Redox and pH gradients drive amino acid synthesis in iron oxyhydroxide mineral systems

Abstract

Iron oxyhydroxide minerals, known to be chemically reactive and significant for elemental cycling, are thought to have been abundant in early-Earth seawater, sediments, and hydrothermal systems. In the anoxic Fe²⁺-rich early oceans, these minerals would have been only partially oxidized and thus redox-active, perhaps able to promote prebiotic chemical reactions. We show that pyruvate, a simple organic molecule that can form in hydrothermal systems, can undergo reductive amination in the presence of mixed-valence iron oxyhydroxides to form the amino acid alanine, as well as the reduced product lactate. Furthermore, geochemical gradients of pH, redox, and temperature in iron oxyhydroxide systems affect product selectivity. The maximum yield of alanine was observed when the iron oxyhydroxide mineral contained 1:1 Fe(II):Fe(III), under alkaline conditions, and at moderately warm temperatures. These represent conditions that may be found, for example, in iron-containing sediments near an alkaline hydrothermal vent system. The partially oxidized state of the precipitate was significant in promoting amino acid formation: Purely ferrous hydroxides did not drive reductive amination but instead promoted pyruvate reduction to lactate, and ferric hydroxides did not result in any reaction. Prebiotic chemistry driven by redox-active iron hydroxide minerals on the early Earth would therefore be strongly affected by geochemical gradients of E_h, pH, and temperature, and liquid-phase products would be able to diffuse to other conditions within the sediment column to participate in further reactions.

Keywords: early Earth; gradients; hydrothermal vents; iron hydroxides; life emergence.

Fig. 1.

Iron hydroxide precipitates simulating seafloor sediment and hydrothermal chimneys. (A) Vial of freshly precipitated iron hydroxides [Fe(II):Fe(III) = 2:1] reacting with pyruvate and ammonia after 72 h. (B) Simulated hydrothermal chimney precipitated from a hydrothermal fluid simulant (containing pyruvate and NaOH) into an early-Earth ocean simulant containing Fe [Fe(II):Fe(III) = 2:1] and ammonia; photo taken after 4 h.

Fig. 2.

Reductive amination of pyruvate to alanine and/or reduction of pyruvate to lactate in the presence of iron hydroxides. The relative yields of each product depended on the pH and Fe(II):Fe(III) ratio in the iron hydroxide precipitate.

Fig. 3.

Pyruvate reactions in the presence of ammonia and freshly precipitated iron hydroxides as a function of time. Experiments conducted at 70 °C are shown; pH and Fe(II) mole fraction in the mineral were varied: (A) 66% Fe²⁺, pH 10 (lactate yield shown in SI Appendix, Fig. S3) and (B) 90% Fe²⁺, pH 9.2. The dotted line represents a least squares (ordinary) fit using a one phase decay model (i.e., first-order decay model; the exponential term can be used to estimate the half-life of the process). Each marker on the graph is the mean of three replicate measurements and the error bars consist of the SE on the mean.

Fig. 4.

Pyruvate reactions after 48 h at pH 9.2 and 70 °C as a function of the Fe(II) vs. Fe(III) mole fraction of the iron hydroxide precipitate. (A) Means and SEM for alanine (blue), pyruvate (red), and lactate (green) over the range of Fe(II) mole fraction tested. (B–D) Plots of analyte reaction yields (B: alanine; C: pyruvate; D: lactate) with values from individual experiments superimposed; the box extends from the 25th to 75th percentiles, with the horizontal line in the box representing the median; whiskers represent the lowest and highest datum.