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Originally published In Press as doi:10.1074/jbc.M211492200 on December 2, 2002

J. Biol. Chem., Vol. 278, Issue 10, 8420-8428, March 7, 2003
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Structural Features of Glycosyltransferases Synthesizing Major Bilayer and Nonbilayer-prone Membrane Lipids in Acholeplasma laidlawii and Streptococcus pneumoniae*,

Maria EdmanDagger §, Stefan BergDagger §, Patrik Storm||, Malin Wikström||, Susanne Vikström**, Anders ÖhmanDagger , and Åke Wieslander||Dagger Dagger

From the Dagger  Department of Biochemistry and the ** Department of Odontology, Umeå University, 90187 Umeå, Sweden and the || Department of Biochemistry and Biophysics, Stockholm University, 10691 Stockholm, Sweden

In membranes of Acholeplasma laidlawii two consecutively acting glucosyltransferases, the (i) alpha -monoglucosyldiacylglycerol (MGlcDAG) synthase (alMGS) (EC 2.4.1.157) and the (ii) alpha -diglucosyl-DAG (DGlcDAG) synthase (alDGS) (EC 2.4.1.208), are involved in maintaining (i) a certain anionic lipid surface charge density and (ii) constant nonbilayer/bilayer conditions (curvature packing stress), respectively. Cloning of the alDGS gene revealed related uncharacterized sequence analogs especially in several Gram-positive pathogens, thermophiles and archaea, where the encoded enzyme function of a potential Streptococcus pneumoniae DGS gene (cpoA) was verified. A strong stimulation of alDGS by phosphatidylglycerol (PG), cardiolipin, or nonbilayer-prone 1,3-DAG was observed, while only PG stimulated CpoA. Several secondary structure prediction and fold recognition methods were used together with SWISS-MODEL to build three-dimensional model structures for three MGS and two DGS lipid glycosyltransferases. Two Escherichia coli proteins with known structures were identified as the best templates, the membrane surface-associated two-domain glycosyltransferase MurG and the soluble GlcNAc epimerase. Differences in electrostatic surface potential between the different models and their individual domains suggest that electrostatic interactions play a role for the association to membranes. Further support for this was obtained when hybrids of the N- and C-domain, and full size alMGS with green fluorescent protein were localized to different regions of the E. coli inner membrane and cytoplasm in vivo. In conclusion, it is proposed that the varying abilities to bind, and sense lipid charge and curvature stress, are governed by typical differences in charge (pI values), amphiphilicity, and hydrophobicity for the N- and (catalytic) C-domains of these structurally similar membrane-associated enzymes.

* This work was supported by the Swedish Science Research Council.The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

The nucleotide sequence(s) reported in this paper has been submitted to the GenBankTM/EBI Data Bank with accession number(s) AY078412.

The on-line version of this article (availabe at http://www.jbc.org) contains supplemental text, supplemental Tables IV and V, and supplemental Refs. 1-8.

§ Both authors have contributed equally to this work.

Present address: Dept. of Microbiology, Colorado State University, Fort Collins, CO 80523-0015.

Dagger Dagger To whom correspondence should be addressed. Tel.: 46-8-16-24-63; Fax: 46-8-15-36-79; E-mail: ake@dbb.su.se.

Copyright © 2003 by The American Society for Biochemistry and Molecular Biology, Inc.
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