The third conceptualization of thermophilic/heat-tolerant lipids is based on a rather different point of view. Because lipids do not function as single molecules but as a membrane, that is, as an enormous number of molecules acting together, which assemble into a biologically functioning organelle, thermophilic lipids should be understood as lipids that normally function as a membrane at a high temperature. This is not achieved by chemical stability alone. At the moment that a lipid membrane came to enclose the cell contents, the real cell as we know it was born. With that event, cell membranes partitioned the inner cytoplasmic compartment away from their surroundings. From this time onward, membranes effectively functioned as a permeability barrier, controlling the in-flow and out-flow of low-molecular-weight compounds. This is the most primitive and essential function of a cell membrane. When cells became enclosed by such a membrane having this sort of permeability barrier, the cells achieved a distinct “individuality” and hence began to compete with the other individual cells in order to survive within the local community, and thus natural selection came more sharply into play. Therefore, the lipid constituents that enable the membrane to function as a highly permeable barrier at high temperatures are designated thermophilic lipids.
Another essential general feature that is required for lipid membrane function is the capacity to persist in the liquid crystalline phase. The phase-transition temperature of the archaeal lipid membranes is far lower than that of fatty acyl ester lipids, reportedly being between –20 and –15°C [26
]. The phase transition temperature of the normal fatty acyl ester phospholipid membrane is in a far higher temperature range (40–50°C) than the archaeal lipids, and this is dependent on their chain length, number of double bonds and the methyl branching position. Therefore, the archaeal polar lipid membrane can be presumed to be in liquid crystalline phase in the temperature range of 0 to 100°C, the range at which most archaea grow (biological temperature), while fatty acyl diester lipid membrane is in either a gel phase or liquid crystalline phase in the same temperature range, depending on their fatty acid composition.
In some archaea, the hydrocarbon chain properties are regulated by the number of cyclopentane rings (, Sulfolobus solfataricus
] or the ratio of caldarchaeol/cyclic archaeol/archaeol (Methanocaldococcus jannaschii
]. The content of the transunsaturation of the isoprenoid chains was reported to decrease with a higher growth temperature in Methanococcoides burtonii
]. However, the organism Methanopyrus kandleri
has a sufficient number of double bonds in the isoprenoid chains in spite of its much higher growth temperature. Unsaturation is not related in a straightforward manner with the adaptation to low temperatures, which occurred in archaea.
One characteristic property of the archaeal lipid membrane is the extremely low permeability of solutes [29
]. In addition, the permeability increases only slightly as the temperature goes up in the 0 to 100°C range.
In contrast to the tetraether lipid liposomes, the fatty acyl ester lipid liposomes exhibit a low permeability at a low temperature, but the permeability drastically increases as the temperature increases [29
]. The experimental results suggest that highly branched isoprenoid chains are a major cause of the low permeability of liposomes, but this phenomenon does not depend on the ether or ester bonds between the glycerophosphate backbone and hydrocarbon chains.
Bacteria grow at a temperature just above the phase-transition temperature at which membrane lipids are in a liquid crystalline state and retain a minimal level of permeability. The permeability of fatty acyl ester lipid membranes is highly temperature dependent and their phase-transition temperature is dependent on the fatty acid composition, so when the growth temperature shifts, the fatty acid composition of membrane lipids is quickly regulated. The phenomena described in Section 3
(regulation of the composition of unsaturated/saturated fatty acids (Figures and ) in E
, and iso/anteiso fatty acids in Bacillus
spp.) are explained by this mechanism. On the other hand, the isoprenoid ether lipids in the archaeal membrane are in a low permeability liquid crystalline state throughout the possible growth temperature range (0–100°C) [33
], and even if the growth temperature changes, the two requirements are met without any need of a biological regulation mechanism.
Because isoprenoid ether lipid membranes are in the liquid crystalline phase and have a low permeability at biological temperatures, archaea are found living at temperatures as low as 1°C and as high as 100°C with the same archaeol and caldarchaeol lipid composition in the membrane. This is the most fundamental characteristic of the archaeal lipid membranes. Bacterial membranes can be characterized by the highly developed regulatory mechanisms they employ to meet the two conditions. We can see actual examples in the case of the hyperthermophilic Pyrococcus furiosus
(optimum temperature, 98°C) [34
], moderately thermophilic Methanothermobacter thermautotrophicus
], mesophilic Methanobacterium formicicum
] and Methanogenium cariaci
]. They all have nearly the same core lipid composition. Unsaturated archaeol (geranylgeranyl group-containing archaeol) is present in the psychrophilic Methanococcoides burtonii
that can grow at 2°C [28
] as well as the hyperthermophilic Methanopyrus kandleri
]. A lipid that can be utilized at both high and low temperatures because of its liquid crystalline phase and low permeability at a wide range of temperatures is aptly termed a “heat tolerant” lipid.
On the other hand, bacterial fatty acyl ester lipid membranes should only function at the lowest temperature at which both a liquid crystalline state and low permeability are retained. This condition may be met at a temperature close to and above its phase transition temperature. Therefore, many bacteria with ester lipids control their fatty acid composition so as to meet these conditions. The control mechanism varies from species to species. In Escherichia coli
, unsaturated fatty acids are maximal at lower growth temperatures. However, unsaturation is not the only mechanism to adapt to lower temperatures. In Bacillus
spp., temperature adaptation is regulated by changing the iso/anteiso fattyacid composition [22
The archaeal lipid membrane does not have to regulate its hydrocarbon composition to meet the two conditions for temperature adaptation, because the two conditions are already in place at such a wide range of temperatures.