The Origin, Succession, and Predicted Metabolism of Bacterial Communities Associated with Leaf Decomposition

Intraspecific variation in plant nutrient and defensive traits can regulate ecosystem-level processes, such as decomposition and transformation of plant carbon and nutrients. Understanding the regulatory mechanisms of ecosystem functions at local scales may facilitate predictions of the resistance and resilience of these functions to change. We evaluated how riverine bacterial community assembly and predicted gene content corresponded to decomposition rates of green leaf inputs from red alder trees into rivers of Washington State, USA. Previously, we documented accelerated decomposition rates for leaves originating from trees growing adjacent to the site of decomposition versus more distant locales, suggesting that microbes have a "home-field advantage" in decomposing local leaves. Here, we identified repeatable stages of bacterial succession, each defined by dominant taxa with predicted gene content associated with metabolic pathways relevant to the leaf characteristics and course of decomposition. "Home" leaves contained bacterial communities with distinct functional capacities to degrade aromatic compounds. Given known spatial variation of alder aromatics, this finding helps explain locally accelerated decomposition. Bacterial decomposer communities adjust to intraspecific variation in leaves at spatial scales of less than a kilometer, providing a mechanism for rapid response to changes in resources such as range shifts among plant genotypes. Such rapid responses among bacterial communities in turn may maintain high rates of carbon and nutrient cycling through aquatic ecosystems.IMPORTANCE Community ecologists have traditionally treated individuals within a species as uniform, with individual-level biodiversity rarely considered as a regulator of community and ecosystem function. In our study system, we have documented clear evidence of within-species variation causing local ecosystem adaptation to fluxes across ecosystem boundaries. In this striking pattern of a "home-field advantage," leaves from individual trees tend to decompose most rapidly when immediately adjacent to their parent tree. Here, we merge community ecology experiments with microbiome approaches to describe how bacterial communities adjust to within-species variation in leaves over spatial scales of less than a kilometer. The results show that bacterial community compositional changes facilitate rapid ecosystem responses to environmental change, effectively maintaining high rates of carbon and nutrient cycling through ecosystems.