Structure, kinetics, and mechanism of Pseudomonas putida sulfoquinovose dehydrogenase, the first enzyme in the sulfoglycolytic Entner-Doudoroff pathway

Biochem J. 2025 Jan 22;482(2):57-72. doi: 10.1042/BCJ20240605.

Abstract

The sulfosugar sulfoquinovose (SQ) is catabolized through the sulfoglycolytic Entner-Doudoroff pathway, beginning with the oxidation of SQ to sulfogluconolactone by SQ dehydrogenase. We present a comprehensive structural and kinetic characterization of Pseudomonas putida SQ dehydrogenase (PpSQDH). PpSQDH is a tetrameric enzyme belonging to the short-chain dehydrogenase/reductase (SDR) superfamily with a strong preference for NAD+ over NADP+. Kinetic analysis revealed a rapid equilibrium ordered mechanism in which the NAD+ cofactor is the first substrate to bind, and NADH is the last product to dissociate. Structural studies revealed a homotetrameric structure in solution and crystals, involving cross-subunit interactions in which the C-terminus residue (Gln260) inserts into the diagonally opposite subunit to form part of the second shell of residues lining the active site. Complexes of PpSQDH with SQ or NAD+ provide insight into the recognition of SQ and together with the kinetic analysis allow the proposal of a catalytic reaction mechanism. Our findings illuminate the mechanism of SQ degradation and the evolution of the SDR superfamily for organosulfonate catabolism.

Keywords: enzyme mechanism; organosulfur; short-chain dehydrogenase/reductase; sulfoglycolysis; sulfur cycle.

MeSH terms

  • Bacterial Proteins* / chemistry
  • Bacterial Proteins* / genetics
  • Bacterial Proteins* / metabolism
  • Carbohydrate Dehydrogenases / chemistry
  • Carbohydrate Dehydrogenases / genetics
  • Carbohydrate Dehydrogenases / metabolism
  • Catalytic Domain
  • Crystallography, X-Ray
  • Kinetics
  • Methylglucosides
  • Models, Molecular
  • NAD* / metabolism
  • NADP / metabolism
  • Pseudomonas putida* / enzymology
  • Pseudomonas putida* / genetics
  • Substrate Specificity

Substances

  • NAD
  • Bacterial Proteins
  • sulfoquinovose
  • Carbohydrate Dehydrogenases
  • NADP
  • Methylglucosides