A bifunctional glycosyltransferase from Agrobacterium tumefaciens synthesizes monoglucosyl and glucuronosyl diacylglycerol under phosphate deprivation

J Biol Chem. 2014 Apr 4;289(14):10104-14. doi: 10.1074/jbc.M113.519298. Epub 2014 Feb 20.

Abstract

Glycolipids are mainly found in phototrophic organisms (like plants and cyanobacteria), in Gram-positive bacteria, and a few other bacterial phyla. Besides the function as bulk membrane lipids, they often play a role under phosphate deprivation as surrogates for phospholipids. The Gram-negative Agrobacterium tumefaciens accumulates four different glycolipids under phosphate deficiency, including digalactosyl diacylglycerol and glucosylgalactosyl diacylglycerol synthesized by a processive glycosyltransferase. The other two glycolipids have now been identified by mass spectrometry and nuclear magnetic resonance spectroscopy as monoglucosyl diacylglycerol and glucuronosyl diacylglycerol. These two lipids are synthesized by a single promiscuous glycosyltransferase encoded by the ORF atu2297, with UDP-glucose or UDP-glucuronic acid as sugar donors. The transfer of sugars differing in their chemistry is a novel feature not observed before for lipid glycosyltransferases. Furthermore, this enzyme is the first glucuronosyl diacylglycerol synthase isolated. Deletion mutants of Agrobacterium lacking monoglucosyl diacylglycerol and glucuronosyl diacylglycerol or all glycolipids are not impaired in growth or virulence during infection of tobacco leaf discs. Our data suggest that the four glycolipids and the nonphospholipid diacylglyceryl trimethylhomoserine can mutually replace each other during phosphate deprivation. This redundancy of different nonphospholipids may represent an adaptation mechanism to enhance the competitiveness in nature.

Keywords: Bacteria; Bifunctional; Chromatography; Glucuronic Acid; Glycolipids; Glycosyltransferases; Gram-negative; Membrane Bilayer; Q-TOF.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Agrobacterium tumefaciens / enzymology*
  • Agrobacterium tumefaciens / genetics
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism*
  • Glucosyltransferases / genetics
  • Glucosyltransferases / metabolism*
  • Glycolipids / biosynthesis*
  • Glycolipids / genetics
  • Nicotiana / microbiology
  • Phosphates / metabolism
  • Plant Leaves / microbiology
  • Uridine Diphosphate Glucose / genetics
  • Uridine Diphosphate Glucose / metabolism
  • Uridine Diphosphate Glucuronic Acid / genetics
  • Uridine Diphosphate Glucuronic Acid / metabolism

Substances

  • Bacterial Proteins
  • Glycolipids
  • Phosphates
  • glucosyl diacylglycerol
  • glucuronosyl diacylglycerol
  • Uridine Diphosphate Glucuronic Acid
  • Glucosyltransferases
  • Uridine Diphosphate Glucose