Extracellular enzyme activities response to nitrogen addition in the rhizosphere and bulk soil: A global meta-analysis

Plant roots play a crucial role in acquiring available nutrients and regulating microbial decomposition, leading to faster nutrient cycling in the rhizosphere than in bulk soil. With increasing nitrogen (N) loading, rhizosphere processes may become more crucial than bulk soil processes for accurately predicting nutrient cycling process changes. However, it remains unclear how the rhizosphere and bulk soil extracellular enzyme activities (EEAs) respond to N addition on a global scale. Therefore, we used a global meta-analysis to examine the effects of N addition on EEAs involved in carbon (C), N, and phosphorus (P) acquisition in paired rhizosphere and bulk soils, based on 1992 observations from 40 studies. Overall, N addition significantly increased β-xylosidase (BXYL) activity by 17.0% in bulk soil, together with urease (URE) activity in both the rhizosphere (25.3%) and bulk soil (33.6%). In addition, N addition marginally significantly decreased phenol oxidase (PHEO) activity in the rhizosphere (−18.4%), as well as peroxidase (PERO) activity in both the rhizosphere (−12.6%) and bulk soil (−13.6%). The reductions may be caused by fungi: bacteria ratio and Gram+ bacteria: Gram− bacteria ratio (F: B and G+: G−, respectively) reductions. We also found that EEAs (e.g., acid/alkaline phosphatase (AP) and PHEO) did not always have a simple linear relationship with higher N addition rate and duration. Additionally, the responses of β-1,4-N-acetyl-glucosaminnidase (NAG) and PHEO significantly increased with increase in mean annual temperature (MAT), whereas those of microbial biomass carbon (MBC) and microbial biomass nitrogen (MBN) significantly decreased with increase in mean annual precipitation (MAP). Moreover, the responses of PHEO and PERO significantly decreased along altitudinal gradients. Furthermore, we found that the N sensitivity of rhizosphere C-acquisition (BG, PHEO, and PERO) and P-acquisition (AP) enzyme activities was significantly lower than that of bulk soil, but no significant difference was noted in N-acquisition enzyme activities except for the NAG which exhibited marginal significant differences between the rhizosphere and bulk soil. Our results suggest that EEAs in the rhizosphere and bulk soil have different response patterns, and these differences might mainly be caused by soil nutrient availability and microbial attributes. These results deepen our understanding of rhizosphere and bulk soil nutrient cycling processes under increasing N loading. They also provide extensive evidence and a basis for the parameterization of global nutrient cycling models that incorporate rhizosphere responses to climate change.