DNA Supercoiling: an Ancestral Regulator of Gene Expression in Pathogenic Bacteria?

DNA supercoiling acts as a global and ancestral regulator of bacterial gene expression. In this review, we advocate that it plays a pivotal role in host-pathogen interactions by transducing environmental signals to the bacterial chromosome and coordinating its transcriptional response. We present available evidence that DNA supercoiling is modulated by environmental stress conditions relevant to the infection process according to ancestral mechanisms, in zoopathogens as well as phytopathogens. We review the results of transcriptomics studies obtained in widely distant bacterial species, showing that such structural transitions of the chromosome are associated to a complex transcriptional response affecting a large fraction of the genome. Mechanisms and computational models of the transcriptional regulation by DNA supercoiling are then discussed, involving both basal interactions of RNA Polymerase with promoter DNA, and more specific interactions with regulatory proteins. A final part is specifically focused on the regulation of virulence genes within pathogenicity islands of several pathogenic bacterial species.

• Publication year

  2019

• Venue

  Computational and Structural Biotechnology Journal

• Publication date

  2019-07-26

• Fields of study

  Biology, Medicine, Environmental Science

• Identifiers
  DOI 10.1016/j.csbj.2019.07.013PMID 31452857PMCID 6700405
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• NapA (Rv0430), a Novel Nucleoid-Associated Protein that Regulates a Virulence Operon in Mycobacterium tuberculosis in a Supercoiling-Dependent Manner.

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• Bacterial genome architecture shapes global transcriptional regulation by DNA supercoiling

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• Transcriptional Bursts in a Nonequilibrium Model for Gene Regulation by Supercoiling.

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  2018cited by this paper
• Properties of gene expression and chromatin structure with mechanically regulated elongation

  2018influential reference
• Single-nucleotide-resolution mapping of DNA gyrase cleavage sites across the Escherichia coli genome

  2018cited by this paper
• Biochemical Basis of E. coli Topoisomerase I Relaxation Activity Reduction by Nonenzymatic Lysine Acetylation

  2018cited by this paper
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• Negative supercoiling of DNA by gyrase is inhibited in Salmonella enterica serovar Typhimurium during adaptation to acid stress

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• Inhibition of the gyrA promoter by transcription-coupled DNA supercoiling in Escherichia coli

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• Supercoiling of an excised genomic island represses effector gene expression to prevent activation of host resistance

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• Regulation of the gyr operon of Mycobacterium tuberculosis by overlapping promoters, DNA topology, and reiterative transcription.

  2018cited by this paper
• Bridging Chromosomal Architecture and Pathophysiology of Streptococcus pneumoniae

  2017cited by this paper
• Mechanism of transcription initiation and promoter escape by E. coli RNA polymerase

  2017cited by this paper
• Transcription facilitated genome-wide recruitment of topoisomerase I and DNA gyrase

  2017cited by this paper
• The Transcriptome of Streptococcus pneumoniae Induced by Local and Global Changes in Supercoiling

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• Control of virulence gene transcription by indirect readout in Vibrio cholerae and Salmonella enterica serovar Typhimurium

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• An increase in negative supercoiling in bacteria reveals topology-reacting gene clusters and a homeostatic response mediated by the DNA topoisomerase I gene

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• DNA supercoiling is a fundamental regulatory principle in the control of bacterial gene expression

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  2016cited by this paper
• Tempo and mode of genome evolution in a 50,000-generation experiment

  2016cited by this paper
• Stochastic Model of Supercoiling-Dependent Transcription.

  2016cited by this paper
• Genome scale patterns of supercoiling in a bacterial chromosome

  2016cited by this paper
• Insights into the Mechanisms of Basal Coordination of Transcription Using a Genome-Reduced Bacterium

  2016cited by this paper
• Transcription-coupled DNA supercoiling dictates the chromosomal arrangement of bacterial genes

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• Conserved Units of Co-Expression in Bacterial Genomes: An Evolutionary Insight into Transcriptional Regulation

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• Chromosomal “Stress-Response” Domains Govern the Spatiotemporal Expression of the Bacterial Virulence Program

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• Genome-wide study of mRNA degradation and transcript elongation in Escherichia coli

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• The Localization and Action of Topoisomerase IV in Escherichia coli Chromosome Segregation Is Coordinated by the SMC Complex, MukBEF

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• From ingestion to colonization: the influence of the host environment on regulation of the LEE encoded type III secretion system in enterohaemorrhagic Escherichia coli

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• Chromosomal position shift of a regulatory gene alters the bacterial phenotype

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• Gene Regulation by H-NS as a Function of Growth Conditions Depends on Chromosomal Position in Escherichia coli

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• Role of the LysR-type transcriptional regulator PecT and DNA supercoiling in the thermoregulation of pel genes, the major virulence factors in Dickeya dadantii.

  2014cited by this paper
• Supercoiling in DNA and chromatin☆

  2014cited by this paper
• Role of Global and Local Topology in the Regulation of Gene Expression in Streptococcus pneumoniae

  2014cited by this paper
• Bacterial Regulon Evolution: Distinct Responses and Roles for the Identical OmpR Proteins of Salmonella Typhimurium and Escherichia coli in the Acid Stress Response

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• Unprecedented High-Resolution View of Bacterial Operon Architecture Revealed by RNA Sequencing

  2014cited by this paper
• Altering gene expression by aminocoumarins: the role of DNA supercoiling in Staphylococcus aureus

  2014cited by this paper
• Mechanism of transcriptional bursting in bacteria.

  2014cited by this paper
• Torsion-Mediated Interaction between Adjacent Genes

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• Making the Bend: DNA Tertiary Structure and Protein-DNA Interactions

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• Twist-DNA: computing base-pair and bubble opening probabilities in genomic superhelical DNA

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• Temperature dependence of the DNA double helix at the nanoscale: structure, elasticity, and fluctuations.

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• Transcription dependent dynamic supercoiling is a short-range genomic force

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• Clinically Relevant Mutant DNA Gyrase Alters Supercoiling, Changes the Transcriptome, and Confers Multidrug Resistance

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• Transcription Under Torsion

  2013cited by this paper
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  2011cited by this paper
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  2011cited by this paper
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  2011cited by this paper
• The genome of Streptococcus pneumoniae is organized in topology-reacting gene clusters

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  2010cited by this paper
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• The functional response of upstream DNA to dynamic supercoiling in vivo

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  2005influential reference
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• Long-Term Experimental Evolution in Escherichia coli. XII. DNA Topology as a Key Target of Selection

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  2003cited by this paper
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  2002cited by this paper
• DNA topology-mediated control of global gene expression in Escherichia coli.

  2002cited by this paper
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  2002cited by this paper

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