Canopy nitrogen deposition drives phyllosphere bacterial diversity loss via foliar traits

Abstract Elucidating the effects of atmospheric nitrogen deposition on forest phyllosphere bacteria α and β diversity is crucial for predicting microbial and ecosystem responses to future environmental change. However, such impacts remain poorly understood, largely because most previous studies have overlooked canopy interception and processing of deposited N. To address this knowledge gap, we performed a decade-long field study comparing canopy addition of N (CN) with understory addition of N (UN) in a temperate forest in China and conducted a comprehensive meta-analysis compiling data on phyllosphere bacterial diversity from 11 studies (most of which focused on UN). Integrating our UN study with the meta-analysis indicated that UN had minimal effects on phyllosphere bacterial α and β diversity. In contrast, CN significantly reduced α diversity by 22%–30% and β diversity by 8%–24%, highlighting the previously unrecognized role of canopy N deposition. This discrepancy likely reflects the direct foliar contact and uptake involved in CN, which are not captured by conventional UN methodologies. Mechanistically, CN reduces α diversity by causing the loss of rare species through diminished specific leaf area, and diminishes β diversity via homogenizing microhabitats and reducing species turnover among communities. These findings provide robust empirical evidence that the plant canopy is not a passive barrier but an active processor of N deposition, fundamentally shaping associated microbial communities. Neglecting this plant-mediated pathway may substantially underestimate the impacts of N deposition on forest microbiota.