Krishna

Anthony G Vecchiarelli

Anjana Badrinarayanan

Affiliations

Soon will be listed here.

Abstract

Faithful propagation of life requires coordination of DNA replication and segregation with cell growth and division. In bacteria, this results in cell size homeostasis and periodicity in replication and division. The situation is perturbed under stress such as DNA damage, which induces filamentation as cell cycle progression is blocked to allow for repair. Mechanisms that release this morphological state for reentry into wild-type growth are unclear. Here we show that damage-induced filaments divide asymmetrically, producing short daughter cells that tend to be devoid of damage and have wild-type size and growth dynamics. The Min-system primarily determines division site location in the filament, with additional regulation of division completion by chromosome segregation. Collectively, we propose that coordination between chromosome (and specifically segregation and cell division may result in asymmetric division in damage-induced filaments and facilitate recovery from a stressed state.

Citing Articles

An ecological and stochastic perspective on persisters resuscitation.

Alonso-Vasquez T, Giovannini M, Garbini G, Dziurzynski M, Bacci G, Coppini E Comput Struct Biotechnol J. 2025; 27:1-9.

PMID: 39760074 PMC: 11697298. DOI: 10.1016/j.csbj.2024.12.002.

Dysregulated DnaB unwinding induces replisome decoupling and daughter strand gaps that are countered by RecA polymerization.

Behrmann M, Perera H, Welikala M, Matthews J, Butterworth L, Trakselis M Nucleic Acids Res. 2024; 52(12):6977-6993.

PMID: 38808668 PMC: 11229327. DOI: 10.1093/nar/gkae435.

Proline-rich acidic protein 1 upregulates mitotic arrest deficient 1 to promote cisplatin-resistance of colorectal carcinoma by restraining mitotic checkpoint complex assembly.

Song J, Chen Y, Yu H, Zheng L, Wang Y, Li D J Cancer. 2023; 14(9):1515-1530.

PMID: 37325046 PMC: 10266255. DOI: 10.7150/jca.84048.

Chromosome Segregation and Cell Division Defects in Recombination Mutants Exposed to Different DNA-Damaging Treatments.

Zahradka K, Repar J, dermic D, Zahradka D Microorganisms. 2023; 11(3).

PMID: 36985274 PMC: 10051365. DOI: 10.3390/microorganisms11030701.

Resuscitation dynamics reveal persister partitioning after antibiotic treatment.

Fang X, Allison K Mol Syst Biol. 2023; 19(4):e11320.

PMID: 36866643 PMC: 10090945. DOI: 10.15252/msb.202211320.

References

Lioy V, Cournac A, Marbouty M, Duigou S, Mozziconacci J, Espeli O . Multiscale Structuring of the E. coli Chromosome by Nucleoid-Associated and Condensin Proteins. Cell. 2018; 172(4):771-783.e18. DOI: 10.1016/j.cell.2017.12.027. View

Tsang M, Bernhardt T . Guiding divisome assembly and controlling its activity. Curr Opin Microbiol. 2015; 24:60-5. PMC: 4380671. DOI: 10.1016/j.mib.2015.01.002. View

Hill N, Kadoya R, Chattoraj D, Levin P . Cell size and the initiation of DNA replication in bacteria. PLoS Genet. 2012; 8(3):e1002549. PMC: 3291569. DOI: 10.1371/journal.pgen.1002549. View

Mannik J, Castillo D, Yang D, Siopsis G, Mannik J . The role of MatP, ZapA and ZapB in chromosomal organization and dynamics in Escherichia coli. Nucleic Acids Res. 2016; 44(3):1216-26. PMC: 4756834. DOI: 10.1093/nar/gkv1484. View

DONACHIE W . Relationship between cell size and time of initiation of DNA replication. Nature. 1968; 219(5158):1077-9. DOI: 10.1038/2191077a0. View

Quinlan A, Hall I . BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics. 2010; 26(6):841-2. PMC: 2832824. DOI: 10.1093/bioinformatics/btq033. View

Wallden M, Fange D, Lundius E, Baltekin O, Elf J . The Synchronization of Replication and Division Cycles in Individual E. coli Cells. Cell. 2016; 166(3):729-739. DOI: 10.1016/j.cell.2016.06.052. View

Justice S, Hung C, Theriot J, Fletcher D, Anderson G, Footer M . Differentiation and developmental pathways of uropathogenic Escherichia coli in urinary tract pathogenesis. Proc Natl Acad Sci U S A. 2004; 101(5):1333-8. PMC: 337053. DOI: 10.1073/pnas.0308125100. View

Taheri-Araghi S, Bradde S, Sauls J, Hill N, Levin P, Paulsson J . Cell-size control and homeostasis in bacteria. Curr Biol. 2014; 25(3):385-391. PMC: 4323405. DOI: 10.1016/j.cub.2014.12.009. View

10.

Aldridge B, Fernandez-Suarez M, Heller D, Ambravaneswaran V, Irimia D, Toner M . Asymmetry and aging of mycobacterial cells lead to variable growth and antibiotic susceptibility. Science. 2011; 335(6064):100-4. PMC: 3397429. DOI: 10.1126/science.1216166. View

11.

Paintdakhi A, Parry B, Campos M, Irnov I, Elf J, Surovtsev I . Oufti: an integrated software package for high-accuracy, high-throughput quantitative microscopy analysis. Mol Microbiol. 2015; 99(4):767-77. PMC: 4752901. DOI: 10.1111/mmi.13264. View

12.

Raghunathan S, Badrinarayanan A . Tracking Bacterial Chromosome Dynamics with Microfluidics-Based Live Cell Imaging. Methods Mol Biol. 2019; 2004:223-238. DOI: 10.1007/978-1-4939-9520-2_17. View

13.

Rudolph C, Upton A, Lloyd R . Replication fork stalling and cell cycle arrest in UV-irradiated Escherichia coli. Genes Dev. 2007; 21(6):668-81. PMC: 1820941. DOI: 10.1101/gad.417607. View

14.

Li H, Durbin R . Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics. 2009; 25(14):1754-60. PMC: 2705234. DOI: 10.1093/bioinformatics/btp324. View

15.

Wu F, Swain P, Kuijpers L, Zheng X, Felter K, Guurink M . Cell Boundary Confinement Sets the Size and Position of the E. coli Chromosome. Curr Biol. 2019; 29(13):2131-2144.e4. PMC: 7050463. DOI: 10.1016/j.cub.2019.05.015. View

16.

Bos J, Zhang Q, Vyawahare S, Rogers E, Rosenberg S, Austin R . Emergence of antibiotic resistance from multinucleated bacterial filaments. Proc Natl Acad Sci U S A. 2014; 112(1):178-83. PMC: 4291622. DOI: 10.1073/pnas.1420702111. View

17.

Badrinarayanan A, Le T, Spille J, Cisse I, Laub M . Global analysis of double-strand break processing reveals in vivo properties of the helicase-nuclease complex AddAB. PLoS Genet. 2017; 13(5):e1006783. PMC: 5443536. DOI: 10.1371/journal.pgen.1006783. View

18.

KANTOR G, DEERING R . Ultraviolet radiation studies of filamentous Escherichia coli B. J Bacteriol. 1966; 92(4):1062-9. PMC: 276379. DOI: 10.1128/jb.92.4.1062-1069.1966. View

19.

Burroughs A, Aravind L . RNA damage in biological conflicts and the diversity of responding RNA repair systems. Nucleic Acids Res. 2016; 44(18):8525-8555. PMC: 5062991. DOI: 10.1093/nar/gkw722. View

20.

Muraleedharan S, Freitas C, Mann P, Glatter T, Ringgaard S . A cell length-dependent transition in MinD-dynamics promotes a switch in division-site placement and preservation of proliferating elongated Vibrio parahaemolyticus swarmer cells. Mol Microbiol. 2018; 109(3):365-384. DOI: 10.1111/mmi.13996. View