Microbial Preference for Soil Organic Carbon Changes Along Redox Gradients as a Function of the Energetic Cost of Respiration

Soil organic carbon (SOC) chemistry is known to impact carbon preservation via mineral associations and physical protection, which chemically or physically block SOC from microbial enzymatic access for decomposition. However, SOC decay models that include these processes do not reliably predict SOC dynamics. We propose that the energetics of respiration additionally regulate SOC cycling. Specifically, organic carbon will only be respired if the available electron acceptors yield enough energy for microbial growth when metabolically coupled to the SOC. To test this hypothesis, we constructed dual pore domain reactors in which water flows normal to a column of packed soil, allowing oxygen to diffuse from the upper channel through the soil and establish a redox gradient. With increasing depth into the soil column, the soil experiences a typical redox profile indicative of anaerobic respiration processes: after oxygen is consumed, nitrate, Mn, Fe, and sulfate serve as electron acceptors. We measure porewater and effluent for nitrate, sulfate, Fe(II) and Mn(II) and take microsensor profiles of dissolved oxygen and H2S to characterize the redox gradient and respiration pathways. To this we couple incubations of solid material at each depth post-experiment and quantify CO2 and CH4 production to assess respiration potential along the redox gradient. Porewater SOC chemistry is analyzed via spectroscopy and mass spectrometry to interpret SOC oxidation state and composition and thus test thermodynamic predictions on SOC stability given the available redox acceptors at a given depth in the reactor. Within 0.5 cm of the soil surface, oxygen concentrations drop below detection and signs of anaerobic respiration (Fe(II) production, loss of nitrate) initiate while respiration rates drops precipitously. More oxidized SOC is preferentially utilized with progression along the redox gradient, supporting thermodynamic predictions. This work highlights the potential of SOC chemistry within specific redox metabolic zones of soils and sediments to drive carbon utilization. An improved understanding on organic carbon utliization is critical to predict SOC dynamics under changing hydrology (e.g. saltwater intrusion, permafrost melting), temperature, and other factors impacting microbial respiration energetics.