Native iron reduces CO2 to intermediates and end-products of the acetyl-CoA pathway

Abstract

Autotrophic theories for the origin of life propose that CO₂ was the carbon source for primordial biosynthesis. Among the six known CO₂ fixation pathways in nature, the acetyl-CoA (AcCoA; or Wood-Ljungdahl) pathway is the most ancient, and relies on transition metals for catalysis. Modern microbes that use the AcCoA pathway typically fix CO₂ with electrons from H₂, which requires complex flavin-based electron bifurcation. This presents a paradox: how could primitive metabolic systems have fixed CO₂ before the origin of proteins? Here, we show that native transition metals (Fe⁰, Ni⁰ and Co⁰) selectively reduce CO₂ to acetate and pyruvate-the intermediates and end-products of the AcCoA pathway-in near millimolar concentrations in water over hours to days using 1-40 bar CO₂ and at temperatures from 30 to 100 °C. Geochemical CO₂ fixation from native metals could have supplied critical C₂ and C₃ metabolites before the emergence of enzymes.

Fig. 1

Mechanistic outline of the ATP-independent AcCoA pathway found in archaea. The reductive carboxylation of AcCoA to pyruvate is also found in the first step of the rTCA cycle. For clarity, organic and metallic co-factors are depicted as a squiggly line.

Fig. 2

Carbon fixation by metals under hydrothermal conditions: 100 °C, 35 bar CO₂, 1 M KCl in H₂O, pH = 7 (except for Mo, where the initial unbuffered pH was 2), 16 h (see SI for experimental and analytical details, as well as error analysis). Bar chart shows mean values of at least two independent runs. ^‡ Formate concentrations: 2.13 mM, 2.44 mM; reported error corresponds to mean standard deviation.

Fig. 3

Effect of temperature, pressure and reaction time on iron-promoted CO₂ fixation in aqueous solution. a Effect of temperature (35 bar CO₂; 16 h). b Effect of CO₂ pressure (30 °C; 16 h). c Reaction progress over time (30 °C; 1 bar CO₂). d Reaction progress over time (100 °C; 35 bar CO₂). All reactions are 1 M Fe in 1 mL of a 1 M KCl solution. In a and b bar charts show mean values of at least two independent runs. In c and d error bars correspond to the mean average deviation from at least two independent runs. Lines connecting the data points do not represent a model fit.

Fig. 4

Plausible mechanism for carbon fixation on the surface of Fe⁰ accounting for the detection of formate, methanol, acetate and pyruvate in aqueous solution upon hydrolysis with KOH. The depicted surface bound acyl structures are deliberately ambiguous and may represent a surface-bound carboxylate or an acyl metal species.

Fig. 5

Hypothetical ancestral proto-anabolic network consisting of a hybrid of the AcCoA pathway and the rTCA cycle, showing the role of its intermediates as universal biosynthetic precursors. The 11 steps of the cycle (A-K) have been assigned colour-coded labels according to their chemical mechanism.