Opposing effects of aboveground and belowground bacterial diversity on ecosystem multifunctionality under global change

Global changes (e.g. climate warming, nitrogen deposition) are known to alter bacterial diversity in soil and the rhizosphere, but their effects on phyllosphere microbes and above-belowground community linkages remain unclear. Using an 18-year temperate desert steppe experiment, we assessed the impacts of warming and nitrogen addition on bacterial communities occupying plant leaves (both epiphytic and endophytic), rhizosphere soil and bulk soil, and their linkages to ecosystem multifunctionality, defined as the simultaneous provision of functions such as productivity, nutrient cycling and carbon storage. We found that warming and nitrogen addition increased both bacterial richness and Shannon diversity in the leaf epiphytic and endophytic compartments, while decreasing both metrics in the rhizosphere and bulk soil. These contrasting responses were driven by changes in plant biomass, soil pH and inorganic nitrogen content. Furthermore, we found that a significant fraction of amplicon sequence variants (ASVs) and higher-level taxa (e.g. phyla) were shared across compartments, indicating taxonomic overlap among the phyllosphere, rhizosphere soil and bulk soil communities. Bulk soil bacterial diversity was directly associated with the diversity of both rhizosphere soil and phyllosphere microbes, underscoring the role of soil as an important reservoir of bacterial diversity linked to both above- and belowground compartments. Importantly, across all treatments aboveground bacterial diversity was positively associated with ecosystem multifunctionality, while belowground bacterial diversity was negatively associated with ecosystem multifunctionality. These findings emphasize the importance of considering both above- and belowground bacterial communities when predicting grassland ecosystem multifunctionality under global change scenarios.