A kinetic modeling approach to the energy metabolism of acetoclastic methanogenesis

Abstract:

Methanogens can consume acetate as an energy resource and conserve energy by chemiosmotic coupling. In both laboratory bioreactors and natural environments, acetoclastic methanogens face a unique challenge, that is the methanogenesis reaction often proceeds close to thermodynamic equlibrium. Despite the recent advance in methaogenesis biochemistry and methanogen genomics, the thermodynamic efficiency of acetoclastic methanogenesis still remains unresolved. Here we apply a kinetic model to simulate acetoclastic methanogenesis of Methanosarcia barkeri. Our model focuses on the enzyme expressions and energy conservation of methanogenesis, and tracks the fluxes of carbon and energy according to enzyme kinetics. Following the current practice of metabolic modeling, we also optimize the expresion levels of the enzymes to maximize the rates of growth. The modeling output includes the enzyme concentrations, the stoichiometry of chemiosmotic coupling and ATP synthesis, and the fluxes through the network of the methanogenesis enzymes, which match with independent laboratory observations that have excluded from the model construction. Among the methanogenesis enzymes, ECH (energy converting hydrogenase) and MTR (Na⁺-translocating methyl-H₄MPT–coenzyme-M-methyltransferase) stand out as the determinant for both the flux and thermodynamic efficiency of methanogenesis. These results link the mechanisms of energy conservation to the macroscopic trade-off between the rate and yield of methanogen growth and, therefore, shed new light on the survial of microrganisms under exterme themrodynamic conditions.