Dynamic state of DNA topology is essential for genome condensation in bacteria

EMBO J. 2006 Nov 29;25(23):5591-602. doi: 10.1038/sj.emboj.7601414. Epub 2006 Nov 9.

Abstract

In bacteria, Dps is one of the critical proteins to build up a condensed nucleoid in response to the environmental stresses. In this study, we found that the expression of Dps and the nucleoid condensation was not simply correlated in Escherichia coli, and that Fis, which is an E. coli (gamma-Proteobacteria)-specific nucleoid protein, interfered with the Dps-dependent nucleoid condensation. Atomic force microscopy and Northern blot analyses indicated that the inhibitory effect of Fis was due to the repression of the expression of Topoismerase I (Topo I) and DNA gyrase. In the Deltafis strain, both topA and gyrA/B genes were found to be upregulated. Overexpression of Topo I and DNA gyrase enhanced the nucleoid condensation in the presence of Dps. DNA-topology assays using the cell extract showed that the extracts from the Deltafis and Topo I-/DNA gyrase-overexpressing strains, but not the wild-type extract, shifted the population toward relaxed forms. These results indicate that the topology of DNA is dynamically transmutable and that the topology control is important for Dps-induced nucleoid condensation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Bacterial Outer Membrane Proteins / antagonists & inhibitors
  • Bacterial Outer Membrane Proteins / genetics
  • Bacterial Outer Membrane Proteins / metabolism*
  • Blotting, Northern
  • Chromosomes, Bacterial / chemistry
  • Chromosomes, Bacterial / metabolism
  • Chromosomes, Bacterial / ultrastructure*
  • DNA Gyrase / genetics
  • DNA Gyrase / metabolism
  • DNA Topoisomerases, Type I / genetics
  • DNA Topoisomerases, Type I / metabolism
  • DNA, Bacterial / chemistry*
  • DNA, Bacterial / metabolism
  • DNA, Bacterial / ultrastructure
  • Escherichia coli / genetics*
  • Escherichia coli / metabolism
  • Escherichia coli Proteins / antagonists & inhibitors
  • Escherichia coli Proteins / genetics
  • Escherichia coli Proteins / metabolism*
  • Escherichia coli Proteins / physiology*
  • Factor For Inversion Stimulation Protein
  • Gene Expression Regulation, Bacterial
  • Gene Expression Regulation, Enzymologic
  • Genome, Bacterial
  • Microscopy, Atomic Force
  • Nucleic Acid Conformation*
  • Oxidative Stress
  • Transcription Factors / genetics
  • Transcription Factors / physiology*

Substances

  • Bacterial Outer Membrane Proteins
  • DNA, Bacterial
  • Escherichia coli Proteins
  • Factor For Inversion Stimulation Protein
  • Fis protein, E coli
  • Transcription Factors
  • dps protein, E coli
  • DNA Topoisomerases, Type I
  • DNA Gyrase