Structural Phenomena in a Vesicle Membrane Obtained through an Evolution Experiment: A Study Based on MD Simulations

Abstract

The chemical evolution of biomolecules was clearly affected by the overall extreme environmental conditions found on Early Earth. Periodic temperature changes inside the Earth's crust may have played a role in the emergence and survival of functional peptides embedded in vesicular compartments. In this study, all-atom molecular dynamic (MD) simulations were used to elucidate the effect of temperature on the properties of functionalized vesicle membranes. A plausible prebiotic system was selected, constituted by a model membrane bilayer from an equimolar mixture of long-chain fatty acids and fatty amines, and an octapeptide, KSPFPFAA, previously identified as an optimized functional peptide in an evolution experiment. This peptide tends to form the largest spontaneous aggregates at higher temperatures, thereby enhancing the pore-formation process and the eventual transfer of essential molecules in a prebiotic scenario. The analyses also suggest that peptide-amphiphile interactions affect the structural properties of the membrane, with a significant increase in the degree of interdigitation at the lowest temperatures under study.

Keywords: molecular dynamics; origin of life; peptide aggregation.

Figure 1

Effect of temperature on the peptide aggregation process. Left: side view of (ODAP—STEP) bilayer systems with peptides at 0 ns (a) and 500 ns at 353 K (b), 338 K (c), and 323 K (d); KSPFPFAA peptides are shown in mauve, while ODAP and STEP are in gray and green, respectively. Right: number of the clusters as a function of time formed during the 500 ns MD simulation with cutoff 0.6 nm at 353 K (e) (previously reported by the authors in Ref. [44]), 338 K (f), and 323 (g).

Figure 2

Lateral mean square displacements as a function of time for ODAP (a), STEP (b), and KSPFPFAA (c) in an ODAP–STEP–KSPFPFAA system at 353 K (green), 338 K (blue), and 323 (black), and in ODAP–STEP bilayers at 353 K (light green), 338 K (light blue), and 323 (grey).

Figure 3

Order parameters (S_CH) for ODAP at 353 K (a), 338 K (b) and 323 K (c), and STEP at 353 K (d), 338 K (e), and 323 K (f) in an ODAP–STEP bilayer (black lines) and in an ODAP–STEP bilayer containing KSPFPFAA (blue lines).

Figure 4

Time-dependent area per amphiphile pair A_AP (left) and membrane thickness h (right) of a pure ODAP–STEP bilayer (black lines) and an ODAP–STEP bilayer containing KSPFPFAA peptides (blue lines) at 353 K (a,d); 338 K (b,e); and 323 K (c,f).

Figure 5

The bilayer thickness profile of KSPFPFAA-containing ODAP–STEP bilayers at 353 K (a), 338 K (b), and 323 K (c). Red regions represent high thickness and blue regions represent low thickness.

Figure 6

Mean curvature, J, of ODAP–STEP bilayer (2, top leaflet; 4, bottom leaflet) and peptide-containing ODAP–STEP bilayers (1, top leaflet; 3, bottom leaflet) at 353 K (a), 338 K (b), an 323 K (c). Orange regions represent positive membrane curvatures and turquoise regions represent negative curvatures.

Figure 7

The 2D number density maps of ODAP–STEP bilayer (2, ODAP; 4, STEP) and peptide-containing ODAP–STEP bilayers (1, ODAP; 3, STEP) at 353 K (a), 338 K (b), and 323 K (c). Dark red regions represent low number densities and dark blue regions represent high number densities.

Figure 8

The 2D number density maps for water in peptide-containing ODAP–STEP bilayers at 353 K (a), 338 K (b), and 323 K (c). Dark red regions represent low number densities and dark blue regions represent high number densities.