Hydrological Perturbations Facilitated Phyllosphere Denitrification of an Urban Greening Tree

In urban ecosystems, nutrient stocks, such as carbon (C), nitrogen (N), and phosphorus (P), are anthropogenically being enriched for material and energy supply. The overloaded nutrients have adverse ecological consequences, such as causing eutrophication of waters and soil in urban areas. Studying the ecophysiology of nutrient-cycling microbes in urban areas is the foundation to explore strategies for removing such excessive nutrients. The phyllosphere is an understudied microbial habitat for examining how the urban microbiome responds to common environmental changes, such as hydrological perturbations. Here, we investigated how successive rainy–sunny cycles within a season affect the genetic potential (gene abundances) for leaf nutrient cycling and particularly the functional potential (enzyme activities) for leaf denitrification of the greening tree Photinia fraseri. Of 41 detected C, N, P, and sulfur (S) cycling genes using high-throughput quantitative polymerase chain reaction, rainfalls only significantly (p < 0.05) increased the abundances of denitrification marker genes nirK and nirS and one C-fixation gene on the phyllosphere while having no significant impacts on other nutrient-cycling genes. The nirK and nirS genes encode nitrite reductases, which catalyze the hallmark step of the denitrification process. Further, a denitrification enzyme activity assay of phyllosphere microbiota showed that, in comparison to sunny weather, rainfalls significantly promoted nitrate reduction (5.48 μmol of NO3– g–1 h–1; p < 0.001) and N2O production (2.07 nmol of N2O g–1 h–1; p < 0.05) rates, respectively. Together, this study revealed that hydrological perturbations can affect tree phyllosphere denitrification. Understating the ecophysiology of urban phyllosphere denitrifying microbes might be important for developing suitable phylloremediation strategies to attenuate urban N inputs.