Physiological Acclimation Extrapolates the Kinetics and Thermodynamics of Methanogenesis From Laboratory Experiments to Natural Environments

Abstract

Chemotrophic microorganisms face the steep challenge of limited energy resources in natural environments. This observation has important implications for interpreting and modeling the kinetics and thermodynamics of microbial reactions. Current modeling frameworks treat microbes as autocatalysts, and simulate microbial energy conservation and growth with fixed kinetic and thermodynamic parameters. However, microbes are capable of acclimating to the environment and modulating their parameters in order to gain competitive fitness. Here we constructed an optimization model and described microbes as self-adapting catalysts by linking microbial parameters to intracellular metabolic resources. From the optimization results, we related microbial parameters to the substrate concentration and the energy available in the environment, and simplified the relationship between the kinetics and the thermodynamics of microbial reactions. We took as examples Methanosarcina and Methanosaeta – the methanogens that produce methane from acetate – and showed how the acclimation model extrapolated laboratory observations to natural environments and improved the simulation of methanogenesis and the dominance of Methanosaeta over Methanosarcina in lake sediments. These results highlight the importance of physiological acclimation in shaping the kinetics and thermodynamics of microbial reactions and in determining the outcome of microbial interactions.