Phylogenetic Conservation of Soil Microbial Responses to Elevated Tropospheric Ozone and Nitrogen Fertilization

Plant primary productivity and crop yields have been reduced due to the doubled level of global tropospheric ozone. Little is known about how elevated ozone affects soil microbial communities in the cropland ecosystem and whether such effects are sensitive to the nitrogen (N) supply. Here, we examined the responses of bacterial and fungal communities in maize soils to elevated ozone (+60 ppb ozone) across different levels of N fertilization (+60, +120, and +240 kg N ha(−1)yr(−1)). The fungal alpha diversity was decreased (P < 0.05), whereas the bacterial alpha diversity displayed no significant change under elevated ozone. Significant (P < 0.05) effects of N fertilization and elevated ozone on both the bacterial and fungal communities were observed. However, no interactive effects between N fertilization and elevated ozone were observed for bacterial and fungal communities (P > 0.1). The bacterial responses to N fertilization as well as the bacterial and fungal responses to elevated ozone were all phylogenetically conserved, showing universal homogeneous selection (homogeneous environmental conditions leading to more similar community structures). In detail, bacterial Alphaproteobacteria, Actinobacteria, and Chloroflexi, as well as fungal Ascomycota, were increased by elevated ozone, whereas bacterial Gammaproteobacteria, Bacteroidetes, and Elusimicrobia, as well as fungal Glomeromycota, were decreased by elevated ozone (P < 0.05). These ozone-responsive phyla were generally correlated (P < 0.05) with plant biomass, plant carbon (C) uptake, and soil dissolved organic C, demonstrating that elevated ozone affects plant-microbe interactions. Our study highlighted that microbial responses to elevated ozone display a phylogenetic clustering pattern, suggesting that response strategies to elevated ozone stress may be phylogenetically conserved ecological traits. IMPORTANCE The interactions of plant and soil microbial communities support plant growth and health. The increasing tropospheric ozone decreases crop biomass and also alters soil microbial communities, but the ways in which crops and their associated soil microbial communities respond to elevated tropospheric ozone are not clear, and it is also obscure whether the interactions between ozone and the commonly applied N fertilization exist. We showed that the microbial responses to both elevated ozone and N fertilization were phylogenetically conserved. However, the microbial communities that responded to N fertilization and elevated ozone were different, and this was further verified by the lack of an interactive effect between N fertilization and elevated ozone. Given that the global tropospheric ozone concentration will continue to increase in the coming decades, the decrease of specific microbial populations caused by elevated ozone would result in the extinction of certain microbial taxa. This ozone-induced effect will further harm crop production, and awareness is urgently needed.