Elasticity and phase behaviour of biomimetic membrane systems containing tetraether archaeal lipids

Abstract

Archaeal single-cell microorganisms are characterised by particularly strong resistance to harsh environments at extreme temperature ranges, pH values, high pressure and salinity. The recognition of molecules rendering the archaeal membranes stable in such conditions represents an important step towards understanding the molecular mechanisms, which underlie the cellular survival, in order to effectively exploit them in biomedicine and bionanotechnology. Here we report on the bending elasticity and phase behaviour of model lipid membranes containing tetraether archaeal lipids. The bending elasticity modulus of membranes composed of palmitoyl-oleoyl phosphatidylcholine and glycerol dialkyl glycerol tetraether extract from the archaeon Thermoplasma acidophilum’s plasma membrane is measured by analysis of the thermal shape fluctuations of nearly spherical giant unilamellar vesicles (tens of micrometers in size). The bending rigidity is reported to non-monotonically depend on the archaeal lipids’ concentration in the bilayer. At 50 wt% of tetraether lipids in the membrane we measure around 20% decrease of the bending modulus compared to the studied single-component phosphocholine bilayer. The membrane resistance to bending increases at archaeal lipids’ content higher than 70 wt%. These findings support the hypothesis about a probable looping conformation at very low amounts of bipolar lipids in the membrane and prevailing spanning tetraether molecules at higher concentrations. Fluorescence microscopy reveals structural phase coexistence at low temperatures (6 °C) for 75 wt% of bolalipids in the bilayer. Laurdan spectroscopy measurements of large unilamellar vesicles (hundreds of nanometers in size) provide evidences for increased lipid ordering at the glycerol level induced by the presence of up to 90 wt% of bolalipid in the bilayer. At this archaeal lipid content we measure increased bending rigidity of the membrane. The fatty acyl chain mobility probed by DPH fluorescence spectroscopy is significantly reduced in the presence of bolalipids. The lipid ordering decreases with increasing the temperature to an extent depending on the bolalipid content in the membrane. The presence of bipolar lipids in the bilayer affects the lipid packing more strongly at the glycerol level compared to the hydrophobic core of the membrane. By elucidating the effect of tetraether lipids on the structural and mechanical properties of the bilayer, the reported results are expected to help in advancing on liposome-based pharmaceuticals and biomedical applications as well as for developments in sensorics and nanotechnology.