The polar lipid composition in membranes of Acholeplasma laidlawii is extensively regulated as a response to environmental changes. In particular, the ratio between the dominating lipids monoglucosyldiglyceride and diglucosyldiglyceride is altered depending on temperature, configuration of incorporated fatty acids, and membrane cholesterol content. Synthesis of monoglucosyldiglyceride is stimulated by low temperature and saturated fatty acids but diminished by the presence of cholesterol. These factors are likely to affect the molecular geometry of the membrane lipids. Monoglucosyldiglyceride and diglucosyldiglyceride have wedge- and rodlike molecular shapes, respectively, that are modifiable to a certain extent. The packing constraints of lipids in amphilphilic aggregates, i.e., hydrocarbon-water interfacial area, hydrocarbon chain volume, and hydrocarbon chain length, are very important in determining the aggregate structure [Israelachvili, J. N. Mitchell, D. J., & Ninham, B. W. (1976) J. Chem. Soc., Faraday Trans. 272, 1525]. Pure monoglucosyldiglyceride forms a reversed hexagonal (HII) phase structure with different fatty acid contents, while diglucosyldiglyceride forms a lamellar phase. However, the only lipid structure compatible with a functional biological membrane is the lamellar phase. Consequently, the balance between lipids forming lamellar and other mesophase structures must keep within certain limits. Here we show that the response in A. liaidlawii lipid metabolism following external and internal stimuli can be predicted on the basis of molecular shapes and is necessary for the cell in order to maintain optimal membrane stability. Furthermore, the reduced capacity of Acholeplasma membranes to incorporate cholesterol is another consequence of this regulation, aiming at preservation of bilayer stability.

The packing of lipids into different aggregates, such as spheres, rods, or bilayers, is dependent on the hydrophobic volume, the hydrocarbon-water interfacial area, and the hydrocarbon chain length of the participating molecules, according to the self-assembly theory [Israelachvili, J. N., Marcelja, S., & Horn, R. G. (1980) Q. Rev. Biophys. 13, 121-200]. The origin of the participating molecules should be of no importance with respect to their abilities to affect the above-mentioned parameters. In this investigation, Acholeplasma laidlawii, with a defined acyl chain composition of the membrane lipids, has been grown in the presence of three different classes of foreign molecules, known to partition into model and biological membranes. This results in an extensive metabolic alteration in the lipid polar head group composition, which is expressed as changes in the molar ratio between the lipids monoglucosyldiglyceride (MGDG) and diglucosyldiglyceride (DGDG), forming reversed hexagonal and lamellar phases in excess water, respectively. The formation of nonlamellar phases by A. laidlawii lipids depends critically upon the MGDG concentration [Lindblom, G., Brentel, I., Sjölund, M., Wikander, G., & Wieslander, A. (1986) Biochemistry (preceding paper in this issue)]. The foreign molecules tested belong to the following groups: nonpolar organic solvents, alcohols, and detergents. Their effects on the gel to liquid crystalline phase transition temperature (Tm), on the order parameter of the acyl chains, and on the phase equilibria between lamellar and nonlamellar liquid crystalline phases in lipid-water model systems are known in several instances.(ABSTRACT TRUNCATED AT 250 WORDS)

Monoglucosyl diglyceride and diglucosyl diglyceride are the dominant lipids of the Acholeplasma laidlawii membrane. Diglucosyl diglyceride forms a lamellar liquid crystalline phase with water while monoglucosyl diglyceride forms a reversed hexagonal phase. Depending on the amounts of unsaturated acyl chains of the lipids, a mixture of monoglucosyl diglyceride and diglucosyl diglyceride forms lamellar or reversed cubic phases at physiological temperatures. A high degree of cis unsaturation favors formation of the cubic phase with increasing monoglucosyl diglyceride content. The structure of the cubic phase is composed of aggregates, where the lipids can diffuse over macroscopical distances. A structure containing close-packed spherical micelles is therefore ruled out, and the NMR diffusion data are compatible with other previously proposed cubic bicontinuous structures [Luzzati, V., & Spegt, P. A. (1967) Nature (London) 215, 701; Scriven, L. E. (1976) Nature (London) 263, 123; Lindblom, G., Larsson, K., Johansson, L. B.-A., Fontell, K., & Forsén, S. (1979) J. Am. Chem. Soc. 101, 5465]. Monoglucosyl diglyceride/diglucosyl diglyceride ratios forming cubic phases have not been observed in vivo. It is concluded that formation of the cubic phase is strongly dependent on the molecular shape of the lipids. The results are significant for the physiological regulation of the lipid composition in A. laidlawii membranes as well as for the function and organization of biological membranes in general.

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The two dominant glucolipids in Acholeplasma laidlawii, viz., 1,2-diacyl-3-O-(alpha-D-glucopyranosyl)-sn-glycerol (MGlcDG) and 1,2-diacyl-3-O-[alpha-D-glucopyranosyl-(1----2)-O-alpha-D-glucopyranosyl ]- sn-glycerol (DGlcDG), have markedly different phase behavior. MGlcDG has an ability to form nonlamellar phases, whereas DGlcDG only forms lamellar phases. For maintenance of a stable lipid bilayer, the polar headgroup composition in A. laidlawii is metabolically regulated in vivo, in response to changes in the growth conditions [Wieslander et al. (1980) Biochemistry 19, 3650; Lindblom et al. (1986) Biochemistry 25, 7502]. To investigate the mechanism behind the lipid regulation, we have here studied bilayers of mixtures of unsaturated MGlcDG and DGlcDG, containing a small fraction of biosynthetically incorporated perdeuterated palmitic acid, with 2H NMR. The order-parameter profile of the acyl chains and an apparent transverse spin relaxation rate (R2) were determined from dePaked quadrupole-echo spectra. The order of the acyl chains in DGlcDG-d31 increases upon addition of protonated MGlcDG, whereas the order of MGlcDG-d31 decreases when DGlcDG is added. The variation of order with lipid composition is rationalized from simple packing constraints. R2 increases linearly with the square of the order parameter (S2) up to S approximately 0.14; then, R2 goes through a maximum and decreases. The increase in R2 with S2, as well as the magnitude of R2, is largest for pure MGlcDG-d31, smallest for DGlcDG-d31, and similar for mixtures with the same molar ratio of MGlcDG/DGlcDG but with the deuterium label on different lipids.(ABSTRACT TRUNCATED AT 250 WORDS)