A Global Scale Scenario for Prebiotic Chemistry: Silica-Based Self-Assembled Mineral Structures and Formamide

Abstract

The pathway from simple abiotically made organic compounds to the molecular bricks of life, as we know it, is unknown. The most efficient geological abiotic route to organic compounds results from the aqueous dissolution of olivine, a reaction known as serpentinization (Sleep, N.H., et al. (2004) Proc. Natl. Acad. Sci. USA 101, 12818–12822). In addition to molecular hydrogen and a reducing environment, serpentinization reactions lead to high-pH alkaline brines that can become easily enriched in silica. Under these chemical conditions, the formation of self-assembled nanocrystalline mineral composites, namely silica/carbonate biomorphs and metal silicate hydrate (MSH) tubular membranes (silica gardens), is unavoidable (Kellermeier, M., et al. In Methods in Enzymology, Research Methods in Biomineralization Science (De Yoreo, J., Ed.) Vol. 532, pp 225–256, Academic Press, Burlington, MA). The osmotically driven membranous structures have remarkable catalytic properties that could be operating in the reducing organic-rich chemical pot in which they form. Among one-carbon compounds, formamide (NH2CHO) has been shown to trigger the formation of complex prebiotic molecules under mineral-driven catalytic conditions (Saladino, R., et al. (2001) Biorganic & Medicinal Chemistry, 9, 1249–1253), proton irradiation (Saladino, R., et al. (2015) Proc. Natl. Acad. Sci. USA, 112, 2746–2755), and laser-induced dielectric breakdown (Ferus, M., et al. (2015) Proc Natl Acad Sci USA, 112, 657–662). Here, we show that MSH membranes are catalysts for the condensation of NH2CHO, yielding prebiotically relevant compounds, including carboxylic acids, amino acids, and nucleobases. Membranes formed by the reaction of alkaline (pH 12) sodium silicate solutions with MgSO4 and Fe2(SO4)3·9H2O show the highest efficiency, while reactions with CuCl2·2H2O, ZnCl2, FeCl2·4H2O, and MnCl2·4H2O showed lower reactivities. The collections of compounds forming inside and outside the tubular membrane are clearly specific, demonstrating that the mineral self-assembled membranes at the same time create space compartmentalization and selective catalysis of the synthesis of relevant compounds. Rather than requiring odd local conditions, the prebiotic organic chemistry scenario for the origin of life appears to be common at a universal scale and, most probably, earlier than ever thought for our planet.

The key role of meteorites in the formation of relevant prebiotic molecules in a formamide/water environment

“…NH 2 CHO/water solutions were recently shown to form a multipurpose reactive mixture in a totally different reaction system33. Unlike recent theoretical argumentation of the contrary40, the data described here and in ref.…”

“…Unlike recent theoretical argumentation of the contrary40, the data described here and in ref. 33 show that NH 2 CHO/water is a flexible and fertile prebiotic incubator.…”

“…Alkaline earth metals and transition metal ions coordinate the nucleophilic centers in NH 2 CHO, to yield complexes with different geometries and stabilities, which are known to lose water in the presence of high energy sources to yield HCN32, one of the key intermediate in the synthesis of both nucleobases and carboxylic acids (SI #8). Different transition metal compounds have been recently reported as efficient catalysts for the prebiotic synthesis of a large panel of prebiotic molecules from NH 2 CHO in geochemical scenarios33. Hydrothermal systems are accepted models of prebiotic environments, and several organics have been detected in abiotic hot springs34.…”

Silica Metal Oxide Vesicles Catalyze Comprehensive Prebiotic Chemistry

“…Interestingly, serpentinization environments may form alkaline waters rich in silica. It has been experimentally demonstrated that these alkaline waters induce the growth of self‐assembled mineral structures, including silica/carbonate biomorphs mimicking the morphology of primitive organisms, calcium carbonate mesocrystals similar to those formed in biominerals, and silica metal oxy/hydroxide bilayer membranes, also known as silica gardens, with interesting catalytic properties . We have synthesized these mineral membranes in alkaline silica‐rich solutions similar to those deriving from serpentinization reactions in the presence of formamide at 80 °C.…”

Stability of 2′,3′ and 3′,5′ cyclic nucleotides in formamide and in water: a theoretical insight into the factors controlling the accumulation of nucleic acid building blocks in a prebiotic pool

“…1,2 Note that numerous independent recent studies demonstrate that non-equilibrium chemical processes could play an important role at the origin of terrestrial life. [55][56][57] Present computations and former experiments 3 show that in water 2',3' cyclic nucleotides are more stable over the whole studied temperature range, i.e. from room temperature up to 363 K. This adds to the credibility of aqueous prebiotic scenarios, which consider 2',3' cyclic nucleotides as the predecessors of the most ancient oligonucleotides.…”