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 H 2 O and O 2 at timescales relevant to not only organismal growth but also billions of years of geobiological evolution. Here, 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, a rise in carbon oxidation state of proteins inferred from the transcriptome in late stages of Bacillus subtilis biofilm growth, and a drop in stoichiometric hydration state of the fruit fly developmental proteome at the same time as a drop in organismal water content. Stoichiometric hydration state also decreases for proteins with more recent gene ages and through stages of biofilm development, leading to predictions of higher hydration potentials at earlier time points. By building chemical representations of protein evolution and developmental proteomes, exciting new types of geobiochemical proxies can be developed.

Two dimensions of chemical variation of the human microbiome across body sites and in COVID-19 patients

“…The specific components – also known as basis species – used in this study are glutamine, glutamic acid, cysteine, H 2 O, and O 2 , which have been referred to as the QEC basis species [29]. The inclusion of amino acids rather than simple inorganic species permits a better separation of trends of oxidation and hydration state among proteins in representative genomes [31]; these particular amino acids were chosen because they are relatively abundant and highly connected metabolites and yield a relatively low covariation between and Z C [29].…”

“…4) For all the proteins in a given genome, there is very little correlation between Z C and n H 2 O (i.e. stoichiometric hydration state) (Dick, 2022). This is important because it shows that metrics for oxidation and hydration state measure different aspects of the chemical variation between proteins.…”

“…Associations between proteomic n H 2 O and the environment or physiology are evident in various systems, including 1000 km-scale salinity gradients, cancer compared to normal tissue, and growth stages of Bacillus subtilis biofilms [29][30][31].…”

“…In contrast to detecting physical interactions of water molecules, stoichiometric hydration state is a chemical metric that is calculated by balancing chemical reactions using the elemental composition of proteins (see below and [29]). Associations between proteomic and the environment or physiology are evident in various systems, including 1000 km-scale salinity gradients, cancer compared to normal tissue, and growth stages of Bacillus subtilis biofilms [29–31].…”

chem16S: community-level chemical metrics for exploring genomic adaptation to environments

“…A projection from elemental composition to chemical composition by means of thermodynamic components (aka basis species) permits the calculation of stoichiometric oxidation state ( n ) and hydration state ( n ). For protein sequences in a given genome, the element-based metric Z and reaction-based metric n strongly covary, but n is largely decoupled from Z ( Dick 2022 ); salinity is one factor that may modulate the differences of n between free-living communities ( Dick et al 2020 ). Other metrics available in chem16S are elemental ratios (H/C, N/C, O/C, and S/C), basic physicochemical quantities including protein length and molecular weight of amino acid residues, and derived quantities including grand average of hydropathicity (GRAVY) and isoelectric point (pI); the latter two are modeled after the ProtParam tool in UniProt ( Gasteiger et al 2005 ).…”