Membrane Properties of Archæal Macrocyclic Diether Phospholipids

Abstract

Several biophysical properties of four synthetic archaeal phospholipids [one polyprenyl macrocyclic lipid A and three polyprenyl double-chain lipids (B, C, D) bearing zero, one or four double bonds in each chain] were studied using differential scanning calorimetry, electron and optical microscopies, stopped-flow/light scattering and solid-state 2H-NMR techniques. These phospholipids gave a variety of self-organized structures in water, in particular vesicles and tubules. These assemblies change in response to simple thermal convection. Some specific membrane properties of these archaeal phospholipids were observed: They are in a liquid-crystalline state over a wide temperature range; the dynamics of their polyprenyl chains is higher than that of n-acyl chains; the water permeability of the membranes is lower than that of n-acyl phospholipid membranes. It was also found that macrocyclization remarkably improves the barrier properties to water and the membrane stability. This may be related to the adaptation of Methanococcus jannaschii to the extreme conditions of the deep-sea hydrothermal vents.

Microbial diversity and adaptation to high hydrostatic pressure in deep-sea hydrothermal vents prokaryotes

“…Part of the adaptation of the archaeal membrane to extreme environments may originate from the original structure of its lipids. While membranes made of fatty acyl ester lipids are in the gel phase or in the liquid crystalline phase depending mostly on their fatty acid composition, archaeol-and caldarchaeol-based polar lipid membranes of Archaea are assumed to be in the liquid crystalline phase at a wide temperature range of 0-100 °C (Stewart et al 1990;Dannenmuller et al 2000). In addition, most if not all Archaea from the hydrothermal environments synthesize membrane-spanning bipolar tetraether lipids that form monolayers.…”

“…(3) The crosslinking of the two acyl-chains of the lipids to yield macrocyclic archaeol or caldarchaeol derivatives by a covalent bond between the isoprenoid chains reduces the motion of the molecule creating a more closely-packed structure and increasing the membrane stability, creating an efficient barrier against water, proton and solute leakage (Dannenmuller et al 2000;Mathai et al 2001). (4) The increase in unsaturation along the isoprenoid chains of the lipids as a function of temperature (Nichols et al 2004) or salinity (Dawson et al 2012) has to date only been described in the psychrophilic methanogen Methanococcoides burtonii (Franzmann et al 1992;Nichols et al 2004), but unsaturated lipids have been characterized in several species of hyperthermophiles (Hafenbradl et al 1993;Gonthier et al 2001), which might indicate the occurrence of a similar adaptive strategy in hydrothermal vent organisms.…”

A molecular dynamics study of an archaeal tetraether lipid membrane: Comparison with a dipalmitoylphosphatidylcholine lipid bilayer

“…The absence in the total density profile of a dip in the membrane midplane is characteristic of a monolayer made of lipids with spanning aliphatic chains. A membrane made up of a macrocyclic ether lipid (34) would likely have a total density profile with a small dip in its hydrophobic core. However, since no free chain ends would be present in a pure membrane made of macrocyclic lipids, the predicted dip should be smaller compared with the one from PC membranes.…”

“…MPL differs from the more classical DPPC phospholipid by the spanning geometry of the lipid within the membrane, and by the presence of methyl groups or cyclopentane rings on the aliphatic backbones, plus a few other structural features such as the ether linkage. Despite their structural discrepancies, the order parameter of DPPC lipid embedded in a membrane is similar to those of monopolar diether lipids and the cyclized macro-cyclic analogs assembled in a bilayer (34). Consequently, the study of a tetraether lipid monolayer should lead to conclusions directly related to the peculiar monolayer organization.…”

Toward Understanding Protocell Mechanosensation

“…Indeed, tetrahymanol, carotenoles, sulfates of ω,ω′-trihydroxylated β-carotene ketones, bacterioruberins, tricyclohexaprenol, and squalene from some archaebacteria also have Chol-like reinforcing effects on artificial phospholipid membranes (Ourisson and Nakatani 1994). These kinds of lipids form membranes that are more stable than those made from ordinary lipids and do not appear to need further reinforcement (Dannenmuller et al 2000). Overall, the nonrandom distribution of some lipids as microdomains may involve remarkable changes in the structural and dynamic properties of protocell membranes, in addition to having very important consequences for membrane protein function (Lindner and Naim 2009).…”