Origin and evolution of biopolymers: filling the gap between geochemistry and biochemistry

In modern biology, energy harvest and reproduction of components are achieved through chemical reaction governed by polypeptides, while evolvability of the system is maintained by exchange or vertical decent of genetic information carried by nucleotide polymers (DNA/RNA). One of the ELSI's main research goal is to provide a plausible and stepwise scenario to the origins of life on Earth, presumably first driven by geochemical processes providing the disequilibrium, which then led to the birth of biochemistry. Different hypotheses prioritize on different aspects (e.g., metabolism-first vs RNA world), and as part of this collective effort, I will be prioritizing on the origin and evolution of biopolymers to fill the gap between the geochemistry and polymer-driven biochemistry. I will introduce three experimental approaches addressing synthesis, selection and coevolution of polymers with regards to origins of life study.

First, we will explore the possibility of biopolymer formation at the boundary of seawater and CO₂ fluid that likely exist at the Hadean deep-sea hydrothermal system. In general, hydrothermal system has been seen as thermodynamically unfavorable condition for polymer synthesis, however due the 1-2% water solubility under high pressure, liquid CO₂ behave as a hydrophobic solvent. By using the original pressure reactor, we will monitor condensation reaction of organic compounds (e.g. amino acids, esters, nucleotide precursors) to see if they can form polymers and other complexed molecules.

Next, we aim to address the question of how polymers can be selected and enriched under certain condition. It has been shown that various mineral surfaces can absorb diverse organic compounds in different geochemical settings. Polymers that are capable of interacting physically and chemically, will remain and alter the surface chemical properties. This selection process will provide emergent function prior to the replication of functional molecules. We have designed an experimental setup to test random peptide adsorption on a Mackinawite (FeS) and nickel sulfide (NiS) surface as a model case. Adsorbed and unadsorbed peptides are subjected to acid hydrolysis to monitor their amino acid composition and we are seeing selective features based on their amino acid profiles. Given the essential role of iron-sulfur (Fe-S) clusters in biology, functional properties of surface-selected peptides will be further evaluated in conjunction with electrochemical settings.

Finally, we will address early evolution of biopolymers during the pre-LUCA period, at the stage when multiple biopolymers were coexistent. The molecular record indicates that functional RNA-protein complexes (RNPs) represent highly conserved assemblies in modern cells, such as the ribosome that carries out transfer of information from nucleotide polymers to polypeptides. However, previous in vitro evolution experiments were mostly focused on evolving a single type of biopolymer. Therefore, using synthetic biology approach, we have been developing a new experimental system to coevolve both RNA and peptide sequences from a random sequence pool to subject the population against specific function such as ATP-binding. Comparison between RNP vs RNA-only (control) have shown divergence of sequences over rounds of selection, suggesting that coexistence of two polymers will undergo different evolutionary trajectory. Our long-term goal is to apply this new technique to address the origin and evolution of ribosome.