4.8 Article

Long-term litter decomposition controlled by manganese redox cycling

Publisher

NATL ACAD SCIENCES
DOI: 10.1073/pnas.1508945112

Keywords

terrestrial carbon cycle; nutrient cycling; forest soil ecosystems; soil-atmosphere interactions; climate change

Funding

  1. Lawrence Livermore National Laboratory (LLNL)
  2. National Science Foundation [DEB-0823380]
  3. US Department of Energy (DOE) by LLNL [DE-AC52-07NA27344]
  4. LLNL Laboratory Directed Research and Development Award Microbes and Minerals: Imaging C Stabilization [10-ERD-021]
  5. Lawrence Berkeley National Laboratory Award from LLNL [IC006762]
  6. DOE-Biological and Environmental Research Sustainable Systems scientific focus area
  7. Institute of Soil Landscape Research at the Zentrum fur Agrarlandschaftsforschung
  8. Office of Science, Office of Basic Energy Sciences, US DOE [DE-AC02-05CH11231]
  9. US Department of Energy, Office of Science, Office of Basic Energy Sciences [DE-AC02-76SF00515]

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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.

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