Modeling the controls on microbial iron and manganese reduction in methanic sediments

Microbial iron and manganese respiration processes have been observed in deep methanic sediments of lacustrine and marine environments, challenging the “classical” model of microbial respiration in aquatic systems. Nonetheless, assessments of the type and relative role of these respiration processes in the methanic zone are lacking. Here, we quantify both the thermodynamic and the kinetic controls of potential iron and manganese respiration processes in the diffusive controlled steady state methanic sediments of lacustrine and marine sites – Lake Kinneret (LK) and the Southeastern Mediterranean Sea (MedS). We consider the substrates (electron donors) and iron and manganese oxides (electron acceptors) at concentrations that have been measured at these sites. Using theoretical bioenergetic methods, we develop a nominal model to calculate catabolic rates, considering both kinetic and thermodynamic parameters. Then, we estimate the biomass growth rates from the catabolic rates, the energy generated in each reduction–oxidation (redox) reaction, the biomass yield from a given amount of energy, the number of cells participating in each reaction, and the energetic needs of the cells. Lastly, we estimate the microbial community sizes of expected iron and manganese reducers. Additionally, we perform a Monte Carlo simulation to account for variations in uncertain parameter values, along with a sensitivity analysis. Together, these calculations enable estimation of the expected total reaction rates of the various metabolic processes.

Our results indicate that the type of iron or manganese oxide, which determines its thermodynamic and kinetic properties, is more significant in influencing bioreaction rates than its concentration. Thus, bioreactions with amorphous manganese oxides are more favorable than those with highly reactive iron oxides. Among the iron oxides, the reduction of amorphous iron oxyhydroxide and ferrihydrite are the only reactions capable of generating biomass in the methanic sediments at both sites. In both environments, manganese oxide reduction by ammonium and methane oxidation are expected to be significant, while manganese oxide reduction by hydrogen and acetate oxidation are expected to be considerable only in LK. The most probable iron oxide reduction process in LK is hydrogen oxidation, followed by methane oxidation. In the MedS iron oxide reduction is most probably coupled to the oxidation of ammonium (Feammox) to molecular nitrogen (N₂), and in a few cases may be coupled to methane oxidation. The Monte Carlo simulation agrees with the nominal model results for manganese reduction, and additionally predicts that iron reduction may be possible with some combinations of parameter values. These findings improve our understanding of the thermodynamic and kinetic controls on the composition of microbial communities and their effect on the geochemistry of methanic sediments.