Effect of independent variations in fatty acid structure and chain length on lipid polar headgroup composition in Acholeplasma laidlawii B membranes: regulation of lamellar/nonlamellar phase propensity.

Abstract

We have studied the biosynthetic regulation of the membrane lipid polar headgroup distribution in Acholeplasma laidlawii B cells made fatty acid auxotrophic by growth in the presence of the biotin-binding agent avidin to test whether this organism has the ability to coherently regulate the lamellar/nonlamellar phase propensity of its membrane lipids. The addition of various single normal growth-supporting exogenous fatty acids to such cell cultures produces fatty acid-homogeneous cells in which the hydrocarbon chain length and structure of the fatty acyl chains of the membrane lipids can be independently varied. Moreover, in analyzing our results, we consider the fact that the individual membrane lipid classes of this organism can form either normal micellar, lamellar, or reversed cubic or hexagonal phases in isolation (Lewis, R. N. A. H., and McElhaney, R. N. (1995) Biochemistry 34, 13818-13824). When A. laidlawii cells are highly enriched in one of a homologous series of methyl isobranched, methyl anteisobranched, or omega-cyclohexyl fatty acids, neither the ratio of normal micellar/lamellar nor of inverted cubic or hexagonal/lamellar phase-forming lipids are coherently regulated, and in fact in the former case, the changes in lipid polar headgroup composition observed are generally in a direction opposite to that required to maintain the overall lamellar/nonlamellar phase preference of the total membrane lipids constant when hydrocarbon chain length is varied. Similarly, when lipid hydrocarbon structure is varied at a constant effective chain length, a similar lack of coherent regulation of membrane lipid polar headgroup distribution is also observed, although in this case a weak overall trend in the expected direction occurs. We also confirm our previous finding (Foht, P. J., Tran, Q. M., Lewis, R. N. A. H., and McElhaney, R. N. (1995) Biochemistry 34, 13811-13817) that the ratio of inverted phase-forming monoglucosyl diacylglycerol to the lamellar phase-forming glycolipid diglucosyl diacylglycerol, previously used to estimate membrane lipid phase preference in A. laidlawii A and B, is not by itself a reliable indicator of the overall lamellar/nonlamellar phase propensity of the total membrane lipids of these organisms. Our results indicate that A. laidlawii B lacks a coherent mechanism to biosynthetically regulate the polar headgroup distribution of its membrane lipids to maintain the micellar/lamellar/inverted phase propensity constant in the face of induced variations in either the chain length or the structure of its lipid hydrocarbon chains. Finally, we suggest that the lack of a coherent regulatory mechanism to regulate the overall phase-forming propensity of the total membrane lipids of this organism under these circumstances may result in part from its inability to optimize all of the biologically relevant physical properties of its membrane lipid bilayer simultaneously.