Combined thermodynamic-kinetic-competitive controls on anaerobic respiration pathways and the chemistry of natural waters

Sergei Katsev , Itay Halevy

Microbial metabolisms underpin geochemical cycling in nearly all of the Earth's biosphere. Anaerobic pathways of carbon mineralization by iron and sulfate reduction and methanogenesis, in particular, have existed over most of Earth history and have been central in shaping the chemistry of the oceans and atmosphere. The governing principles by which microbial metabolisms contribute to water-column chemistry, however, are incompletely understood in natural systems where microbes compete for resources. Contrary to common assumptions, thermodynamics often fails to reproduce the observed metabolic succession. Here, we analyze the coupled effects of thermodynamics, kinetics, population dynamics, and physical transport on the composition of microbial communities, their integrated rates of metabolic activity, and effects on the chemistry of aqueous environments. Together, these controls explain the microbiology and chemistry of modern lakes and seas, and constrain the expected variability in the Earth's oceans over geologic time. We find, in particular, that microbial sulfate reduction, despite being less thermodynamically favored than iron reduction, can account for a significant fraction of organic matter remineralization, even without producing measurable concentrations of aqueous sulfide. In ferruginous water columns, methanogenesis is viable under low (<~100 uM) sulfate conditions, but methane accumulation in early oceans was unlikely before a widespread oxygenation of the ocean surface. We also illustrate how processes in anoxic water columns become reflected in the deposition of iron sulfide minerals that are commonly used as proxies of paleoredox conditions.