Conformational changes allow processing of bulky substrates by a haloalkane dehalogenase with a small and buried active site

J Biol Chem. 2018 Jul 20;293(29):11505-11512. doi: 10.1074/jbc.RA117.000328. Epub 2018 Jun 1.

Abstract

Haloalkane dehalogenases catalyze the hydrolysis of halogen-carbon bonds in organic halogenated compounds and as such are of great utility as biocatalysts. The crystal structures of the haloalkane dehalogenase DhlA from the bacterium from Xanthobacter autotrophicus GJ10, specifically adapted for the conversion of the small 1,2-dichloroethane (DCE) molecule, display the smallest catalytic site (110 Å3) within this enzyme family. However, during a substrate-specificity screening, we noted that DhlA can catalyze the conversion of far bulkier substrates, such as the 4-(bromomethyl)-6,7-dimethoxy-coumarin (220 Å3). This large substrate cannot bind to DhlA without conformational alterations. These conformational changes have been previously inferred from kinetic analysis, but their structural basis has not been understood. Using molecular dynamic simulations, we demonstrate here the intrinsic flexibility of part of the cap domain that allows DhlA to accommodate bulky substrates. The simulations displayed two routes for transport of substrates to the active site, one of which requires the conformational change and is likely the route for bulky substrates. These results provide insights into the structure-dynamics function relationships in enzymes with deeply buried active sites. Moreover, understanding the structural basis for the molecular adaptation of DhlA to 1,2-dichloroethane introduced into the biosphere during the industrial revolution provides a valuable lesson in enzyme design by nature.

Keywords: active site; conformational change; dichloroethane degradation; enzyme catalysis; enzyme kinetics; enzyme mechanism; ethylene dichloride; haloalkane dehalogenase; molecular dynamics; molecular evolution; organic halogen; organohalogen; protein conformation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Catalytic Domain
  • Coumarins / chemistry
  • Coumarins / metabolism*
  • Crystallography, X-Ray
  • Ethylene Dichlorides / metabolism
  • Halogenation
  • Hydrolases / chemistry
  • Hydrolases / metabolism*
  • Kinetics
  • Methylation
  • Molecular Docking Simulation
  • Molecular Dynamics Simulation
  • Protein Conformation
  • Substrate Specificity
  • Xanthobacter / chemistry
  • Xanthobacter / enzymology*
  • Xanthobacter / metabolism

Substances

  • Coumarins
  • Ethylene Dichlorides
  • ethylene dichloride
  • Hydrolases
  • haloalkane dehalogenase

Associated data

  • PDB/2YXP
  • PDB/1B6G
  • PDB/1EDE
  • PDB/2HAD
  • PDB/1EDB
  • PDB/2DHE
  • PDB/2EDA
  • PDB/2DHD
  • PDB/1EDD
  • PDB/2EDC
  • PDB/2DHC
  • PDB/1HDE