Alkanes increase the stability of early life membrane models under extreme pressure and temperature conditions

Abstract

Terrestrial life appeared on our planet within a time window of [4.4-3.5] billion years ago. During that time, it is suggested that the first proto-cellular forms developed in the surrounding of deep-sea hydrothermal vents, oceanic crust fractures that are still present nowadays. However, these environments are characterized by extreme temperature and pressure conditions that question the early membrane compartment's capability to endure a stable structural state. Recent studies proposed an adaptive strategy employed by present-day extremophiles: the use of apolar molecules as structural membrane components in order to tune the bilayer dynamic response when needed. Here we extend this hypothesis on early life protomembrane models, using linear and branched alkanes as apolar stabilizing molecules of prebiotic relevance. The structural ordering and chain dynamics of these systems have been investigated as a function of temperature and pressure. We found that both types of alkanes studied, even the simplest linear ones, impact highly the multilamellar vesicle ordering and chain dynamics. Our data show that alkane-enriched membranes have a lower multilamellar vesicle swelling induced by the temperature increase and are significantly less affected by pressure variation as compared to alkane-free samples, suggesting a possible survival strategy for the first living forms.

Fig. 1. Protomembrane models.

Sketch of the three protomembrane models investigated in this study. a C10 mix; b C10 mix + 2% eicosane; and c C10 mix + 2% squalane. d Molecular structure and name of each compound used.

Fig. 2. Example of SAXS curves.

SAXS curves obtained for the sample C10 mix + 2% squalane at p = 1 bar. The errors are calculated by propagating the errors of the 30 averaged frames (which come from Poisson distribution). Most of the error bars are smaller than the symbol size. All curves were vertically shifted for clarity.

Fig. 3. d-spacing vs p–T.

MLV d-spacing of the three measured samples at all T–p points where a lamellar correlation was fitted. a C10 mix; b C10 mix + 2% h-eicosane; and c C10 mix + 2% h-squalane. The errors are calculated by propagation of the fit parameter errors, as detailed in the main text.

Fig. 4. Atomic mean square displacements.

MSD for the two samples studied: C10 mix (empty symbols) and C10 mix with d-eicosane (full symbols). All lines are linear fits to the data. Note the clear dependence on temperature and pressure for the sample missing the eicosane, while all MSD values vary little at all T–p when the eicosane is added. The errors are calculated by propagation from I_sum, as detailed in the main text. Inset: vertical zoom of the C10 mix + 2% d-eicosane data.

Fig. 5. Pseudo-force constants.

Histogram comparing the derivative of the MSD data vs temperature assuming a simple linear model. Note that the value of C10 mix at p = 10 bar is a likely underestimation. Each value is shown with its error from the linear fit.

Fig. 6. Sample lamellarity at ambient temperature.

SANS curves obtained for the three samples at 80 mM concentration and T = 21 °C. The arrows indicate the position of the first two orders of the MLV correlation for the three samples. The curves of eicosane- and squalane-enriched samples were shifted vertically for clarity.

Fig. 7. Fitting the SAXS data.

Example of SAXS data fitting using Gaussian functions with a q^−c background. The curves show the SAXS signal from the sample C10 mix + 2% eicosane, T = 20 °C and p = 10, 400, 700, 1000 bar respectively. Arrows show the two first correlation orders, proving the membrane lamellar ordering (together with the data shown in Fig. 6). The white lines are fits to the data. Inset: zoom in the mid-wide q-range. All related fitting parameters, errors and resulting χ² can be found in the Supplementary Information (Supplementary Table 1, see also Supplementary Note 2 and Supplementary Fig. 5).

Fig. 8. Elastic intensity decay and GA validity range.

Example of intensity curves obtained from the EINS experiment and range of validity of the GA (shown as a linear behaviour in this representation). The data shown are the ones of C10 mix and C10 mix + 2% eicosane at p = 10 bar and T = 84 and 24 °C, respectively. The light green region highlights the q² data range used for the analysis. The q² > 2 Å⁻² data for the C10 mix at T = 84 °C approach zero and are not visible in the log(I_inc) representation. The errors are obtained from Poisson distribution.