Organic Matter Degradation in Energy-Limited Subsurface Environments—A Bioenergetics-Informed Modeling Approach

Abstract

Microbial degradation of organic matter is a key driver of subsurface biogeochemistry. Here, we present a bioenergetics-informed kinetic model for the anaerobic degradation of macromolecular organic matter that accounts for extracellular hydrolysis, fermentation, and respiration. The catabolic energy generated by fermentation and respiration is allocated to biomass growth, production of extracellular hydrolytic enzymes, and cellular maintenance. Microbial cells are assumed to exist in active or dormant states with marked differences in maintenance energy requirements. Dormant cells are further assumed to fulfill their maintenance energy requirements by utilizing their own biomass instead of relying on external substrates. When the catabolic Gibbs energy production for a given functional group of microorganisms exceeds the total maintenance energy requirement of the active cells, biomass growth, re-activation of dormant cells, and production of extracellular hydrolytic enzymes are possible. The latter, in turn, allows the microbial community to access more of the available external organic substrates. In the opposite case, active cells decay or become dormant. We apply the model to simulate the anaerobic degradation of cellulose by a hypothetical microbial community consisting of cellulolytic fermenting bacteria and sulfate-reducing bacteria, under conditions representative of those encountered in water-saturated subsurface environments.