J Plant Ecol ›› Advance articles     DOI:10.1093/jpe/rtag134

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Canopy nitrogen deposition drives phyllosphere bacterial diversity loss via foliar traits

Yongtao Huang1†, Handan Dai2†, Shenglei Fu1, Yuhua Tan1, Die Li1, Chenlu Zhang1, Xiaowei Li1, Biao Dong1, Xiao Zhang2, 3*   

  1. 1 College of Geographical Science, Faculty of Geographical Science and Engineering, Henan University, Zhengzhou, Henan, 450046, China;
    2 College of Forestry, Northwest A&F University, Yangling, Shaanxi, 712100, China;
    3 Qinling National Forest Research Station, Ningshan, Shaanxi, 711699, China
    These authors have contributed equally to this work and share the first authorship.
    *Correspondence: Xiao Zhang
    Email:zhang_xiao@nwsuaf.edu.cn
  • Received:2026-02-01 Revised:2026-05-09 Accepted:2026-05-24 Published:2026-06-16
  • Supported by:
    This research was supported by the Natural Science Foundation of China (31800375, 32571863, 32071556); the National Key Research and Development Program of China (2024YFF1306501, 2023YFE0112800); the High-Level Innovation and Entrepreneurship Talent Project of Qinchuangyuan (QCYRCXM-2022-347); the High-Level Talents Introduction Plan of Shaanxi Province (F2020124001); and the Chinese Universities Scientific Fund (2452024411). We also thank the High-Performance Computing platform of Northwest A&F University for providing computing resources.

林冠氮沉降通过影响叶片性状导致叶际细菌多样性丧失

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.

Key words: canopy N deposition, understory N deposition, phyllosphere bacterial α/β diversity, rare species, community assembly processes, leaf functional traits

摘要:
阐明大气氮沉降对森林叶际细菌的α和β多样性的影响,对于预测微生物及生态系统对未来环境变化的响应至关重要。然而,以往研究忽略了林冠的截留作用,对氮沉降影响的认识仍然十分有限。为弥补这一知识空白,我们在中国温带森林开展了长达十年的野外实验,比较林冠氮添加(CN)和林下氮添加(UN)的影响,并整合了11项叶际细菌多样性研究(其中大多数关注UN)的数据,进行了系统性的荟萃分析。结合本研究的UN实验结果与荟萃分析表明,林下施氮对叶际细菌α和β多样性的影响甚微。相比之下,林冠施氮则使α多样性显著降低了22%-30%,β多样性显著降低了8%-24%,揭示了过去未被认识到的林冠氮沉降效应。这种差异很可能源于林冠施氮中氮素能直接接触叶片并被吸收,而传统林下施氮方法无法模拟这一过程。从机制上看,林冠氮沉降通过降低比叶面积导致稀有物种丧失,从而减少α多样性;同时通过引起生境同质化、降低群落间的物种周转,削弱β多样性。这些发现提供了扎实的经验证据:植物冠层并非被动屏障,而是氮沉降的主动调控者,从根本上塑造着相关的微生物群落。忽视这一由植物介导的途径,可能会严重低估氮沉降对森林微生物群落的影响。

关键词: 林冠施氮, 林下施氮, 叶际细菌α和β多样性, 稀有种, 群落构建过程, 叶片功能性状