Isoprenoids enhance the stability of fatty acid membranes at the emergence of life potentially leading to an early lipid divide

Abstract

Two key problems concern cell membranes during the emergence and early evolution of life: what was their initial composition, and why did the membranes of archaea and bacteria diverge? The composition of the first cell membranes could shed light on the most likely environment for the emergence of life. The opposing stereochemistry of modern lipid glycerol-phosphate headgroups in bacteria and archaea suggests that early membranes were composed of single chain amphiphiles, perhaps both fatty acids and isoprenoids. We investigated the effect of adding isoprenoids to fatty acid membranes using a combination of UV–visible spectroscopy, confocal microscopy and transmission electron microscopy. We tested the stability of these membranes across a pH range and under different concentrations of ionic species relevant to oceanic hydrothermal environments, including Na 2+ , Cl − , Mg 2+ , Ca 2+ , HC O 3 − , Fe 3+ , Fe 2+ and S 2− . We also tested the assembly of vesicles in the presence of Fe particles and FeS precipitates. We found that isoprenoids enhance the stability of membranes in the presence of salts but require 30-fold higher concentrations for membrane formation. Intriguingly, isoprenoids strongly inhibit the tendency of vesicles to aggregate together in the presence of either Fe particles or FeS precipitates. These striking physical differences in the stability and aggregation of protocells may have shaped the divergence of bacteria and archaea in early hydrothermal environments.

Spontaneous assembly of redox-active iron-sulfur clusters at low concentrations of cysteine

“…The concentration-dependence of [4Fe4S] cluster assembly on cysteine concentration and its tight correlation with the signature absorbance shoulder at 420 nm, suggests that other types of cluster were indeed masked by the presence of [4Fe4S] clusters. We therefore used room temperature 57 Fe Mössbauer spectroscopy to determine the proportions of individual species present 34 . The samples were prepared by lyophilization (see the 'Methods' section) as our initial preparations of N 2 -dried samples did not produce normal UV-Vis traces when reconstituted (unlike our lyophilized samples).…”

“…11). Attempts to characterise these samples further using 57 Fe Mössbauer spectroscopy were hindered by the fragility of the samples during sample preparation. After lyophilisation, samples were brittle with a floss-like structure making it impossible to transfer to Mössbauer sample holders.…”

Possible mechanisms of CO 2 reduction by H 2 via prebiotic vectorial electrochemistry

“…If that were the case, then the topology of protocells would be correct (figure 2 d ). We have previously shown that vesicles formed from single-chain amphiphiles such as fatty acids and fatty alcohols are stable at pH 11 and above [92,93], so the scheme depicted in figure 2 d is feasible. The major question that we explore now is whether suitably steep H + gradients could develop across inorganic barriers containing disordered Fe(Ni)S minerals, which could ultimately promote the reduction of CO 2 by H 2 .…”

The Emergence of Life

“…Nevertheless, it is worth noting that most of these studies have commonly used one type of amphiphilic molecule in order to assemble such vesicles. For instance, recent work shows that using mixtures of amphiphiles of differing tail lengths (Jordan et al 2019b), or the addition of other types of amphiphiles such as isoprenoids (Jordan et al 2019a)-a more realistic simulation of the 'dirty chemistry' world of prebiotic chemistry-can yield vesicles which are significantly more resistant to higher salinity and pH values. In any case, such land-water interface sites which are characterized by fluctuating fresh water hydrothermal pools could also support other reactions.…”