Plausible Sources of Membrane-Forming Fatty Acids on the Early Earth: A Review of the Literature and an Estimation of Amounts

Abstract

The first cells were plausibly bounded by membranes assembled from fatty acids with at least 8 carbons. Although the presence of fatty acids on the early Earth is widely assumed within the astrobiology community, there is no consensus regarding their origin and abundance. In this Review, we highlight three possible sources of fatty acids: (1) delivery by carbonaceous meteorites, (2) synthesis on metals delivered by impactors, and (3) electrochemical synthesis by spark discharges. We also discuss fatty acid synthesis by UV or particle irradiation, gas-phase ion-molecule reactions, and aqueous redox reactions. We compare estimates for the total mass of fatty acids supplied to Earth by each source during the Hadean eon after an extremely massive asteroid impact that would have reset Earth's fatty acid inventory. We find that synthesis on iron-rich surfaces derived from the massive impactor in contact with an impact-generated reducing atmosphere could have contributed ∼10² times more total mass of fatty acids than subsequent delivery by either carbonaceous meteorites or electrochemical synthesis. Additionally, we estimate that a single carbonaceous meteorite would not deliver a high enough concentration of fatty acids (∼15 mM for decanoic acid) into an existing body of water on the Earth's surface to spontaneously form membranes unless the fatty acids were further concentrated by another mechanism, such as subsequent evaporation of the water. Our estimates rely heavily on various assumptions, leading to significant uncertainties; nevertheless, these estimates provide rough order-of-magnitude comparisons of various sources of fatty acids on the early Earth. We also suggest specific experiments to improve future estimates. Our calculations support the view that fatty acids would have been available on the early Earth. Further investigation is needed to assess the mechanisms by which fatty acids could have been concentrated sufficiently to assemble into membranes during the origin of life.

Figure 1

Fatty acid assembly depends on the pH of the surrounding solution. When the pH is below the effective pK_a of the fatty acids in a bilayer, fatty acids form an oil that is immiscible with the surrounding aqueous solution (bottom). When the pH is near the effective pK_a, fatty acids assemble into bilayers in a membrane (middle). Vesicles, spherical shells of these membranes, may have served as the membrane compartments for the first cells on Earth. When the pH is above the pK_a of the fatty acids in a bilayer, the fatty acids assemble into micelles, which cannot encapsulate aqueous solutes (top).

Figure 2

There are three well-characterized sources that could have provided fatty acids to the early Earth. (A) Carbonaceous meteorites can deliver fatty acids.⁻ (B) Metal surfaces can catalyze fatty acid synthesis. As one example, Nooner and Oro mixed filings of the Canyon Diablo meteorite (containing iron and nickel) with deuterium and carbon monoxide gases, and the mixture was heated to 400 °C to produce fatty acids. Similar experiments have used pure Fe, Ni, or Fe- and Ni-containing minerals as catalysts and a variety of carbon and hydrogen sources to synthesize fatty acids (Table 1). (C) Fatty acids can also be synthesized during electrical sparking (Table 2). As one example, Yuen et al. used an electric discharge to synthesize fatty acids from methane.

Figure 3

A single fragment of a carbonaceous meteorite cannot directly deliver enough decanoic acid to a body of water to form membranes. To exceed the critical vesicle concentration (∼15 mM), the volume of the meteorite (red line) would exceed the volume of the water. However, subsequent evaporation of the water could concentrate decanoic acid and enable membrane formation. A CM2 type meteorite is assumed because it contains the most decanoic acid on average (20 ppm by mass). The density of CM-type meteorites is 2100 kg/m³. Only meteorites with radii less than 100 m (∼10⁶ m³ for a spherical meteorite) can fragment and impact the Earth’s surface with low enough energy to preserve fatty acids.^, See eq 1 for details of the calculation.

Figure 4

Fatty acid synthesis occurs at the interfaces between reducing metal surfaces and a gaseous headspace. (A) Nooner and Oro showed that deuterium and carbon monoxide gases react together on the surface of hot (400 °C) meteorite filings to produce membrane-forming fatty acids.^, When the meteorite filings were artificially oxidized, fatty acid synthesis was not observed. (B) In hydrothermal experiments, McCollum et al. report that the synthesis of membrane-forming fatty acids occurs within gaseous bubbles adsorbed onto oxidation-resistant stainless steel surfaces. When oxidized metal surfaces are present instead of stainless steel, only short-chain (<5 carbons) fatty acids are formed.^,− In these hydrothermal experiments, aqueous formic acid or oxalic acid is used for experimental convenience as a source of H₂ and CO₂.

Figure 5

Length of fatty acids delivered by meteorites (labeled “Meteor.”) or produced in abiotic synthesis experiments. Fatty acids with at least eight carbons, indicated by the dashed red line, can assemble into membranes. All the fatty acids produced are saturated and unbranched (except in Scheidler et al. 2016, where experiments also produced unsaturated fatty acids). Note that detection of a fatty acid with a certain length may not have been attempted during every experiment.

Figure 6

Alternative reaction types that have demonstrated fatty acid synthesis. (A) Groth and Weyssenhoff used UV photochemistry to convert ethane into fatty acids. (B) Kaiser et al. irradiated an ultracold (10 K) mixture of ∼99% CH₄ and ∼1% O₂ with 9 MeV alpha particles to produce fatty acids. (C) Blagojevic et al. report reactions between gas-phase ions (CH₂⁺ and C₂H₄⁺) and CO to produce fatty acids. (D) Novotný et al. report the decomposition of monosaccharides into fatty acids under mild alkaline conditions (50 mM NaOH).