Serpentinization as the source of energy, electrons, organics, catalysts, nutrients and pH gradients for the origin of LUCA and life

Abstract

Serpentinization in hydrothermal vents is central to some autotrophic theories for the origin of life because it generates compartments, reductants, catalysts and gradients. During the process of serpentinization, water circulates through hydrothermal systems in the crust where it oxidizes Fe (II) in ultramafic minerals to generate Fe (III) minerals and H2. Molecular hydrogen can, in turn, serve as a freely diffusible source of electrons for the reduction of CO2 to organic compounds, provided that suitable catalysts are present. Using catalysts that are naturally synthesized in hydrothermal vents during serpentinization H2 reduces CO2 to formate, acetate, pyruvate, and methane. These compounds represent the backbone of microbial carbon and energy metabolism in acetogens and methanogens, strictly anaerobic chemolithoautotrophs that use the acetyl-CoA pathway of CO2 fixation and that inhabit serpentinizing environments today. Serpentinization generates reduced carbon, nitrogen and — as newer findings suggest — reduced phosphorous compounds that were likely conducive to the origins process. In addition, it gives rise to inorganic microcompartments and proton gradients of the right polarity and of sufficient magnitude to support chemiosmotic ATP synthesis by the rotor-stator ATP synthase. This would help to explain why the principle of chemiosmotic energy harnessing is more conserved (older) than the machinery to generate ion gradients via pumping coupled to exergonic chemical reactions, which in the case of acetogens and methanogens involve H2-dependent CO2 reduction. Serpentinizing systems exist in terrestrial and deep ocean environments. On the early Earth they were probably more abundant than today. There is evidence that serpentinization once occurred on Mars and is likely still occurring on Saturn’s icy moon Enceladus, providing a perspective on serpentinization as a source of reductants, catalysts and chemical disequilibrium for life on other worlds.

The Moon‐Forming Impact and the Autotrophic Origin of Life

“…[43,108] In the case of the acetyl-CoA pathway from H 2 and CO 2 to pyruvate, [39,40,74,210] we finally have a concrete and reproducible example in hand where it actually happens, the function of 127 proteins (Figure 4) being replaced by a metal that, in nature, is synthesized in serpentinizing hydrothermal vents. [58] The findings of Preiner et al [49] are not an isolated report. Recent findings by the team of Harun Tüysüz at the Max-Planck Institute for Coal Research in Mülheim have characterized various parameters affecting transition metal-catalyzed H 2dependent CO 2 reduction, as summarized in Table 2.…”

“… [49] Wächtershäuser and others have proposed that single inorganic catalysts might be able to catalyze entire biochemical pathways, for example the reverse TCA cycle or purine synthesis on mineral surfaces [43,108] . In the case of the acetyl‐CoA pathway from H 2 and CO 2 to pyruvate, [39,40,74,210] we finally have a concrete and reproducible example in hand where it actually happens, the function of 127 proteins (Figure 4) being replaced by a metal that, in nature, is synthesized in serpentinizing hydrothermal vents [58] …”

“…[52][53][54][55][56] Because the effluent of serpentinizing systems is alkaline and H 2 rich, often 10 mM H 2 and more, [57] and the redox potential of the 2H + /H 2 pair is pH-dependent, the redox potential in serpentinizing systems (and laboratory simulations thereof) is on the order of À 700 to À 800 mV (Table 1). [57][58][59] This supplies the reducing power necessary for CO 2 reduction to proceed, provided that suitable metal or mineral surfaces such as Ni 3 Fe as catalysts are present. [49] The first reduced carbon compounds relevant for the origin of life could have formed from H 2 and CO 2 .…”

“…Serpentinizing systems have immense reducing power within the range of biologically relevant reactions. They can convert CO 2 to organics, N 2 to NH 3 , possibly phosphate to phosphite (recently reviewed by Schwander et al [58] …”

Opinion: The Key Steps in the Origin of Life to the Formation of the Eukaryotic Cell

“…This setting allows the path to the origin of life to be protracted, in part because it does not depend on proto-life having to be spatially autonomous from the outset. The hypothesis is also attractive given the vast number of microchambers in a given locality [34] and the possibility that the driving geochemistry, serpentinization [8,38], may have been especially widespread in the Hadean, when life evolved [34]. Note that the alkaline hydrothermal vent scenario actually requires the notion of protracted development, given that alkaline aqueous environments are inimical to the formation of RNA and DNA.…”