Control of Membrane Lipid Fluidity by Molecular Thermosensors

Abstract

Bacteria can encounter a wide range of environments and must adapt to new conditions in order to survive. As the se- lective barrier between living cells and their environment, the plasma membrane plays a key role in cell viability. The barrier function of the cytoplasmic membrane is known to depend critically on the physical state of lipid bilayers (17), making it susceptible to changes in environmental temperature. In fact, it has been established that normal cell function requires mem- brane lipid bilayers that are largely fluid; indeed, the bilayers of most organisms are entirely or mostly fluid at physiological temperatures. However, at lower temperatures, membrane lipid bilayers undergo a reversible change of state from a fluid (disordered) to a nonfluid (ordered) array of the fatty acyl chains (21, 56). The temperature at the midpoint of this tran- sition is called the transition temperature, and the change of state accompanying an increase in temperature is called the lipid phase transition, the gel-liquid crystalline transition, or most properly, the order-disorder transition. The transition temperature is a function of the membrane lipid composition and, in organisms deficient in cholesterol, mainly depends on the fatty acid composition of the membrane lipids (21, 56). The (overly simplified) rule of thumb is that phospholipids that contain unsaturated fatty acids (UFAs) have much lower tran- sition temperatures than those lipids made of saturated fatty acids (SFAs). The effect is due to different packing of the two types of phospholipid acyl chains. SFA acyl chains can pack tightly, but the steric hindrance imparted by the rigid kink of the cis double bond results in much poorer chain packing of UFAs, even below the phase transition temperature (16, 17). From these considerations, it seems clear that bacteria and most (if not all) poikilothermic organisms must regulate their phase transition in response to temperature. Without regula- tion, an organism shifted from a high to a low temperature would have membrane lipids with suboptimal fluidity, result- ing in subnormal membrane function. The mechanism of reg- ulation in all of the cases examined seems to occur via the incorporation of proportionally more UFAs (or fatty acids of analogous properties) as the temperature decreases. This reg- ulatory mechanism system, called thermal control of fatty acid synthesis, seems to be a universally conserved adaptation re- sponse allowing cells to maintain the appropriate fluidity of membrane lipids regardless of the ambient temperature. This means that cells must process temperature signals to adjust enzyme activities or to activate unique genes necessary to adapt the membranes to the new temperature. The question arises, how do cells sense a change in temperature and adjust the fluidity of the membrane lipid bilayer accordingly? Here, we discuss the basic features of thermal regulation of membrane lipid fluidity in Escherichia coli and Bacillus subtilis, in which the proposed mechanisms are firmly based on both genetic and biochemical evidence. Although the physiological consequences of this regulation are the same in both organ- isms, the mechanisms involved are entirely different.