Ozone strengthens the ex vivo but weakens the in vivo pathway of the microbial carbon pump in poplar plantations

Elevated ozone (eO₃) and atmospheric nitrogen (N) deposition are important climate change components that can affect plant growth and plant-soil-microbe interactions. However, the understanding of how eO₃ and its interaction with N deposition affect soil microbially mediated carbon (C) cycling and the fate of soil C stocks is limited. This study aimed to test how eO₃ and N deposition affected soil microbial metrics (i.e., respiration, enzyme activities, biomass, necromass, and community composition) and resulting soil organic C (SOC) fractions in the rhizosphere of poplar plantations with different sensitivity to O₃. Exposure to O₃ and/or N deposition for four years was conducted within a free-air O₃ concentration-enrichment facility. Elevated O₃ reduced soil microbial respiration and biomass C but enhanced the enzymatic acquisition of C (i.e., potential soil hydrolase and oxidase activity) and shifted to a fungi-dominated community composition. These responses suggest that microbial C availability decreased and microbes allocated more energy to obtain C and nutrients from biochemically resistant substrates under eO₃. Elevated O₃ decreased bacterial necromass C and total necromass C, which could explain the observed decreases in mineral-associated organic C and SOC. The effects of eO₃ on soil microbial C availability and community composition were strengthened by N addition, whereas there were no differences in the below-ground effects of eO₃ between the two poplar clones. Taken together, the increased soil extracellular enzyme activities and slightly increased particulate organic C content suggest that the microbial C pump pathway via microbial ex vivo modification was strengthened by eO₃, whereas the pathway via microbial in vivo turnover was weakened, as suggested by the decreases in soil microbial respiration, biomass, necromass, and mineral-associated organic C. Our study provides evidence that aboveground eO₃ effects on trees may affect belowground microbial processing of organic matter and ultimately the persistence of SOC.