Correlation between Thermal Death and Membrane Fluidity in Bacillus stearothermophilus

Abstract

Paramagnetic resonance spectra of spin labels partitioned into spheroplast membranes of Bacillus stearothermophilus indicate lateral lipid phase separations. Cells adjust their lipid composition in response to temperature changes so that the same change of state in membrane phospholipids is achieved at the respective growth temperature. A temperature-sensitive mutant that fails to change its lipid composition above a certain temperature can survive only up to the higher temperature boundary for lateral phase separation. These data are interpreted to indicate that the maximal and minimal growth temperatures of thermophiles are regulated by the onset and conclusion of phase separations of the particular lipid composition they synthesize.'It is suggested that isolated lipid domains are required for functional membrane assembly.Prokaryotic microorganisms have the remarkable ability to adapt to temperature extremes that are usually considered lethal for other forms of life. This so-called biokinetic temperature zone for microorganisms extends from -100 to nearly 100°(1, 2). The capacity of thermophilic organisms to grow at very high temperatures resides in their ability to synthesize cell components that have a greater heat stability than the corresponding components synthesized by mesophiles and psychrophiles. It is well documented (for review, see ref.3) that proteins from thermophiles are not readily heatdenatured. Likewise, Tm values, which characterize the melting behavior of DNA and RNA, are higher for thermophilic strains of a given genus (2,4). However, these observations do not give an indication about the mechanisms that lead to the creation of thermostable macromolecules. In addition, there is no ready explanation for the observed differences in maximal growth temperature (Tmax), optimal growth temperature (T0pt), and minimal growth temperature (Tmin) among different species.The idea that the maximal growth temperature any organism can achieve is determined by its membrane stability has also been entertained by many investigators. In early work, Heilbrunn (5) and BelehrAdek. (6) postulated that organisms adapt to changes in temperature by altering their plasma lipid composition and that heat resistance was, therefore, related to the melting temperature-of the lipids. At the time of their work, the presence of lipids in membranes was not yet known. More recently, Johnston and Roots (7) argued Abbreviations: 5-doxyl stearate, 4',4'-dimethyloxazolidine-Noxyl derivative of 5-keto stearate; TEMPO, 2,2,6,6-tetramethylpiperidine-1-oxyl; EPR, electron paramagnetic resonance. 4111that cells must maintain lipids near the critical point of phase transition in order to achieve an appropriate degree of expansibility and solid-liquid ratio. They argued further that varying the degree of fatty acid unsaturation could provide an effective way to preserve this particular state. Only in the past few years were these ideas incorporated into proposals for membrane structure in general (for review, see ref. 8).The impo...

Spin-label studies on rat liver and heart plasma membranes: Do probe-probe interactions interfere with the measurement of membrane properties?

“…[24], egg lecithin and dipalmitoyllecithin liposomes [-61, spheroplasts from Bacillus stearothermophilus [21], guinea pig ileum plasma membrane [65], lymphocytes and L cells [36]. Our experiments on rat liver membranes suggest that the probe partitions between the membrane lipid and the aqueous environment, in agreement with similar studies performed on erythrocytes [8] and model membrane liposomes [6].…”

“…However, S" is a function of both the polarity and fluidity of the membrane; changes in S" necessarily reflect fluidity alterations only in the limiting case where the polarity of the membrane is identical to that of the reference crystal. Thus, previous I(m, n) label studies which interpreted changes in S" (or Tll ) only in terms of a membrane fluidity change overlooked the possible involvement of polarity alterations [11,17,21,35,43,[57][58][59]66]. Nor can it be assumed that T H will be insensitive to probe-probe interactions in all membrane systems, since increases in TII with probe concentration were noted in a I(12,3)-labelled erythrocyte membrane study [73].…”

Microbial transport: Adaptations to natural environments

“…The membranes of the thermophilic bacteria T. maritima and B. stearothermophilus, however, have a much higher proton permeability than the other organisms at their growth temperatures. Squares indicate the proton permeability at the growth temperature fervidus (previously Clostridium fervidus) (Speelmans et al 1993a, b), an organism that can grow at a temperature of 70°C (Esser and Souza 1974;Patel et al 1987). C. fervidus has a Na + -translocating V-type ATPase that excretes sodium ions at the expense of ATP.…”

Evolutionary adaptation of membranes to temperature.

“…In Tetrahymena (3) and the synaptosomal membranes of the goldfish Carassius auratus (4), partial compensation is achieved after laboratory acclimation at different temperatures, but it is somewhat less than that required to maintain a constant "fluidity" at all environmental temperatures; partial compensation may be associated with the eurythermal properties of these animals. Bacterial membranes show a complete compensation (2,5).…”