Abstract
Determining the limits of subsurface microbial life and its response to climatic and anthropic forcing requires understanding its link with environmental conditions. Thermodynamics has been used for decades to related mineral and fluid composition to the physicochemical variables of the environment; however, application to the biosphere has been scarce. Here, using data from shotgun metagenomic sequencing, I developed a thermodynamic model of the chemical activity of in-silico proteins to investigate the relationship between the chemical and taxonomic composition of microbial communities and subsurface redox potential. The model relies on metagenomic data from peat soils characterized by sharp redox gradients from the surface to a few meters depth. The average oxidation state of carbon and the redox potential of maximum relative activities of in-silico proteins decrease with depth. The protein-informed Eh values are consistent with the successive occurrence of anaerobic metabolisms. The evolution of taxonomic abundance with depth encodes the chemical variability of in-silico proteins, which allows linking quantitatively taxonomic evolution and redox potential.   These results show that a metastable state of thermodynamic equilibrium is reached between the environmental redox conditions and the chemical composition of community-level proteomes which encodes the taxonomic abundance. This is a paradigm shift in which microbial life is not entirely out of equilibrium. Instead, the minimization of chemical disequilibrium of community-level proteomes relative to the prevailing environmental conditions is an evolutionary process, resulting either from phylogenetic or ecological adaptation. By providing a mechanistic understanding of the coevolution of the biosphere and geosphere, this work offers prospects for the predictive modeling of microbial community composition and physicochemical conditions in various environments.  
Published Version
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