Molecular Structure and Dynamics of Bacterial Nucleoids

Higgins, N. Patrick; Booker, Betty M.; Manna, Dipankar

doi:10.1007/978-90-481-3473-1_7

Cited by 3 publications

(8 citation statements)

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“…The twin domain impact of RNA transcription was also confirmed in Salmonella in 2010. Booker showed that supercoil density is elevated behind the highly transcribed rrnG operon and supercoils are depleted in the domain downstream of the operon [8,12]. Thus, RNA polymerase not only supercoils DNA in vivo at rates comparable to gyrase, transcription also forms the most abundant supercoil domain boundaries in the bacterial cell [62].…”

Section: Discussionmentioning

confidence: 99%

“…If gyrase binds to a domain with a transcription complex stalled by (+) supercoiling, a second burst occurs. When strong gyrase sites were added to plasmid bursting experiments along with gyrase, the bursting response was converted to a smooth expression pattern, which is the characteristic of rrnG operon and the 100 most highly transcribed operons in E. coli and Salmonella [12].…”

Section: Discussionmentioning

confidence: 99%

“…Topo I, a type IA topoisomerase, removes negative supercoiling in a cofactor-independent reaction that protects DNA from forming toxic R-loops caused by RNA invasion of DNA at hyper-supercoiled regions [10,11]. Gyrase replenishes (–) supercoils depleted downstream of operons [9,12] and Topo IV untangles and decatenates DNA strands and removes (+) supercoils generated during DNA replication and segregation [13,14,15].…”

Section: Introductionmentioning

confidence: 99%

“…Mutations that reduce the supercoil density (σ) of E. coli DNA by only 15% are toxic and alter the efficiency and/or fidelity of DNA replication [16], chromosome segregation [17,18], RNA transcription [19,20], homologous and site-specific recombination [16] and gene transposition reactions [21,22,23]. In sharp contrast, wild type (WT) Salmonella Typhimurium grows naturally at an average supercoil density 15% lower than E. coli [3] and Salmonella grows and produces well-formed colonies in strains having a complete loss of diffusible chromosome supercoiling [9,12].…”

Section: Introductionmentioning

confidence: 99%

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Supercoil Levels in E. coli and Salmonella Chromosomes Are Regulated by the C-Terminal 35–38 Amino Acids of GyrA

et al. 2019

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Prokaryotes have an essential gene—gyrase—that catalyzes negative supercoiling of plasmid and chromosomal DNA. Negative supercoils influence DNA replication, transcription, homologous recombination, site-specific recombination, genetic transposition and sister chromosome segregation. Although E. coli and Salmonella Typhimurium are close relatives with a conserved set of essential genes, E. coli DNA has a supercoil density 15% higher than Salmonella, and E. coli cannot grow at the supercoil density maintained by wild type (WT) Salmonella. E. coli is addicted to high supercoiling levels for efficient chromosomal folding. In vitro experiments were performed with four gyrase isoforms of the tetrameric enzyme (GyrA2:GyrB2). E. coli gyrase was more processive and faster than the Salmonella enzyme, but Salmonella strains with chromosomal swaps of E. coli GyrA lost 40% of the chromosomal supercoil density. Reciprocal experiments in E. coli showed chromosomal dysfunction for strains harboring Salmonella GyrA. One GyrA segment responsible for dis-regulation was uncovered by constructing and testing GyrA chimeras in vivo. The six pinwheel elements and the C-terminal 35–38 acidic residues of GyrA controlled WT chromosome-wide supercoiling density in both species. A model of enzyme processivity modulated by competition between DNA and the GyrA acidic tail for access to β-pinwheel elements is presented.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Supercoil Levels in E. coli and Salmonella Chromosomes Are Regulated by the C-Terminal 35–38 Amino Acids of GyrA

et al. 2019

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“…In eukaryotes, this is accomplished by well-defined histone proteins that form nucleosomal and chromatin structures and yet can be remodeled to allow for the decondensation critical for gene expression 5–9 . Although the bacterial genome must also be densely compacted, more than one-thousand-fold, and also organized for optimum functionality (chromosome replication/segregation, recombination and transcription) 10–14 , the mechanisms by which this is accomplished remain unclear. The lack of “beads-on-a-string” morphology indicates different and/or multiple roles for nucleoid-associated proteins.…”

Section: Introductionmentioning

confidence: 99%

Role of RNA Polymerase and Transcription in the Organization of the Bacterial Nucleoid

2013

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Nucleoid Expansion in RNAP Mutants Defective in rRNA Synthesis in Nutrient-Rich LB 8673 3.7.3. Lacking Transcription Foci and Expanded Nucleoid in Δ6rrn Mutant Cells 8674 3.7.4. Apparent Transcription Foci and Nucleoid Compaction in the "Relaxed" relA Mutant Cells during Amino Acid Starvation 8674 3.7.5. Evident Transcription Foci and Nucleoid Compaction in Cells Treated with Protein Synthesis Inhibitors 8674 3.8. Transcribing RNAP Locates at the Surface of the Nucleoid 8674 3.8.1. Transcription Foci Appear to Position at the Voids of the Nucleoid 8675 3.8.2. DNA Loops Enriched with RNAP Locate at the Periphery of the Nucleoid 8675 3.8.3. Non-Transcribing RNAP Scatters across the Nucleoid 8675 4. Model: Transcription Foci Condense the Nucleoid 8675 5. Conclusion and Perspectives 8677 Author Information 8677 Corresponding Author 8677 Notes 8677 Biographies 8677 Acknowledgments 8678 References 8678

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DNA topology of highly transcribed operons in Salmonella enterica serovar Typhimurium

Booker

Deng

Higgins

2010

Molecular Microbiology

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SummaryBacteria differ from eukaryotes by having the enzyme DNA gyrase, which catalyses the ATP-dependent negative supercoiling of DNA. Negative supercoils are essential for condensing chromosomes into an interwound (plectonemic) and branched structure known as the nucleoid. Topo-1 removes excess supercoiling in an ATP-independent reaction and works with gyrase to establish a topological equilibrium where supercoils move within 10 kb domains bounded by stochastic barriers along the sequence. However, transcription changes the stochastic pattern by generating supercoil diffusion barriers near the sites of gene expression. Using supercoildependent Tn3 and gd resolution assays, we studied DNA topology upstream, downstream and across highly transcribed operons. Whenever two Res sites flanked efficiently transcribed genes, resolution was inhibited and the loss in recombination efficiency was proportional to transcription level. Ribosomal RNA operons have the highest transcription rates, and resolution assays at the rrnG and rrnH operons showed inhibitory levels 40-100 times those measured in low-transcription zones. Yet, immediately upstream and downstream of RNA polymerase (RNAP) initiation and termination sites, supercoiling characteristics were similar to poorly transcribed zones. We present a model that explains why RNAP blocks plectonemic supercoil movement in the transcribed track and suggests how gyrase and TopA control upstream and downstream transcriptiondriven supercoiling.

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Molecular Structure and Dynamics of Bacterial Nucleoids

Cited by 3 publications

References 122 publications

Supercoil Levels in E. coli and Salmonella Chromosomes Are Regulated by the C-Terminal 35–38 Amino Acids of GyrA

Supercoil Levels in E. coli and Salmonella Chromosomes Are Regulated by the C-Terminal 35–38 Amino Acids of GyrA

Role of RNA Polymerase and Transcription in the Organization of the Bacterial Nucleoid

DNA topology of highly transcribed operons in Salmonella enterica serovar Typhimurium

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