Mineral Surface-Templated Self-Assembling Systems: Case Studies from Nanoscience and Surface Science towards Origins of Life Research

Abstract

An increasing body of evidence relates the wide range of benefits mineral surfaces offer for the development of early living systems, including adsorption of small molecules from the aqueous phase, formation of monomeric subunits and their subsequent polymerization, and supramolecular assembly of biopolymers and other biomolecules. Each of these processes was likely a necessary stage in the emergence of life on Earth. Here, we compile evidence that templating and enhancement of prebiotically-relevant self-assembling systems by mineral surfaces offers a route to increased structural, functional, and/or chemical complexity. This increase in complexity could have been achieved by early living systems before the advent of evolvable systems and would not have required the generally energetically unfavorable formation of covalent bonds such as phosphodiester or peptide bonds. In this review we will focus on various case studies of prebiotically-relevant mineral-templated self-assembling systems, including supramolecular assemblies of peptides and nucleic acids, from nanoscience and surface science. These fields contain valuable information that is not yet fully being utilized by the origins of life and astrobiology research communities. Some of the self-assemblies that we present can promote the formation of new mineral surfaces, similar to biomineralization, which can then catalyze more essential prebiotic reactions; this could have resulted in a symbiotic feedback loop by which geology and primitive pre-living systems were closely linked to one another even before life’s origin. We hope that the ideas presented herein will seed some interesting discussions and new collaborations between nanoscience/surface science researchers and origins of life/astrobiology researchers.

Biological phase separation: cell biology meets biophysics

“…5). Finally, ATPS droplets can scaffold the assembly of a layer of clay minerals, themselves an important prebiotically available geological structure promoting the synthesis and self-assembly of primitive polymers (Gillams and Jia 2018), around the droplet edge (Pir Cakmak and Keating 2017) (similar to a Pickering emulsion (Yang et al 2017)), helping to catalyze prebiotically relevant chemical reactions and to prevent coalescence of the droplets. The addition of a clay mineral layer (and perhaps a lipid layer as well) serves to preserve each droplet's individuality (Smith and Morowitz 2016), an important property important for selective evolution of primitive replicating polymers within compartments (Bansho et al 2016).…”

Recent Advances in Origins of Life Research by Biophysicists in Japan

“…Other important prebiotic catalysts include mineral surfaces, which provide not only increased local concentrations and electrochemical driving forces, but can also result in favorable orientational specificity of adsorbed molecules [46]. To date, much work has focused on harnessing these catalytic properties to study nucleic acid [47,48] and peptide polymerization in non-enzymatic mineral-catalyzed settings, but these mineral surfaces could also provide a protective or stabilizing property for these biopolymers (or components thereof) [49].…”

“…Not only do mineral surfaces catalyze prebiotic chemical reactions and polymerization of primitive biopolymers, they also effect the self-assembly of molecules to form functional structures with complex emergent properties without the need for formation of new high-energy covalent bonds (instead utilizing spontaneous thermodynamically-favorable interactions, such as van der Waals interactions, hydrogen bonding, and hydrophobic interactions, to name a few). These catalyzed phenomena include changes in nucleic acid secondary structure, assembly of organic monolayers, and formation of peptide amyloids [46]. In particular, peptide amyloid fibrils, which are assembled from a hydrophobic peptide found in Alzheimer's disease patients [52], although Not only do mineral surfaces catalyze prebiotic chemical reactions and polymerization of primitive biopolymers, they also effect the self-assembly of molecules to form functional structures with complex emergent properties without the need for formation of new high-energy covalent bonds (instead utilizing spontaneous thermodynamically-favorable interactions, such as van der Waals interactions, hydrogen bonding, and hydrophobic interactions, to name a few).…”

“…In particular, peptide amyloid fibrils, which are assembled from a hydrophobic peptide found in Alzheimer's disease patients [52], although Not only do mineral surfaces catalyze prebiotic chemical reactions and polymerization of primitive biopolymers, they also effect the self-assembly of molecules to form functional structures with complex emergent properties without the need for formation of new high-energy covalent bonds (instead utilizing spontaneous thermodynamically-favorable interactions, such as van der Waals interactions, hydrogen bonding, and hydrophobic interactions, to name a few). These catalyzed phenomena include changes in nucleic acid secondary structure, assembly of organic monolayers, and formation of Challenges 2019, 10, 28 5 of 21 peptide amyloids [46]. In particular, peptide amyloid fibrils, which are assembled from a hydrophobic peptide found in Alzheimer's disease patients [52], although themselves not prebiotically plausible due to their length (42 amino acids), provide a model system by which other potential prebiotic self-assembling peptide fiber systems (which are much shorter in length), such as tripeptides, like KYF (K: Lysine, Y: Tyrosine, F: Phenylalanine) [20], can be studied.…”

“…However, in spite of all of this focus on lipid vesicles, primitive compartments need not necessarily be lipid bilayer vesicles, as there are many other model systems that could have afforded essentially the same properties as lipid vesicles, including amphiphilic peptide vesicles [104], cationic organic amphiphile membrane vesicles [87], inorganic chemical cells [105], oil-in-water microdroplets [69], coacervate [106][107][108] (Figure 4) and aqueous two-phase system [109,110] droplets, and even membraneless polyester microdroplets [111], each of which is important for not only biophysicists, but also materials scientists. We look forward to the further collaboration between these two fields in Japan and abroad not only for further elucidation of the assembly and dynamics of primitive compartments in the context of OoL research, but also perhaps for the development of new therapeutic tools or new discoveries about modern biological systems as well [46]. in mixed dioleoylphosphatidylglycerol (DOPG) and dioleoylphosphatidylcholine (DOPC) phospholipid vesicle membranes, causing leakage of the internal components, which when applied to real bacterial cells, results in cell death.…”