Long-term litter decomposition controlled by manganese redox cycling

To the best of our knowledge, one or more authors of this paper were federal employees when contributing to this work. This is the publisher’s final pdf. The published article is copyrighted by National Academy of Sciences and can be found at: http://www.pnas.org/Litter decomposition is a keystone ecosystem process impacting nutrient cycling and productivity, soil properties, and the terrestrial carbon (C) balance, but the factors regulating decomposition rate are still poorly understood. Traditional models assume that the rate is controlled by litter quality, relying on parameters such as lignin content as predictors. However, a strong correlation has been observed between the manganese (Mn) content of litter and decomposition rates across a variety of forest ecosystems. Here, we show that long-term litter decomposition in forest ecosystems is tightly coupled to Mn redox cycling. Over 7 years of litter decomposition, microbial transformation of litter was paralleled by variations in Mn oxidation state and concentration. A detailed chemical imaging analysis of the litter revealed that fungi recruit and redistribute unreactive Mn²⁺ provided by fresh plant litter to produce oxidative Mn³⁺ species at sites of active decay, with Mn eventually accumulating as insoluble Mn³⁺/⁴⁺ oxides. Formation of reactive Mn³⁺ species coincided with the generation of aromatic oxidation products, providing direct proof of the previously posited role of Mn³⁺-based oxidizers in the breakdown of litter. Our results suggest that the litter-decomposing machinery at our coniferous forest site depends on the ability of plants and microbes to supply, accumulate, and regenerate short-lived Mn³⁺ species in the litter layer. This observation indicates that biogeochemical constraints on bioavailability, mobility, and reactivity of Mn in the plant–soil system may have a profound impact on litter decomposition rates