Peat particulate organic matter (POM) in the anoxic subsurface of peatlands is increasingly recognized as an important terminal electron acceptor (TEA) in anaerobic respiration. While POM reduction has been demonstrated in laboratory peat-soil incubations and (electro-) chemical reduction assays, direct demonstration of POM reduction in peat soils under in situ, field conditions involving quantification of transferred electrons remain missing. Herein, we demonstrate that deployment of an oxidized reference POM in the anoxic, methanogenic subsurface of three ombrotrophic bogs, followed by one year incubation, resulted in the transfer of approximately 150–170 μmol of electrons per gram POM to the deployed reference POM. The capacity of this reduced POM to accept electrons was partially restored upon subsequent exposure to dissolved oxygen. These findings provide direct evidence for POM acting as regenerable and sustainable TEA for anaerobic respiration in temporarily anoxic parts of peat soils. Based on the number of electrons transferred to POM and thermodynamic considerations, we estimate that anaerobic respiration to POM may largely suppress methanogenesis in peat soils, particularly close to the oxic-anoxic interface across which POM is expected to undergo redox cycling.

Northern peatlands store approximately 500 Pg carbon in the form of peat particulate organic matter (POM). Ombrotrophic bogs are peatlands that only receive water and nutrients through precipitation, creating anoxic, water-logged soils deprived of inorganic terminal electron acceptors (TEAs). In the absence of suitable TEAs for anaerobic respiration, methanogenesis prevails as final step in the degradation of organic matter and is expected to result in equimolar CO2:CH4 production ratios. However, field and laboratory studies revealed higher CO2:CH4 production ratios than expected based on low concentrations of canonical inorganic TEAs, suggesting the presence of a previously unrecognized TEA used in anaerobic microbial respiration. It has been hypothesized that oxidized particulate organic matter (POMox) functions as TEA, explaining elevated CO2:CH4 production ratios. Through seasonal water table fluctuations, POM gets re-oxidized abiotically, creating a microbial hotspot at the oxic-anoxic interface. To investigate these processes, incubation studies linking CO2 and CH4 production to the reduction of POMox are indispensable. Here, we present data strongly indicating that POM collected from ombrotrophic bogs in Sweden functions as TEA in anaerobic respiration, suppressing methanogenesis. We ran anoxic incubations with various initial ratios of oxidized and reduced POM and hence a range of starting electron accepting capacities, which we quantified using a novel spectrophotometric assay. Increasing contributions of POMox resulted in higher CO2:CH4 production ratios and prolonged transition times from anaerobic respiration to methanogenesis. These findings strongly support the use of POM as TEA, suppressing methanogenesis until POMox was depleted through respiration. Additionally, we developed an incubation system that allowed amending incubations with 13C-labeled substrates to selectively track their conversion to 13CO2 and 13CH4. Using 13C-glucose we successfully linked 13CO2 and 13CH4 formation ratios to POM redox state. Our results advance our understanding of microbial carbon turnover in peatlands in the present and future climate.