Invasive plant competitivity is mediated by nitrogen use strategies and rhizosphere microbiome

Invasive plants disrupt native biodiversity and ecosystem functions and their distribution increase with ongoing global land-use changes. Clarifying plant nitrogen (N) uptake and use strategies mediated by rhizosphere microbes is key to understand the success of plant invasion. We used 15N labeling to assess the N uptake rate and N use efficiency (NUE) of four invasive species and their native congeners growing either alone (without competition) or pairwise (interspecific competition). Functional gene abundance and enzyme activities in the soil were linked to the richness and community composition of rhizosphere bacteria. Without competition, invasive plants have larger biomass (∼40%) and NUE (∼68%) than native plants, but the native plants had a faster NO3− uptake rate (∼10%) than invasive plants. Interspecific competition decreases the plant biomass but increases the NUE of both invasive and native plants and increases the NH4+ and NO3− uptake by invasive plants. Consequently, invasive plants produce more biomass due to their stronger competitive ability (higher Relative Competition Index) and faster NH4+ uptake rate than the native plants. Invasive plants have a larger microbial biomass, higher activity of β-D-cellobiosidase, faster nitrification, denitrification, and nitrogenase activity, and higher abundances of nifH, nirS, and nosZ genes than native plants when growing pairwise. Competition leads to the enrichment in a set of OTUs in the rhizosphere of invasive and native plants compared with those grown alone, and the enrichment of another set in invasive compared with native plants grown together. Structural Equation Models showed that the plant biomass, N uptake rate, and NUE are influenced by rhizosphere bacteria via the acceleration of N transformation in the soil. We conclude that the competitive advantage of invasive plants is achieved by fast NH4+ uptake, rather than by strengthening NUE as would be the case in the absence of competition. These findings provide important insights into the critical mechanisms of plant N uptake during invasion by alien plants.