Bioenergetic Controls on Anaerobic Oxidation of Methane (AOM) in Coastal Marine Sediments: A Theoretical Analysis

Abstract

A kinetic-bioenergetic reaction model for the anaerobic oxidation of methane (AOM) in coastal marine sediments is presented. The model considers a fixed depth interval of sediments below the zone of bioturbation (the window-of-observation), subject to seasonal variations of temperature and inputs of organic substrates and sulfate. It includes (1) nine microbially-mediated reaction pathways involved in CH4 production/consumption; (2) an explicit representation of five functional microbial groups; and (3) bioenergetic limitations of the microbial metabolic pathways. Fermentation of organic substrates is assumed to produce hydrogen (H2) and acetate (Ac) as key reactive intermediates. Competition among the metabolic pathways is controlled by the relative kinetic efficiencies of the various microbial processes and by bioenergetic constraints. Model results imply that the functional microbial biomasses within the window-of-observation undergo little variation over the year, as a result of kinetic and thermodynamic buffering of the seasonal forcings. Furthermore, the microbial processes proceed at only small fractions of their maximum potential rates. These findings provide a theoretical justification for the approximation of steady-state microbial biomasses, which is frequently used in diagenetic modeling. In contrast, AOM rates show a strong seasonal evolution: AOM only becomes spontaneous in winter, when hydrogenotrophic sulfate reduction (hySR) sufficiently reduces the local H2 concentration. The bioenergetic limitation of AOM is thus a critical factor modulating this process in seasonally-forced nearshore marine sediments. A global sensitivity analysis based on a 2-level factorial design reveals that AOM rates are most sensitive to the kinetic parameters describing hySR and acetotrophic methanogenesis (acME). The growth and substrate uptake kinetics of AOM are unimportant, whereas the threshold value of ATP energy conservation for AOM is the most sensitive thermodynamic parameter. These results confirm that anaerobic methane oxidizing microorganisms are metabolizing close to their thermodynamic limit, with the energetic balance being controlled by the relative rates of hySR and acME. The removal of Ac by acME primarily allows more sulfate (SO42−) to be utilized for H2 oxidation, thereby promoting AOM.