Stress-induced Condensation of Bacterial Genomes Results in Re-pairing of Sister Chromosomes

Shechter, Nelia; Zaltzman, Liron; Weiner, Allon; Brumfeld, Vlad; Shimoni, Eyal; Fridmann-Sirkis, Yael; Minsky, Abraham

doi:10.1074/jbc.m113.473025

Cited by 22 publications

(34 citation statements)

References 73 publications

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“…Less critical repair may be mainly performed during the diffuse and extended nucleoid phase of the SOS response. The observations by Shechter et al (2013) and Levin-Zaidman et al (2000) of DNA condensation and formation of an ordered RecA-DNA coaggregate in DNA-damaged cells support the idea of an early SOS response stage involving stabilization of the DNA.…”

Section: Diffuse and Extended Nucleoidssupporting

confidence: 61%

DNA compaction in the early part of the SOS response is dependent on RecN and RecA

Odsbu

Skarstad

2014

Microbiology

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The nucleoids of undamaged Escherichia coli cells have a characteristic shape and number, which is dependent on the growth medium. Upon induction of the SOS response by a low dose of UV irradiation an extensive reorganization of the nucleoids occurred. Two distinct phases were observed by fluorescence microscopy. First, the nucleoids were found to change shape and fuse into compact structures at midcell. The compaction of the nucleoids lasted for 10-20 min and was followed by a phase where the DNA was dispersed throughout the cells. This second phase lasted for~1 h. The compaction was found to be dependent on the recombination proteins RecA, RecO and RecR as well as the SOS-inducible, SMC (structural maintenance of chromosomes)-like protein RecN. RecN protein is produced in high amounts during the first part of the SOS response. It is possible that the RecN-mediated 'compact DNA' stage at the beginning of the SOS response serves to stabilize damaged DNA prior to recombination and repair.

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Section: Diffuse and Extended Nucleoidssupporting

confidence: 61%

DNA compaction in the early part of the SOS response is dependent on RecN and RecA

Odsbu

Skarstad

2014

Microbiology

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“…This suggests that during the first 120 min of post‐irradiation incubation, the cell cycle was not completely blocked, and nucleoid segregation that began before irradiation ended during this time (http://onlinelibrary.wiley.com/doi/10.1111/mmi.13064/suppinfo). However, we cannot exclude that, as in E. coli , stress‐induced condensation of bacterial genomes results, in some cells, in re‐pairing of sister chromosomes to facilitate DNA repair (Shechter et al ., ), contributing to the decrease of the bilobed nucleoid proportion.…”

Section: Resultsmentioning

confidence: 97%

“…This hypothesis is in agreement with the observations of Shechter et al . () in E. coli , where stress‐induced condensation of bacterial genomes results in re‐pairing of sister chromosomes to facilitate DNA repair.…”

Section: Discussionmentioning

confidence: 99%

Nucleoid organization in the radioresistant bacterium Deinococcus radiodurans

Passot

Nguyen

Dard-Dascot³

et al. 2015

Molecular Microbiology

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SummaryProcesses favoring the exceptional resistance to genotoxic stress of Deinococcus radiodurans are not yet completely characterized. It was postulated that its nucleoid and chromosome(s) organization could participate in the DNA double strand break repair process. Here, we investigated the organization of chromosome 1 by localization of three chromosomal loci including oriC, Ter and a locus located in its left arm. For this purpose, we used a ParB-parS system to visualize the position of the loci before and after exposure to γ-rays. By comparing the number of fluorescent foci with the number of copies of the studied loci present in the cells measured by quantitative polymerase chain reaction (qPCR), we demonstrated that the 4-10 copies of chromosome 1 per cell are dispersed within the nucleoid before irradiation, indicating that the chromosome copies are not prealigned. Chromosome segregation is progressive but not co-ordinated, allowing each locus to be paired with its sister during part of the cell cycle. After irradiation, the nucleoid organization is modified, involving a transient alignment of the loci in the late stage of DNA repair and a delay of segregation of the Ter locus. We discuss how these events can influence DNA double strand break repair.

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“…Some species (e.g., Bacillus subtilis) also possess a rudimentary analog to the eukaryotic nonhomologous end-joining pathway (NHEJ) (34), and a modified version of NHEJ, named alternative end joining (A-EJ), exists in E. coli (35). Recently, genome condensation under stress conditions was suggested as an additional DSB repair mechanism that operates in E. coli (36). Of these DNA DSB repair mechanisms, only genes involved in HR pathways have been identified in the P. arcticus genome (19).…”

Section: Discussionmentioning

confidence: 99%

DNA Double-Strand Break Repair at −15°C

Dieser

Battista

Christner

2013

Appl Environ Microbiol

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The survival of microorganisms in ancient glacial ice and permafrost has been ascribed to their ability to persist in a dormant, metabolically inert state. An alternative possibility, supported by experimental data, is that microorganisms in frozen matrices are able to sustain a level of metabolic function that is sufficient for cellular repair and maintenance. To examine this experimentally, frozen populations of Psychrobacter arcticus 273-4 were exposed to ionizing radiation (IR) to simulate the damage incurred from natural background IR sources in the permafrost environment from over ϳ225 kiloyears (ky). High-molecularweight DNA was fragmented by exposure to 450 Gy of IR, which introduced an average of 16 double-strand breaks (DSBs) per chromosome. During incubation at ؊15°C for 505 days, P. arcticus repaired DNA DSBs in the absence of net growth. Based on the time frame for the assembly of genomic fragments by P. arcticus, the rate of DNA DSB repair was estimated at 7 to 10 DSBs year ؊1 under the conditions tested. Our results provide direct evidence for the repair of DNA lesions, extending the range of complex biochemical reactions known to occur in bacteria at frozen temperatures. Provided that sufficient energy and nutrient sources are available, a functional DNA repair mechanism would allow cells to maintain genome integrity and augment microbial survival in icy terrestrial or extraterrestrial environments. The results from decades of studying the stability of DNA in bacteria may be summarized in two uncomplicated axioms. First, genomic DNA is not inert; the genetic material will degrade with time, and damage will accumulate unless that degradation is repaired. And second, if this degradation is not reversed, the cell will die. The repair processes that cope with DNA damage are integral to life, and it is assumed that all species express means of maintaining genetic integrity.The importance of DNA repair to cell viability motivated extensive study of the biochemistry and molecular biology of these repair processes in model organisms such as Escherichia coli (1). Although the advantages of using this species for such studies are well documented, there is a question as to whether detailed knowledge of DNA repair in E. coli as observed under standard laboratory conditions adequately represents the full spectrum of bacterial responses to DNA damage. For instance, DNA repair is an energy-intensive activity (2, 3), but microbial species in nature rarely experience optimal conditions for growth or have access to nutrient excess. Without a generous supply of energy, cells may need to generate a more measured response, rationing available resources in a manner that prioritizes the most important tasks for survival. Moreover, viability in the absence of cellular reproduction is sustained only by cells that do not accumulate a level of damage (e.g., to DNA) that exceeds a threshold beyond which effective repair is no longer possible.Genomic DNA and viable bacteria are preserved in ancient ice and permafrost for hun...

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Stress-induced Condensation of Bacterial Genomes Results in Re-pairing of Sister Chromosomes

Cited by 22 publications

References 73 publications

DNA compaction in the early part of the SOS response is dependent on RecN and RecA

DNA compaction in the early part of the SOS response is dependent on RecN and RecA

Nucleoid organization in the radioresistant bacterium Deinococcus radiodurans

DNA Double-Strand Break Repair at −15°C

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