Long-term litter decomposition controlled by manganese redox cycling

Abstract

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 Mn 2+ provided by fresh plant litter to produce oxidative Mn 3+ species at sites of active decay, with Mn eventually accumulating as insoluble Mn 3+/4+ oxides. Formation of reactive Mn 3+ species coincided with the generation of aromatic oxidation products, providing direct proof of the previously posited role of Mn 3+ -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 Mn 3+ 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.terrestrial carbon cycle | nutrient cycling | forest soil ecosystems | soil-atmosphere interactions | climate change D ecomposition of above-ground plant detritus (litter) is a fundamental process regulating the release of nutrients for plant growth and the formation of soil organic matter (SOM) in forest ecosystems (1). Litter decomposition regulates the proportion of litter-derived carbon (C) that is either retained in the system as SOM or lost as CO 2 (2), thereby influencing net C storage in soils. Although even small decomposition rate increases may accelerate climate change by virtue of increasing CO 2 emissions from soils (3), uncertainty persists over the ratecontrolling mechanisms (4, 5).Litter decomposition rates are strongly influenced by climatic factors (e.g., temperature and moisture) and have long been linked to litter chemistry, specifically lignin content (6). Ligninan aromatic biopolymer-often makes up between 15% and 40% of the litter mass and is concentrated in cell walls (7). It encrusts cellulose microfibrils to form protective physical units ("ligno-cellulose complexes") that are embedded in a matrix of hemicellulose. Conventional thinking suggests that the relatively high initial litter decomposition rates are due to the preferential use of soluble and readily accessible polysaccharides and hemicelluloses relative to lignin components. In later stages, decompositi...

Soil Respiration Components and their Temperature Sensitivity Under Chemical Fertilizer and Compost Application: The Role of Nitrogen Supply and Compost Substrate Quality

“…Similarly, Klotzbücher et al () observed a sharp decrease of lignin content in decomposing litter after ~80 days of decomposition. In fact, lignin is usually degraded via cometabolism in the presence of enough available C because the production of ligninolytic enzymes is highly energy and C demanding (Keiluweit et al, ; Klotzbücher et al, ). Hence, the decomposition of lignin, mainly the most easily degraded cinnamyl units (Bahri et al, ; Baumann et al, ), was likely to have occurred during the initial 2 months and made contribution to Rh flux, especially in BPFS.…”

Understanding the dominant controls on litter decomposition

“…Keiluweit et al . ) and it is feasible that decomposer microorganisms exert control independent of climate and litter quality (Strickland et al . ; McGuire & Treseder ; Keiser et al .…”

Long-Term (13 Years) Decomposition Rates of Forest Floor Organic Matter on Paired Coniferous and Deciduous Watersheds with Contrasting Temperature Regimes

“…Mn concentrations in the litter of the two deciduous watersheds averaged 1.1 mg/g for litter and 1.7 mg/g for humus [24]. Mn concentrations may be critical for Mn dependent lignin and humic acid peroxidation [30,31]. The range in the deciduous litter and humus was intermediate compared to the ranges of most concentrations of the litter in the late stages of decomposition in the study of Berg et al (1-2 mg/g) which showed a relationship with mass loss in the later stages of decomposition [30].…”