Long-term tropospheric ozone pollution disrupts plant-microbe-soil interactions in the agroecosystem

Tropospheric ozone (O₃ ) threatens agroecosystems, yet its long-term effects on intricate plant-microbe-soil interactions remain overlooked. This study employed two soybean genotypes of contrasting O₃ -sensitivity grown in field plots exposed elevated O₃ (eO₃ ) and evaluated cause-effect relationships with their associated soil microbiomes and soil quality. Results revealed long-term eO₃ effects on belowground soil microbiomes and soil health surpass damage visible on plants. Elevated O₃ significantly disrupted belowground bacteria-fungi interactions, reduced fungal diversity, and altered fungal community assembly by impacting soybean physiological properties. Particularly, eO₃ impacts on plant performance were significantly associated with arbuscular mycorrhizal fungi, undermining their contribution to plants, whereas eO₃ increased fungal saprotroph proliferation, accelerating soil organic matter decomposition and soil carbon pool depletion. Free-living diazotrophs exhibited remarkable acclimation under eO₃ , improving plant performance by enhancing nitrogen fixation. However, overarching detrimental consequences of eO₃ negated this benefit. Overall, this study demonstrated long-term eO₃ profoundly governed negative impacts on plant-soil-microbiota interactions, pointing to a potential crisis for agroecosystems. These findings highlight urgent needs to develop adaptive strategies to navigate future eO₃ scenarios.