Spark of Life: Role of Electrotrophy in the Emergence of Life

Abstract

The emergence of life has been a subject of intensive research for decades. Different approaches and different environmental "cradles" have been studied, from space to the deep sea. Since the recent discovery of a natural electrical current through deep-sea hydrothermal vents, a new energy source is considered for the transition from inorganic to organic. This energy source (electron donor) is used by modern microorganisms via a new trophic type, called electrotrophy. In this review, we draw a parallel between this metabolism and a new theory for the emergence of life based on this electrical electron flow. Each step of the creation of life is revised in the new light of this prebiotic electrochemical context, going from the evaluation of similar electrical current during the Hadean, the CO₂ electroreduction into a prebiotic primordial soup, the production of proto-membranes, the energetic system inspired of the nitrate reduction, the proton gradient, and the transition to a planktonic proto-cell. Finally, this theory is compared to the two other theories in hydrothermal context to assess its relevance and overcome the limitations of each. Many critical factors that were limiting each theory can be overcome given the effect of electrochemical reactions and the environmental changes produced.

Keywords: electroreduction of CO2; electrotrophy; emergence of life; hydrothermal vents; prebiotic synthesis.

Figure 1

Estimation of onset potential E of half reactions and Gibbs free energy ΔG_r for the production of a spontaneous electrical current in different scenarios, depending on the chemistry of the HydroThermal Vent (HTV). Onset potential E were estimated with the Nernst equation, using the temperature coefficient dE/dT of each half reaction to correct the standard potential E⁰ [27], using average temperature estimated of the ocean during Archaean of 55 °C [29], and using concentrations C estimated in the literature for H₂S [30], O₂ [31], H₂O₂ [32], NO₃⁻ [26], NH₄⁺ [33], CO₂ [30], and CH₄ [34]. Concentrations are expressed as “reactant”/”product” concentrations. Potentials are expressed vs. SHE. All compounds are supposed to be dissolved in aqueous solution due to the high hydrostatic pressure (up to 600 bars), and the temperature coefficients are assumed to be constant from 25 to 450 °C, introducing a potential error. Fg: fougerite, FeS₂: pyrite or associated polymetallic sulfur.

Figure 2

Wächtershäuser, Fischer–Tropsch reactions (reaction 1) and geoelectrochemical reduction of CO₂ (reaction 2) toward the synthesis of Short Carbon Fatty Acids (SCFA). Concentration of SCFA would lead to the accumulation of amphiphilic molecules (blue pins), the formation of micelles, and the formation of the proto-membrane (reaction 3).

Figure 3

Schematic of the electrotrophy proto-metabolism hypothesis. Reaction 1 corresponds to the H₂S or H₂ oxidation step of the hydrothermal fluid leading to the production of the electric current and the release of protons. Reaction 2 corresponds to the reduction in nitrate by consuming the protons and electrons of the electric current. The confinement in a space bounded by the semi-permeable proto-membranes leads to the progressive depletion of proton from the intracellular space in case of nitrate reduction faster than the proton transport through the proto-membrane. This proton difference would lead to the creation of a driving proton force (Reaction 3).

Figure 4

Schematic of the hypothetical evolution of the proton-motive-force system. It starts, in the Part 1, with the natural proton gradient produced by the electro-reduction reactions on the chimney wall. The Part 2 represents the transition to a proto-ATP synthase transforming proto-ADP (pADP) into proto-ATP (pATP). Finally, the Part 3 shows the development of a proto-respiratory chain system (green blocks) fed by a proto-enzyme oxidizing an electron donor (yellow block), for example H₂, to maintain the proton gradient while detaching from the chimney wall and the electrical current as energy source.

Figure 5

Reconstitution of the autotrophic pathways through prebiotic synthesis by metal catalyze (green arrows) or electrochemical reaction (red arrows) from the literature review. When both type of reaction were possible, the arrow was set in red. Black arrows represent the steps of the pathways not yet replicated by prebiotic synthesis. Conditions of each reaction is referred in the boxes. References: 1—[71], 2—[68], 3—[69], 4—[72], 5—[73], 6—[74], 7—[75], 8—[62], 9—[76], 10—[74].

Figure 6

Schematic of the development of autotrophic and anabolic proto-metabolisms, leading to polymerization (reaction 1), the stabilization of the processes in an organic matrix, and to proto-enzymes (reaction 2). Stabilized processes and proto-membrane allow the translocation on the proto-cell in planktonic phase using redox mediators (reaction 3), diversification of the electron donor to soluble compounds (reaction 4), and the evolution to a self-replicative system.