Abstract
It has been proposed that adaptation to high temperature involved the synthesis of monolayer-forming ether phospholipids. Recently, a novel membrane architecture was proposed to explain the membrane stability in polyextremophiles unable to synthesize such lipids, in which apolar polyisoprenoids populate the bilayer midplane and modify its physico-chemistry, extending its stability domain. Here, we have studied the effect of the apolar polyisoprenoid squalane on a model membrane analogue using neutron diffraction, SAXS and fluorescence spectroscopy. We show that squalane resides inside the bilayer midplane, extends its stability domain, reduces its permeability to protons but increases that of water, and induces a negative curvature in the membrane, allowing the transition to novel non-lamellar phases. This membrane architecture can be transposed to early membranes and could help explain their emergence and temperature tolerance if life originated near hydrothermal vents. Transposed to the archaeal bilayer, this membrane architecture could explain the tolerance to high temperature in hyperthermophiles which grow at temperatures over 100 °C while having a membrane bilayer. The induction of a negative curvature to the membrane could also facilitate crucial cell functions that require high bending membranes.
Highlights
It has been proposed that adaptation to high temperature involved the synthesis of monolayer-forming ether phospholipids
Regardless of the environmental constraint, Archaea are usually found to be adapted to the most extreme values of these parameters. This ability has been linked to their specific membrane lipids, which differ from those found in Eukarya and Bacteria: they are isoprenoid hydrocarbon chains linked by ether bonds to sn-glycerol-1-phosphates (Fig. 1a)[4,5]
In archaeal bilayer, the insertion is proposed to extend the stability domain and enhance the functionality of the membrane[21,22]. This hypothesis has numerous implications: amongst them, it would provide evidence for a novel putative adaptation route of the membrane to high temperature in Archaea, which could be applicable to Archaea ancestors predating the invention of bipolar lipids and which would be congruent with a possible origin of life in deep sea hydrothermal vent systems[25,26]
Summary
It has been proposed that adaptation to high temperature involved the synthesis of monolayer-forming ether phospholipids. We used small-angle X-ray scattering (SAXS) to explore the possibility of squalane-induced phase transitions by determining the structure of fully hydrated synthetic archaeal-like lipids (DoPhPC:DoPhPE (9:1)) and the impact of 1 mol% squalane on their self-assembled structure as a function of temperature (10 to 85 °C, 15 °C steps) and hydrostatic pressure (1 to 1000 bar, 50 bar steps).
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