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

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