Input of labile carbon may accelerate the decomposition of existing soil organic matter (priming effect), with the priming intensity depending on changes in soil nitrogen availability after permafrost thaw. However, experimental evidence for the linkage between the priming effect and post-thaw nitrogen availability is unavailable. Here we test the hypothesis that elevated nitrogen availability after permafrost collapse inhibits the priming effect by increasing microbial metabolic efficiency based on a combination of thermokarst-induced natural nitrogen gradient and nitrogen addition experiment. We find a negative correlation between the priming intensity and soil total dissolved nitrogen concentration along the thaw sequence. The negative effect is confirmed by the reduced priming effect after nitrogen addition. In contrast to the prevailing view, this nitrogen-regulated priming intensity is independent of extracellular enzyme activities but associated with microbial metabolic efficiency. These findings demonstrate that post-thaw nitrogen availability regulates topsoil carbon dynamics through its modification of microbial metabolic efficiency.

Plant-microbial interactions alter C and N balance in the rhizosphere and affect the microbial carbon use efficiency (CUE)–the fundamental characteristic of microbial metabolism. Estimation of CUE in microbial hotspots with high dynamics of activity and changes of microbial physiological state from dormancy to activity is a challenge in soil microbiology. We analyzed respiratory activity, microbial DNA content and CUE by manipulation the C and nutrients availability in the soil under Beta vulgaris. All measurements were done in root-free and rhizosphere soil under steady-state conditions and during microbial growth induced by addition of glucose. Microorganisms in the rhizosphere and root-free soil differed in their CUE dynamics due to varying time delays between respiration burst and DNA increase. Constant CUE in an exponentially-growing microbial community in rhizosphere demonstrated the balanced growth. In contrast, the CUE in the root-free soil increased more than three times at the end of exponential growth and was 1.5 times higher than in the rhizosphere. Plants alter the dynamics of microbial CUE by balancing the catabolic and anabolic processes, which were decoupled in the root-free soil. The effects of N and C availability on CUE in rhizosphere and root-free soil are discussed.