How varying natural metal concentrations shape climate change impacts on nutrient cycling in bulk and rhizosphere agricultural soils

Climate change, marked by rising atmospheric CO₂ levels and temperature, can strongly influence soil processes such as nutrient cycling and microbial dynamics. Metals can negatively impact soil functionality, and modify microbial community composition and activity, introducing additional complexity to nutrient cycling under shifting environmental conditions. In addition, metals can disrupt plant growth and nutrient uptake, affect root development and activity, and trigger stress responses, ultimately compromising plant productivity. On the other hand, elevated CO₂ and temperature stimulate plant primary productivity, increasing carbon inputs to the soil through root exudates, litter, and rhizodeposition. Climate-altered root activities influence soil microbial processes, which are critical in regulating nutrient dynamics. While the responses of microbial communities and nutrient cycling processes to climate change are often scenario-dependent, the interplay between soil metal backgrounds and climate drivers remains underexplored.

This study investigates the susceptibility of agricultural soils with varying natural metal levels to climate change, focusing on nutrient cycling processes in both bulk and rhizosphere compartments. By exploring how metal backgrounds influence nutrient availability and transformations, this work aims to shed light on the resilience and vulnerability of these soils under changing environmental conditions. A greenhouse pot study was set up with the plant Arabidopsis halleri, using three agricultural soils with natural contents of cadmium (Cd): low-Cd (0.2 ppm), mid-Cd (1 ppm), and high-Cd (14 ppm). Soils and plants were exposed to today’s and future climatic conditions (according to IPCC SSP3-7: +3.5 ºC and +400 ppm_v CO₂ predicted to 2100 vs. preindustrial times). Soil microbial processes were analyzed by combining stable isotope analysis for tracking N transformations and carbon use efficiency (CUE) with qPCR N functional genes, potential hydrolytic enzyme activities (C, N, P), and the nutrients pools (C, N, P) assessment by colorimetric methods.

Future climatic conditions enhanced plant growth and triggered changes in soil processes in the rhizosphere with minimal fluctuations in bulk soil responses. Under future climatic conditions, rhizosphere nutrient cycling was accelerated by higher organic matter decomposition (boosted enzyme activities and ammonification) at low-Cd soil. The future climate also impacted the rhizosphere response in the mid-Cd soil by reducing CUE and shifting N transformation processes such as nitrate production and consumption rates, ammonification, and denitrification, highlighting higher microbial N demand and stress. High-Cd soils, however, showed resilience to climate change, but this stability was primarily due to the overriding effects of metal toxicity, which impaired microbial responses. Here we demonstrate that the rhizosphere exhibited higher susceptibility to future climatic conditions compared to bulk soil, which can be related to enhanced plant growth demanding more nutrients. Our findings suggest that soil metal contents modulate the resilience and adaptability of soils to climate drivers, with distinct outcomes for nutrient cycling and microbial functionality.