While peatlands are freshwater wetlands that make up just 3 percent of the Earth’s landmass, they store about one-third of the planet’s soil carbon as thick peat deposits. Most peatlands are found in cooler wetter regions where the microbial breakdown of organic matter is relatively slow. As global temperatures rise, microbes could break into the peatland carbon bank and the resulting decomposition of the ancient, combustible plant biomass would lead to increased levels of greenhouse gases (carbon dioxide and methane) being released into the atmosphere, accelerating climate change. Our overall goal is to uncover the mechanisms or biochemical pathways by which microbes, plants, and the environment interact to control the various steps in the microbial degradation of soil organic matter in peatlands. In particular, previous work by our team and others indicates that phenolic compounds, produced during the breakdown of lignocellulose found in the cell walls of certain plants, may slow down microbial metabolism of soil organic matter. Understanding the mechanisms and controls of the microbial breakdown of organic matter with respect to the overlying vegetation will allow us to improve predictions of how the peatland soil carbon bank will be affected by climate change. Hypotheses driving the proposed research are: 1) When peat soils are flooded with water, phenolic compounds derived from certain plants act as “bottlenecks” to microbial soil organic matter decomposition by binding and preventing enzymatic attack of organic matter polymers; thus the degradation of these polymers is the rate limiting step in peatland soil organic matter decomposition (referred to as ‘enzyme latch’ mechanism). 2) Since the enzymes that catalyze the breakdown of phenolic compounds are dependent upon oxygen, soil moisture content and oxygen availability largely determine which microbes and biochemical pathways are operative in the degradation of lignocellulose and lignin, thereby regulating soil organic matter storage (the opposite of decomposition) through the ‘enzyme latch’. 3) Climate change, which is expected to warm and dry out peatlands, will release the ‘enzyme latch’ and cause microbes to break into the carbon bank by stimulating the enzymatic decomposition of phenolic compounds and organic polymers. 4) Conversely, changes in plant communities caused by climate change, the replacement of mosses by lignin-rich vascular plants (shrubs), will act to strengthen the ‘enzyme latch’, by preventing microbial decomposition through the accumulation of plant-derived phenolic compounds. Specific research objectives will be to: Task I. Test the ‘enzyme latch’ hypothesis (prevention of soil organic matter decomposition by the accumulation of plant-derived phenolic compounds) in the field. Task II. Test the ‘enzyme latch’ hypothesis and its response to environmental conditions linked to climate change (temperature, redox, water content) under controlled conditions in the laboratory. Task III. Determine the response of the ‘enzyme latch’ to the manipulation of climate conditions (temperature, elevated carbon dioxide levels in the atmosphere) at the whole ecosystem scale. Task IV. Use field and laboratory investigations to improve predictions of future carbon storage and develop quantitative indicators of the microbe-plant-environment interactions that control soil organic matter degradation in peatlands exposed to climate change. Task V. Create a curated, comprehensive, and searchable genome and gene database that documents the microbial populations and processes mediating lignocellulose and lignin degradation in soils on a global scale, along with underlying physico-chemical data, geocoded via GIS to reveal geographic distribution patterns of the populations. Our approach leverages the resources and expertise of the U.S. Department of Energy’s Joint Genome Institute along with the extensive infrastructure and site characterization datasets of DOE’s Spruce and Peatland Responses Under Changing Environments (SPRUCE), located within the Marcell Experimental Forest (MN, USA). At this site, experiments are performed at the ecosystem scale using an experimental design that allows for statistical testing of how environmental conditions impacted by climate change (temperature, elevated atmospheric carbon dioxide, changes to plant communities) alter the flow of organic matter in peatlands.