A Thermodynamic Model for Water Activity and Redox Potential in Evolution and Development

Abstract

Reactions involving water and oxygen are basic features of geological and biological processes. To understand how life interacts with its environment requires monitoring interactions with $\mathrm{H}_{2}\mathrm{O}$ and $\mathrm{O}_{2}$ not only at timescales relevant to organismal growth but also over billions of years of geobiological evolution. Chemical transformations intrinsic to evolution and development were characterized by analyzing data from recent phylostratigraphic and proteomic studies. This two-stage analysis involves obtaining chemical metrics (carbon oxidation state and stoichiometric hydration state) from the elemental compositions of proteins followed by modeling the relative stabilities of target proteins against a proteomic background to infer thermodynamic parameters [oxygen fugacity, water activity, and virtual redox potential (Eh)]. The main results of this study are a rise in carbon oxidation state of proteins spanning the time of the Great Oxidation Event, a rise in virtual redox potential that coincides with the likely emergence of aerobic metabolism, and a rise in carbon oxidation state of proteins inferred from the transcriptome in late stages of Bacillus subtilis biofilm growth. Furthermore, stoichiometric hydration state of expressed proteins decreases through stages of biofilm development, drops at the same time as a drop in organismal water content during fruit fly development, and is lower for proteins with more recent gene ages, all of which support the inference of higher hydration potentials at earlier time points. These results show how the evolutionary and developmental dynamics of major chemical variables can be deciphered through thermodynamic analysis of proteins as chemical entities.