Tracking interlinked microbial and geochemical succession over decades in landfilled municipal solid waste.

Landfills are heterogeneous built environments embedded in natural freshwater systems. They pose increasing risks of groundwater contamination from metal-bearing leachates over time. The interlinked succession of waste decomposition processes, microbial community membership, and metal cycling across a landfill's lifespan has not been explored, reducing our ability to predict the long-term environmental impacts of landfills. Working with 1,647 metagenome-assembled genomes from a single landfill, from samples spanning over 39 years of waste decomposition, we identified changes in landfill biogeochemistry and connected these changes to shifts in microbial community composition and predicted functions over time. Comparing Older (aged 31-39 years) and Newer (aged 3-20 years) waste cells identified significant shifts in the availability of labile carbon, redox-associated processes, and concentrations of mobile metals-all higher in Newer cells. Newer cells were dominated by chemoorganoheterotrophs, while Older cells contained higher proportions of chemolithoautotrophs and organisms with higher metabolic versatility. Metal resistance and metal cycling genes were significantly more abundant in Older cells. Using geochemical data from the time of filling to the present and microbial membership data across six landfill cells of different ages, we developed a conceptual model of landfill characteristics across time. This model connects redox conditions and metal fate, highlighting leachate recirculation as a key process impacting many geochemical parameters and defining site chemistry. Our work highlights the substantial changes occurring over the stabilization phase and provides a conceptual model for understanding this critical, final stage in a landfill's life cycle.IMPORTANCEAging landfills pose significant risks to environmental stability and are currently poorly modeled beyond ~20 years. Our examination of a single landfill across 39 years of waste degradation was a unique opportunity to examine the impact of time within a connected system. Our work connects geochemical data, microbial membership, and predicted function, as well as physical processes (e.g., leachate recirculation). Our conceptual model interlinks these facets across the lifespan of a landfill, providing an empirical data-based model of landfill aging. Previous models were extrapolated from younger waste and did not include the microbial dimension-a critical facet of the landfill ecosystem. Our model clarifies processes taking place in older wastes (30+ years), including oxygen infiltration, that have important implications for methane emission and metal mobility and fate over the longer term.