Primitive Earth - Biomolecules Interacting with hydrothermal Oceanic Minerals – PREBIOM

Characterization of adsorption mechanism of nucleotides and amino acids onto mineral surface
We targeted a series of minerals that could be formed from the hydrothermal alteration of peridotites, komatiites, basalts and gabbros. They include serpentine minerals, talc, brucite, magnesium and iron-rich clay minerals such as nontronite and amorphous silica previous in a large variety of natural environments.
We paid great attention and dedicated significant effort to measure in detail the physical and chemical properties of the reactive surfaces of minerals, prior to adsorption measurements. Then adsorption isotherms have been measured at ambient pressure and temperature; some were measured as a function of hydrostatic pressure in the high-pressure reactors developed in this project. We also investigated the effect of the chemistry of the aqueous solution corresponding to different hypotheses on the chemical composition of the primitive ocean.The interpretation of adsorption isotherms has been completed and validated by low pressure gas adsorption, by Raman and/or infrared vibrational spectroscopy, by in situ X-ray spectroscopy (XANES) at high spatial resolution of the adsorbed molecules as well as by numerical calculations of molecular dynamics. When possible, adsorbates were desorbed and analyzed by liquid chromatography (HPLC) and mass spectrometry (ESI-MS).

We studied the adsorption of RNA and DNA monomers on minerals that were abundant in the early Earth environment as the result of aqueous or hydrothermal alteration of the primitive oceanic crust. It included Fe-Mg rich swelling clays and non-swelling phyllosilicates suspended in an aqueous saline solution analog to seawater. We found that DNA adsorbs much more strongly than RNA, and that any monomer containing the G nucleobase adsorbed more strongly than one containing the C nucleobase. We could infer that all nucleotides behave as homologous molecules in regard to their adsorption onto the studied mineral surfaces. At low to moderate surface loadings and pH 7, adsorption certainly proceeds by ligand exchange between the phosphate group and the hydroxyls of the broken edges of phyllosilicates leading to the saturation of lateral surfaces. Below pH 4, swelling clays also adsorb nucleotides through cation exchange on basal surfaces. We propose that Fe-Mg rich phyllosilicates tightly bind nucleotides and concentrate them up to 1000 times the solution concentration under ambient conditions. Nontronites have the most diverse and favorable adsorption behaviors and could have helped to the concentration and polymerization of nucleotides under primitive Earth-like conditions. Although the salinity of the primitive ocean is still a matter of debate, we could show that the adsorption capacity of swelling clays is very sensitive to the actual salinity and composition of the ocean. An hadean ocean richer in divalent cations that the modern ocean would strongly enhance the role of clay surfaces with respect to their adsorption capacity toward nucleotides and potentially favor their polymerization.
Finally, we could show that amino acids polymerize rapidly under hydrothermal conditions over a limited pressure range and the yield of the reaction depends on the presence of catalyst minerals such as magnetite.

Interactions between nucleotides and mineral surfaces obviously depend on the properties of the surfaces but also largely of the chemistry of the aqueous solution; pH, concentration and nature of the divalent cations in particular, transition metals strongly enhancing nucleotides adsorption and even more at high pH. The polymerization of the simplest amino acid glycine occurs spontaneously under hydrothermal conditions, with the dominant formation of linear oligomers (for the first time), the mineral surfaces tested (silica, magnetite) enhance polymerization and induce amino acids selectivity.

The numerous results were translated in 8 publications in international journals targeting different scientific communities (chemistry, astrobiology, clays). Beyond publications and communications at international conferences, the consortium has organized a dedicated session at the Euroclays conference (Paris, 2019). Moreover, on the topic of the origin of life that triggers the curiosity of the society, the PREBIOM results have been widely presented to the public at large (several townhall meetings).

The question of the origin of life is a long standing one, the answer to which is likely to be very complex and require the consideration of concepts from many disciplines including biology, chemistry, astrophysics, and the Earth and Planetary sciences. The aim of this proposal is not to solve the whole issue of the origin of life but to focus on one aspect that is amenable to the time frame of a 3.5 year proposal: the concentration of the elementary building blocks of life such as amino acids and nucleotides on mineral surfaces to levels allowing polymerization, a prerequisite to forming the proto-biopolymers of proteins and nucleic acids. We recognize the existence of other explanations for the rise in biological complexity, and we do not exclude them, but the focus of our proposal is to explore the chemistry that occurs at mineral surfaces.
The PREBIOM proposal (Primitive Earth Biomolecules Interacting with Oceanic Minerals) focuses on the minerals that were abundant in the Hadean oceans and the pressure and temperature conditions characteristics of oceanic hydrothermal systems. We target a series of minerals that could be formed from the hydrothermal alteration of peridotites, komatiites, basalts and gabbros. They include serpentine minerals, talc, brucite, magnesium and iron-rich clay minerals such as nontronite and saponite, iron oxides and sulfides. Adsorption isotherms of amino acids and nucleotides will be measured at ambient pressure when not yet available as well as under hydrothermal conditions. To the best of our knowledge, adsorption of organic molecules under hydrothermal conditions has never been performed, although hydrothermal organic synthesis has already revealed facile reaction mechanisms for the production and polymerization of a variety of biomolecules. Interpretation of adsorption isotherms with in situ and ex situ spectroscopic analyses of the adsorbed biomolecules and theoretical calculations should lead to a detailed understanding of the reaction mechanisms for condensation, adsorption and polymerization. In addition to the above minerals, the experiments will also be performed on the one hand on high-surface silica as a reference material and on the other hand on natural samples of hydrothermal black and white chimneys representative of the three types of hydrothermal venting systems known to date. A limited number of biomolecules have been chosen to focus on representative interaction mechanisms with the selected minerals.
The PREBIOM interdisciplinary consortium is composed of 5 partners (LGL, Lyon; LRS, Paris; PhENIx, Paris; LIEC, Nancy; JHU/GL-CIW, USA) all of them already involved in the investigation of the interactions between organic molecules and mineral surfaces. Some partners in this consortium have collaborated. However the consortium has been significantly enlarged. It now involves complementary experimental, analytical and theoretical skills in mineralogy, chemistry, physical chemistry and geology. Collaborative experimental and theoretical work is new to this topic.
Results from the PREBIOM project are expected at various levels. The experimental and theoretical work proposed here will provide unique fundamental results on the condensation, adsorption and polymerization under thermodynamic conditions that have not yet been explored but were probably mandatory for the development of the abiotic organic synthesis of proteins and nucleic acids of intermediate length. They are a prerequisite to conduct any further (geo)chemical and thermodynamic modelling. The careful selection of mineral surfaces, biomonomers or simple molecules, and thermodynamic conditions will certainly put constraints on a suitable geological environment that may have witnessed some steps of the emergence of life on Earth. Project results will be broadly disseminated through publications and communications at international conferences and may in addition generate some interest to a broader audience.