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 (or Wood-Ljungdahl) pathway is the most ancient, and relies on transition metals for catalysis. Modern microbes that use the acetyl CoA 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, Co0) selectively reduce CO2 to acetate and pyruvate, the intermediates and end-products of the AcCoA pathway, in near mM levels in water over hours to days using 1-40 bar CO2 and at temperatures from 30-100 °C. Geochemical CO2 fixation from native metals could have supplied critical C2 and C3 metabolites before the emergence of enzymes.

Something special about CO‐dependent CO2 fixation

“…Nevertheless, the special bond between CO and transition metals also enables carbonyl insertion, both in industrial chemistry (heterogenic catalysis) , and in one very ancient and important biological reaction – CODH/acetyl‐CoA synthase , which requires the essential Ni‐Fe‐S cluster for achieving the slow reduction of CO 2 to CO. Recent studies showing that CO 2 is efficiently reduced by native metals to acetyl and pyruvoyl moieties entail metal bound carbonyl groups and carbonyl insertions in the proposed reaction mechanisms . This parallels the Fischer‐Tropsch type reaction mechanisms suggested for geochemical CO 2 reduction processes giving rise to abiotic organic molecules in hydrothermal vents .…”

“…Its linear nature, chemical simplicity, favorable energetics, and occurrence among both Bacteria and Archaea set it apart from other pathways of CO 2 fixation and suggest that the WL is the most ancient of CO 2 fixation pathways . Strong evidence supporting the antiquity of the WL pathway comes from new findings showing that its main reactions are facile, with its central intermediates including pyruvate arising spontaneous in laboratory reactions overnight from CO 2 and water at temperatures of 30–100 °C in the absence of enzymes, with native metals such as Fe 0 and Ni 0 functioning as catalysts and reductants . From the standpoint of energetics, there is something very special about the reductive acetyl‐CoA pathway among metabolic pathways.…”

A thermodynamic atlas of carbon redox chemical space

“…It would be particularly interesting to include carboxylation and decarboxylation reactions (both reductive/oxidative and non-reductive/non-oxidative), which would effectively connect the different n-carbon redox chemical spaces to each other, but would significantly increase the complexity of the analysis. In addition, including additional types of reactions such as aldol/retro-aldol reactions and hydrations/dehydrations would fully map the chemical space model to experimentally tractable reaction networks 25,[64][65][66] .…”

Photosynthesis on exoplanets and exomoons from reflected light

“…Of these five networks, the two most important are the reverse tricarboxylic acid (rTCA) cycle and the Wood-Ljungdahl pathway. A combination of physiological, genomic and bioenergetic arguments have been marshalled (Smith and Morowitz, 2016;Weiss et al, 2018;Nunoura et al, 2018) in conjunction with promising laboratory experiments (Muchowska et al, 2017;Varma et al, 2018;Muchowska et al, 2019) to suggest these pathways were the first to emerge on Earth; in fact, certain proposals hypothesize that a hybrid of these two networks might have constituted the ancestral metabolic pathway (Braakman and Smith, 2012;Camprubi et al, 2017).…”