Mapping the Environmental Boundaries for Methanogenesis in Serpentinizing Systems using a Cell-scale Numerical Model

Serpentinizing systems occur where liquid water reacts with ultramafic minerals. The reaction releases heat and produces an alkaline fluid that is rich in H₂. The abundant H₂ suggests that the energetics of methane production by CO₂ reduction is highly favorable (ΔG ~ -10² kJ/mol CH₄ for [H₂] ~ 10^-2 M). Given the possibility of subsurface water and ultramafic minerals on Mars, methanogenesis in serpentinizing systems has been considered as a possible model for photosynthesis-independent, extraterrestrial life. However, the high pH (9 - 11) and possibly elevated temperature have a negative impact on the overall cellular energy balance by increasing the cell's maintenance energy and reducing the concentration of CO₂ substrate. We developed a reaction-transport model on the scale of a methanogen cell to investigate how the overall bioenergetics of methane production is influenced by the interplay between pH, temperature, and H₂ and CO₂ concentration. The model differentiates the cell into three basic structural units (cell wall, cell membrane with gated ion channels, and cytoplasm) and employs both thermodynamic and kinetic controls to estimate an upper-limit energy yield as a function of environmental conditions. The model provides a map of the range of environmental extremes for which the energy balance for microbial methane production is positive. The model also provides a tool for exploring the energetics of different metabolic strategies that methanogens could use to cope with stresses associated with life in an alkaline, low-CO₂ environment.