Structural basis of chiral wrap and T-segment capture by Escherichia coli DNA gyrase

Proc Natl Acad Sci U S A. 2024 Dec 3;121(49):e2407398121. doi: 10.1073/pnas.2407398121. Epub 2024 Nov 26.

Abstract

Type II topoisomerase DNA gyrase transduces the energy of ATP hydrolysis into the negative supercoiling of DNA. The postulated catalytic mechanism involves stabilization of a chiral DNA loop followed by the passage of the T-segment through the temporarily cleaved G-segment resulting in sign inversion. The molecular basis for this is poorly understood as the chiral loop has never been directly observed. We have obtained high-resolution cryoEM structures of Escherichia coli gyrase with chirally wrapped 217 bp DNA with and without the fluoroquinolone moxifloxacin (MFX). Each structure constrains a positively supercoiled figure-of-eight DNA loop stabilized by a GyrA β-pinwheel domain which has the structure of a flat disc. By comparing the catalytic site of the native drug-free and MFX-bound gyrase structures both of which contain a single metal ion, we demonstrate that the enzyme is observed in a native precatalytic state. Our data imply that T-segment trapping is not dependent on the dimerization of the ATPase domains which appears to only be possible after strand passage has taken place.

Keywords: DNA crossover; DNA-binding protein; antibiotics; molecular machine; topoisomerase.

MeSH terms

  • Catalytic Domain
  • Cryoelectron Microscopy
  • DNA Gyrase* / chemistry
  • DNA Gyrase* / metabolism
  • DNA, Bacterial / metabolism
  • DNA, Superhelical / chemistry
  • DNA, Superhelical / metabolism
  • Escherichia coli* / enzymology
  • Escherichia coli* / genetics
  • Escherichia coli* / metabolism
  • Fluoroquinolones / chemistry
  • Fluoroquinolones / pharmacology
  • Models, Molecular
  • Moxifloxacin* / chemistry
  • Nucleic Acid Conformation
  • Topoisomerase II Inhibitors / chemistry
  • Topoisomerase II Inhibitors / pharmacology

Substances

  • DNA Gyrase
  • Moxifloxacin
  • Fluoroquinolones
  • DNA, Superhelical
  • DNA, Bacterial
  • Topoisomerase II Inhibitors