Structure of galactarate dehydratase, a new fold in an enolase involved in bacterial fitness after antibiotic treatment

Protein Sci. 2020 Mar;29(3):711-722. doi: 10.1002/pro.3796. Epub 2019 Dec 17.

Abstract

Galactarate dehydratase (GarD) is the first enzyme in the galactarate/glucarate pathway and catalyzes the dehydration of galactarate to 3-keto-5-dehydroxygalactarate. This protein is known to increase colonization fitness of intestinal pathogens in antibiotic-treated mice and to promote bacterial survival during stress. The galactarate/glucarate pathway is widespread in bacteria, but not in humans, and thus could be a target to develop new inhibitors for use in combination therapy to combat antibiotic resistance. The structure of almost all the enzymes of the galactarate/glucarate pathway were solved previously, except for GarD, for which only the structure of the N-terminal domain was determined previously. Herein, we report the first crystal structure of full-length GarD solved using a seleno-methoionine derivative revealing a new protein fold. The protein consists of three domains, each presenting a novel twist as compared to their distant homologs. GarD in the crystal structure forms dimers and each monomer consists of three domains. The N-terminal domain is comprised of a β-clip fold, connected to the second domain by a long unstructured linker. The second domain serves as a dimerization interface between two monomers. The C-terminal domain forms an unusual variant of a Rossmann fold with a crossover and is built around a seven-stranded parallel β-sheet supported by nine α-helices. A metal binding site in the C-terminal domain is occupied by Ca2+ . The activity of GarD was corroborated by the production of 5-keto-4-deoxy-D-glucarate under reducing conditions and in the presence of iron. Thus, GarD is an unusual enolase with a novel protein fold never previously seen in this class of enzymes.

Keywords: Escherichia coli; antibiotic treatment; bacterial fitness; enolase; galactarate dehydratase; intestinal pathogens; novel fold.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Anti-Bacterial Agents / pharmacology*
  • Bacteria / drug effects*
  • Bacteria / enzymology*
  • Crystallography, X-Ray
  • Hydro-Lyases / chemistry*
  • Hydro-Lyases / metabolism
  • Microbial Sensitivity Tests
  • Models, Molecular
  • Molecular Structure
  • Phosphopyruvate Hydratase / chemistry*
  • Phosphopyruvate Hydratase / metabolism
  • Protein Folding / drug effects

Substances

  • Anti-Bacterial Agents
  • Hydro-Lyases
  • Phosphopyruvate Hydratase