Prebiotically relevant mixed fatty acid vesicles support anionic solute encapsulation and photochemically catalyzed trans-membrane charge transport

Abstract

The spontaneous assembly of amphiphile-based compartments in aqueous solution is widely viewed as a key step in models for the abiotic formation of primitive cell-like structures. Proposed organic components for such systems consist of mixed short chain fatty acids (FA) and polycyclic aromatic hydrocarbon (PAH) species, the composition of which have been modeled after organic extracts of carbonaceous meteorites. Self-assembly of amphiphiles from these extracts into aqueous suspensions of bilayer structures was long ago demonstrated, although little has since been reported concerning the stability and potential functionality of these complex mixtures. This work explores the thermodynamic and kinetic stability of vesicles prepared from complex mixtures of short chain FA species (CH 3 COOH-C 9 H 19 COOH) with membrane solubilized PAH species. Critical vesicle concentration measurements and ultrafiltration analyses of decanoic acid in the presence of other shorter chain FA species indicate the formation of mixed component vesicle phases composed mainly of C 10 -C 8 FA components. An electrostatic barrier to trans-membrane diffusion of negative charges allows observation of stably encapsulated poly-anionic solutes inside these vesicles. As a model for primitive energy transduction, trans-membrane electron transfer between EDTA and encapsulated ferricyanide was demonstrated, driven catalytically via PAH photochemistry without substantial decomposition of the chromophores or vesicles. These results indicate a plausible role for compartmentalization and catalysis by short chain fatty acids and PAH species in prebiotic vesicle-encapsulated systems.

Photochemically driven redox chemistry induces protocell membrane pearling and division

“…PAHs are the most abundant polyatomic organic molecules in the universe, have been postulated to play important roles in the origin of life (16,17), and have been shown to stabilize short-chain fatty acid membranes (18). We therefore asked whether oxygenated derivatives of PAHs, such as 1-hydroxypyrene (while HPTS itself is also a hydroxypyrene derivative, it is unlikely to be prebiotically abundant), can be incorporated into vesicle membranes and act as photosensitizers that can absorb UV radiation, generate ROS, and facilitate the division of protocells.…”

“…Such hydrophobic molecules are likely to have been selectively solubilized and concentrated in primitive membranes. Indeed, hydroxypyrene, a simple oxygenated PAH, has been shown to integrate into and stabilize membranes composed of short chain fatty acids (18). In a high UV surface environment, membrane-localized PAHs would be expected to absorb UV radiation and generate ROS, even under anaerobic conditions (16).…”

Primitive Membrane Formation, Characteristics and Roles in the Emergent Properties of a Protocell

“…Here again, protocell membranes could play a crucial role, as their counterparts in cells do it, and the question of whether these simple structures (compared to cellular membranes) can maintain gradients during their build-up until the gradient amplitude is large enough to allow it to drive uphill reactions. It is possible to create a chemical gradient across a membrane using simple photosensitive membrane bound PAHs as shown with a simple chemical network [44]. In this system, a PAH, [2,3a]-naphthopyrene spontaneously associated with the fatty acid bilayers of vesicles which contained encapsulated ferricyanide, while EDTA was present in the external medium.…”

“…PAHs are used for straightforward activities such as staining bilayers for fluorescence microscopy (Nile Red, Texas Red). However, photoexcitation can also lead to more complex phenomena such as building up transbilayer pH- [42,43] or electron-gradients [44]. PAH are also useful in stabilizing bilayer structures to reduce the permeability of single chain amphiphiles [45].…”

Physico-chemical interactions between compartment-forming lipids and other prebiotically relevant biomolecules

“…A recent test of PAH as a transducer of electron transport was carried out by Cape et al [29] who used a simple photochemical trans-membrane charge transfer reaction in which Fe(CN) 6 -3 could be reduced to Fe(CN) 6 -4 inside decanoic acid vesicles while EDTA (ethylenediaminetetraacetic acid) was oxidized outside. They used naphtho [2,3a]-pyrene and perylene as PAH catalysts for the photochemical reaction.…”