By Reuben Hudson et al.

Significance

Biology is built of organic molecules, which originate primarily from the reduction of CO₂ through several carbon-fixation pathways. Only one of these—the Wood–Ljungdahl acetyl-CoA pathway—is energetically profitable overall and present in both Archaea and Bacteria, making it relevant to studies of the origin of life. We used geologically pertinent, life-like microfluidic pH gradients across freshly deposited Fe(Ni)S precipitates to demonstrate the first step of this pathway: the otherwise unfavorable production of formate (HCOO^–) from CO₂ and H₂. By separating CO₂ and H₂ into acidic and alkaline conditions—as they would have been in early-Earth alkaline hydrothermal vents—we demonstrate a mild indirect electrochemical mechanism of pH-driven carbon fixation relevant to life’s emergence, industry, and environmental chemistry.

Abstract

All life on Earth is built of organic molecules, so the primordial sources of reduced carbon remain a major open question in studies of the origin of life. A variant of the alkaline-hydrothermal-vent theory for life’s emergence suggests that organics could have been produced by the reduction of CO₂ via H₂ oxidation, facilitated by geologically sustained pH gradients. The process would be an abiotic analog—and proposed evolutionary predecessor—of the Wood–Ljungdahl acetyl-CoA pathway of modern archaea and bacteria. The first energetic bottleneck of the pathway involves the endergonic reduction of CO₂ with H₂ to formate (HCOO^–), which has proven elusive in mild abiotic settings. Here we show the reduction of CO₂ with H₂ at room temperature under moderate pressures (1.5 bar), driven by microfluidic pH gradients across inorganic Fe(Ni)S precipitates. Isotopic labeling with ¹³C confirmed formate production. Separately, deuterium (²H) labeling indicated that electron transfer to CO₂ does not occur via direct hydrogenation with H₂ but instead, freshly deposited Fe(Ni)S precipitates appear to facilitate electron transfer in an electrochemical-cell mechanism with two distinct half-reactions. Decreasing the pH gradient significantly, removing H₂, or eliminating the precipitate yielded no detectable product. Our work demonstrates the feasibility of spatially separated yet electrically coupled geochemical reactions as drivers of otherwise endergonic processes. Beyond corroborating the ability of early-Earth alkaline hydrothermal systems to couple carbon reduction to hydrogen oxidation through biologically relevant mechanisms, these results may also be of significance for industrial and environmental applications, where other redox reactions could be facilitated using similarly mild approaches.

The full article appeared on the PNAS website at https://www.pnas.org/content/117/37/22873