Anaerobic microbial growth near thermodynamic equilibrium as a function of ATP/ADP cycle: The effect of maintenance energy requirements

• A model for anaerobic growth for low yielding energy environments has been proposed.
• Maintenance energy requirements take precedence over cell synthesis reactions.
• Thermodynamic equilibrium determines ATP utilization rate.
• Model verification using experimental data on arsenate reduction by Bacillus arsenicoselenatis.

For predicting microbial metabolism in low energy yielding environments, various rate laws have been proposed to account for the effects of thermodynamic state (as a measure of product-inhibition) as well as maintenance requirements on energetics of mediated reactions. Explicit or implicit modeling of simplified ATP reactions allows distinction between energy and ATP producing (catabolic, treated as kinetic and reversible) and energy and ATP consuming (anabolic) processes including maintenance requirements. Here, we provide a comparison of several approaches for modeling microbial metabolism in anaerobic environments considering thermodynamic factors, and maintenance energy requirements. We develop a mathematical model for microbial metabolism in anaerobic systems, which couples catabolic and anabolic processes considering the limiting effects of intermediate concentrations on reaction rate through the reduction of chemical potential and reversibility, and that explicitly partitions energy (ATP) allocation between cell growth and maintenance. We include an approach where maintenance energy requirements are assumed to take precedence over ATP-consuming cell synthesis reactions. Also, substrate utilization terminates when the catabolic reactions reach thermodynamic equilibrium with respect to ATP formation, including maintenance energy. The comparison of the proposed model to other modeling approaches shows the benefits of incorporating product inhibition and maintenance requirements in situations which maintenance energy requirements are comparable in size to growth energy requirements. An example application is also presented, where the proposed model is applied to an experimental study of arsenate reduction by Bacillus arsenicoselenatis conducted by Blum et al. (Arch Microbiol. 171 (1998) 19-30), in which the rate of metabolism is controlled by thermodynamics.