Monoglucosyldiacylglycerol, a Foreign Lipid, Can Substitute for Phosphatidylethanolamine in Essential Membrane-associated Functions in Escherichia coli

Malin Wikström, Jun Xie, Mikhail Bogdanov, Eugenia Mileykovskaya, Philip Heacock, Åke Wieslander, William Dowhan

Research output: Contribution to journalArticle

52 Citations (Scopus)

Abstract

The mechanisms by which lipid bilayer properties govern or influence membrane protein functions are little understood, but a liquid-crystalline state and the presence of anionic and nonbilayer (NB)-prone lipids seem important. An Escherichia coli mutant lacking the major membrane lipid phosphatidylethanolamine (NB-prone) requires divalent cations for viability and cell integrity and is impaired in several membrane functions that are corrected by introduction of the "foreign" NB-prone neutral glycolipid α-monoglucosyldiacylglycerol (MGlcDAG) synthesized by the MGlcDAG synthase from Acholeplasma laidlawii. Dependence on Mg2+ was reduced, and cellular yields and division malfunction were greatly improved. The increased passive membrane permeability of the mutant was not abolished, but protein-mediated osmotic stress adaptation to salts and sucrose was recovered by the presence of MGlcDAG. MGlcDAG also restored tryptophan prototrophy and active transport function of lactose permease, both critically dependent on phosphatidylethanolamine. Three mechanisms can explain the observed effects: NB-prone MGlcDAG improves the quenched lateral pressure profile across the bilayer; neutral MGlcDAG dilutes the high anionic lipid surface charge; MGlcDAG provides a neutral lipid that can hydrogen bond and/or partially ionize. The reduced dependence on Mg2+ and lack of correction by high monovalent salts strongly support the essential nature of the NB properties of MGlcDAG.

Original languageEnglish (US)
Pages (from-to)10484-10493
Number of pages10
JournalJournal of Biological Chemistry
Volume279
Issue number11
DOIs
StatePublished - Mar 12 2004
Externally publishedYes

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Escherichia coli
Membranes
Lipids
Salts
Acholeplasma laidlawii
Lipid bilayers
Active Biological Transport
Glycolipids
Osmotic Pressure
Divalent Cations
Lipid Bilayers
Surface charge
Membrane Lipids
Tryptophan
Sucrose
Hydrogen
Permeability
Cell Survival
Hydrogen bonds
Membrane Proteins

ASJC Scopus subject areas

  • Biochemistry
  • Molecular Biology
  • Cell Biology

Cite this

Monoglucosyldiacylglycerol, a Foreign Lipid, Can Substitute for Phosphatidylethanolamine in Essential Membrane-associated Functions in Escherichia coli. / Wikström, Malin; Xie, Jun; Bogdanov, Mikhail; Mileykovskaya, Eugenia; Heacock, Philip; Wieslander, Åke; Dowhan, William.

In: Journal of Biological Chemistry, Vol. 279, No. 11, 12.03.2004, p. 10484-10493.

Research output: Contribution to journalArticle

Wikström, Malin ; Xie, Jun ; Bogdanov, Mikhail ; Mileykovskaya, Eugenia ; Heacock, Philip ; Wieslander, Åke ; Dowhan, William. / Monoglucosyldiacylglycerol, a Foreign Lipid, Can Substitute for Phosphatidylethanolamine in Essential Membrane-associated Functions in Escherichia coli. In: Journal of Biological Chemistry. 2004 ; Vol. 279, No. 11. pp. 10484-10493.
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