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Background: The phyllosphere microbiome is crucial for plant health and ecosystem functioning. While host species play a determining role in shaping the phyllosphere microbiome, host trees of the same species that are subjected to different environmental conditions can still exhibit large degrees of variation in their microbiome diversity and composition. Whether these intra-specific variations in phyllosphere microbiome diversity and composition can be observed over the broader expanse of forest landscapes remains unclear. In this study, we aim to assess the variation in the top canopy phyllosphere bacterial communities between and within host tree species in the temperate European forests, focusing on Fagus sylvatica (European beech) and Picea abies (Norway spruce). Results: We profiled the bacterial diversity, composition, driving factors, and discriminant taxa in the top canopy phyllosphere of 211 trees in two temperate forests, Veluwe National Parks, the Netherlands and Bavarian Forest National Park, Germany. We found the bacterial communities were primarily shaped by host species, and large variation existed within beech and spruce. While we showed that there was a core microbiome in all tree species examined, community composition varied with elevation, tree diameter at breast height, and leaf-specific traits (e.g., chlorophyll and P content). These driving factors of bacterial community composition also correlated with the relative abundance of specific bacterial families. Conclusions: While our results underscored the importance of host species, we demonstrated a substantial range of variation in phyllosphere bacterial diversity and composition within a host species. Drivers of these variations have implications at both the individual host tree level, where the bacterial communities differed based on tree traits, and at the broader forest landscape level, where drivers like certain highly plastic leaf traits can potentially link forest canopy bacterial community variations to forest ecosystem processes. We eventually showed close associations between forest canopy phyllosphere bacterial communities and host trees exist, and the consistent patterns emerging from these associations are critical for host plant functioning. [ABSTRACT FROM AUTHOR]

Aims: The phyllosphere and soil are crucial and distinct microbial spheres in forests, connected through trees that interact with both. As part of the tree's holobiont, these communities are vital to the fitness and evolution of the host. Differences between the spheres may be particularly evident at the two extreme ends of tall and long-lived trees of natural temperate forest; the top-canopy and the soil. Here, we evaluated the connectivity between the top-canopy and soil microbial communities of European beech and Norway spruce trees to determine the significance of tree-sphere and host-species identity, and to assess the contribution of taxa inhabiting both spheres. Methods: Bacterial and fungal community composition was determined through metabarcoding analysis of linked top-canopy leaf and bulk soil samples collected from tall (old) trees in the natural forest of Bavarian Forest National Park. Results: This study shows sphere-specific communities in European temperate forests, characterized by low connectivity. Results highlight that spheres exert stronger influence than host identity. Only a few taxa inhabited both spheres, yet they accounted for the bulk of the (relative) abundance in each sphere. Conclusion: Analysing the divergence and shared characteristics of these interlinked communities redefines the tree holobiont concept and enhances our understanding of the evolution of plant-associated microbial communities in a sphere-specific manner. This study emphasizes the importance of examining multiple microbiome components for a thorough understanding of temperate forest ecology, while also highlighting the existence of a small group of overlapping taxa that may play a bigger role than previously anticipated. [ABSTRACT FROM AUTHOR]