Thermodynamic Limitations on Microbial Respiration Using Ferric Iron as Terminal Electron Acceptor

Floodplain soils are characterized by heterogeneous redox environments that arise in structured porous media due to dynamic hydrological, and resulting biogeochemical, states. These different redox environments are reflected in variations in microbial metabolic pathways of organic matter mineralization. Under oxygen-depleted conditions, microbial respiration is potentially limited by low energetic yields of the reduction of solid phase (particulate) terminal electron acceptors (TEAs). Understanding such thermodynamic limitations is key to assess shifts in microbial respiration pathways in floodplain soils under changing environmental conditions. Here, we assess thermodynamic limitations on microbial respiration under iron-reducing conditions in soils from the Slate and East River floodplains in Colorado, U.S.A. We incubated soils from two sites and from various depths (sampling a gradient in native redox states) under anoxic conditions quantifying CO2 production as a measure of microbial respiration and the reactivity of particulate TEAs in mediated electrochemical reduction as a measure of the energetic yield of TEA reduction. We found that initial rates of CO2 production scaled with particulate TEA reactivity across field sites and soil depths. Ferric iron phases were the main particulate TEA used by microorganisms and the crystallinity of these phases was linked to their redox reactivity: highly reactive minerals were less crystalline than poorly reactive minerals based on Mössbauer spectroscopy. These findings indicate that thermodynamic limitations set by particulate TEAs, at least in part, limited microbial respiration in our soil incubations. This work improves our understanding of the energetic controls on anaerobic microbial respiration and thereby helps to predict changes in microbial respiration in floodplain soils under future climate scenarios and consequences for biogeochemical processes and element cycling.