Mineral surface chemistry control for origin of prebiotic peptides

Abstract

Some seventy years ago, John Desmond Bernal proposed a role for clays in the origin of life. While much research has since been dedicated to the study of silicate clays, layered double hydroxides, believed to be common on the early Earth, have received only limited attention. Here we examine the role that layered hydroxides could have played in prebiotic peptide formation. We demonstrate how these minerals can concentrate, align and act as adsorption templates for amino acids, and during wetting-drying cycles, promote peptide bond formation. This enables us to propose a testable mechanism for the growth of peptides at layered double hydroxide interfaces in an early Earth environment. Our results provide insights into the potential role of mineral surfaces in mimicking aspects of biochemical reaction pathways.

Fig. 1

Amino acids and peptides intercalated in hydrated LDH. Example of modeled systems, showing how natural mixtures of a amino acids, b short, and c long peptides adsorb onto the LDH interlayers via their C-terminal. Colors are as follows: Mg, pink spheres; Al, gray spheres; Cl, blue spheres; O, red; H, white; N, blue; and backbone is represented with a yellow spline. For clarity water and H atoms on the amino acids are not shown

Fig. 2

Amino acids and peptides adsorbed onto LDH. a Percentage of adsorbed amino acids as a function of their hydration (number of water molecules per amino acid). b Percentage of adsorbed di-peptides, hexa-peptides, and 24-mers in a fully hydrated system. Error bars represent standard deviation. With the exception of lysine, both single amino acids and peptides adsorb onto the LDH surface (distance <2.5 Å). Aspartate can adsorb both via its backbone (labeled ASP bb) and side-chain (ASP sc). Though less adsorbed than di-peptides, hexa-peptides, and 24-mers still feature significant adsorption rates, indicating that chain length has only a minor effect on peptide adsorption

Fig. 3

Dehydration promotes formation of reactive pairs. a Percentage of amino acids' reactive pairs as a function of their hydration (number of water molecules per amino acids). Error bars represent standard deviation. For all amino acids, the percentage of reactive pairs in the system increases upon dehydration. b Top view of amino acids adsorbed and co-aligned onto the LDH surface, forming potential reactive pairs (shown spheres, where the backbone nitrogen is colored in blue, and most proximal backbone oxygen in red). c Reactive pairs show a range of different possible orientation, involving one or both adjacent LDH layers. Colors are as follows: Mg, pink spheres; Al, gray spheres; Cl, blue spheres; O, red; H, white; N, blue; and backbone is represented with yellow spline. For clarity water and H-atoms on the amino acids are not shown

Fig. 4

Adsorbed amino acids and peptides remain mobile. a Velocities of adsorbed amino acids as a function of their hydration (number of water molecules per amino acid). b Velocities of adsorbed di-peptides, hexa-peptides, and 24-mers in a fully hydrated system. c Time bound of adsorbed amino acids after a first adsorption event as a function of their hydration (number of water molecules per amino acid). d Time bound of adsorbed amino acids after a first adsorption event of adsorbed di-peptides, hexa-peptides, and 24-mers in a fully hydrated system. Error bars represent standard deviation. When adsorbed, amino acids and peptides remain mobile upon the LDH surface. Even upon full dehydration, drift on the LDH plane can be observed for all amino acids. Upon a first adsorption event, both amino acids and peptides remain in contact with the LDH surface for majority of the time. Nevertheless, short desorption events (in average ~5% of the time) are still observed

Fig. 5

Proposed mechanism for LDH supported peptide bond formation. a Upon dehydration, the N- and C-termini of adsorbed amino acids co-align, allowing the formation of a peptide bond. The newly formed di-peptide remains tethered via C-terminus only. The bond formation leads to the loss of charge, facilitating introduction of a new amino acid. The N-terminal of amino acid is then able to form a bond with the C-terminal of di-peptide, thus triggering further peptide growth. b A kinetic model of peptide growth upon multiple dehydrations—rehydration cycles. After a single dehydration, only dimers to hexamers are observed. Subsequent washing cycles lead to the formation of longer chains