Mannitol-1-phosphate dehydrogenases/phosphatases: a family of novel bifunctional enzymes for bacterial adaptation to osmotic stress

Environ Microbiol. 2015 Mar;17(3):711-9. doi: 10.1111/1462-2920.12503. Epub 2014 Jun 4.

Abstract

The nutritionally versatile soil bacterium Acinetobacter baylyi ADP1 copes with salt stress by the accumulation of compatible solutes, a strategy that is widespread in nature. This bacterium synthesizes the sugar alcohol mannitol de novo in response to osmotic stress. In a previous study, we identified MtlD, a mannitol-1-phosphate dehydrogenase, which is essential for mannitol biosynthesis and which catalyses the first step in mannitol biosynthesis, the reduction of fructose-6-phosphate (F-6-P) to the intermediate mannitol-1-phosphate (Mtl-1-P). Until now, the identity of the second enzyme, the phosphatase that catalyses the dephosphorylation of Mtl-1-P to mannitol, was elusive. Here we show that MtlD has a unique sequence among known mannitol-1-phosphate dehydrogenases with a haloacid dehalogenase (HAD)-like phosphatase domain at the N-terminus. This domain is indeed shown to have a phosphatase activity. Phosphatase activity is strictly Mg(2+) dependent. Nuclear magnetic resonance analysis revealed that purified MtlD catalyses not only reduction of F-6-P but also dephosphorylation of Mtl-1-P. MtlD of A. baylyi is the first bifunctional enzyme of mannitol biosynthesis that combines Mtl-1-P dehydrogenase and phosphatase activities in a single polypeptide chain. Bioinformatic analysis revealed that the bifunctional enzyme is widespread among Acinetobacter strains but only rarely present in other phylogenetic tribes.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acinetobacter / enzymology*
  • Acinetobacter / genetics
  • Amino Acid Sequence
  • Fructosephosphates / metabolism
  • Mannitol / metabolism
  • Mannitol Phosphates / metabolism
  • Molecular Sequence Data
  • Osmotic Pressure / physiology*
  • Phosphoric Monoester Hydrolases / genetics
  • Phosphoric Monoester Hydrolases / metabolism*
  • Phylogeny
  • Sugar Alcohol Dehydrogenases / genetics*
  • Sugar Alcohol Dehydrogenases / metabolism*

Substances

  • Fructosephosphates
  • Mannitol Phosphates
  • mannitol-1-phosphate
  • Mannitol
  • fructose-6-phosphate
  • Sugar Alcohol Dehydrogenases
  • mannitol-1-phosphate dehydrogenase
  • Phosphoric Monoester Hydrolases