Nitrogen addition accelerates ecosystem phosphorus cycling at multiple scales in a temperate grassland of Northeast China

Plant phosphorus (P) resorption, mutualistic symbiosis with mycorrhizas, such as arbuscular mycorrhizal fungi (AMF) and soil organic P mineralization are crucial strategies for acquiring sufficient P to meet plant nutrient demand. Which is the main strategy, however, responding to elevated nitrogen (N) addition to alleviate P deficiency caused by N enrichment remains unclear in terrestrial ecosystems. We explored the responses of foliar P resorption of dominate species (Leymus chinensis), soil microbial properties and organic P mineralization to multi-level N addition in a temperate meadow steppe, Northeast China. We found the enhancements in plant biomass, microbial biomass C and N (MBC, MBN), alkaline phosphatase activities (ALP), and phoD gene abundance (main gene coded soil ALP), while the reductions in soil pH, available P, microbial biomass P, and AMF abundance, and no significant responses of foliar P content under simulative N deposition. When the rates exceeded the threshold 10 g N m^-2yr^-1, plants and microbes had little additional responses to N enrichment. Notably, N addition had distinct effects on three plant P acquisition strategies, that no conspicuous increase in P resorption efficiency, reduced dependence on mutualistic with AMF symbiosis and accelerated organic P mineralization. A positive correlation between ALP activity, phoD gene abundance and P mineralization rate suggested increases in phosphatase activities and its functional gene copies play crucial roles in organic P mineralization. Nitrogen addition aggravated P deficiency to the production of plant and microbial biomass, which further accelerated soil organic P mineralization and foliar P resorption. Due to lack of plasticity in P resorption efficiency and reduced dependence on mutualistic with AMF symbiosis, however, the organic P mineralization dominated in P acquisition to meet increased P demand. Furthermore, the increase in ALP activities, activation of phoD genes and decrease in soil pH were the main pathways to accelerate organic P mineralization and consequently alleviated P deficiency caused by anthropogenic N deposition, especially at conditions of N saturation. Our results provide strong evidences that N addition can accelerate the rate of P cycling and mobilize plant P uptake strategies such as soil organic P mineralization and leaf P resorption, which are important to better maintain sustainable ecosystem development in the more fertilized word.

Acknowledgments: This work was supported by the National Key Research and Development Program of China (2016YFC0500602), National Natural Science Foundation of China (31570470, 31870456), the Fundamental Research Funds for the Central Universities (2412018ZD010), and the Program of Introducing Talents of Discipline to Universities (B16011). H.C. acknowledges support from Chinese Scholarship Council (CSC).