Biochemical and structural characterization of a short-chain dehydrogenase/reductase of Thermus thermophilus HB8: a hyperthermostable aldose-1-dehydrogenase with broad substrate specificity

Chem Biol Interact. 2009 Mar 16;178(1-3):117-26. doi: 10.1016/j.cbi.2008.09.018. Epub 2008 Sep 24.

Abstract

Thermus thermophilus HB8 is a hyperthermophilic bacterium, thriving at environmental temperature near 80 degrees C. The genomic analysis of this bacterium predicted 18 genes for proteins belonging to the short-chain dehydrogenase/reductases (SDR) superfamily, but their functions remain unknown. A SDR encoded in a gene (TTHA0369) was chosen for functional and structural characterization. Enzymatic assays revealed that the recombinant tetrameric protein has a catalytic activity as NAD(+)-dependent aldose 1-dehydroganse, which accepts various aldoses such as d-fucose, d-galactose, d-glucose, l-arabinose, cellobiose and lactose. The enzyme also oxidized non-sugar alicyclic alcohols, and was competitively inhibited by hexestrol, 1,10-phenanthroline, 2,3-benzofuran and indole. The enzyme was stable at pH 2-13 and up to 85 degrees C. We have determined the crystal structure of the enzyme-NAD(+) binary complex at 1.65A resolution. The structure provided evidence for the strict coenzyme specificity and broad substrate specificity of the enzyme. Additionally, it has unusual features, aromatic-aromatic interactions among Phe141 and Phe249 in the subunit interface and hydrogen networks around the C-terminal Asp-Gly-Gly sequence at positions 242-244. Stability analysis of the mutant D242N, F141A and F249A enzymes indicated that the two unique structural features contribute to the hyperthermostability of the enzyme. This study demonstrates that aldose 1-dehydrogenase is a member of the SDR superfamily, and provides a novel structural basis of thermostability.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Carbohydrate Dehydrogenases / chemistry
  • Carbohydrate Dehydrogenases / isolation & purification
  • Carbohydrate Dehydrogenases / metabolism*
  • Crystallization
  • Enzyme Stability
  • Hydrogen-Ion Concentration
  • Oxidoreductases Acting on CH-CH Group Donors / chemistry
  • Oxidoreductases Acting on CH-CH Group Donors / isolation & purification
  • Oxidoreductases Acting on CH-CH Group Donors / metabolism*
  • Protein Conformation
  • Substrate Specificity
  • Temperature
  • Thermus thermophilus / enzymology*

Substances

  • Carbohydrate Dehydrogenases
  • Oxidoreductases Acting on CH-CH Group Donors