Climate change vs. Cd: Which one has a stronger impact on nitrogen cycling in soils under phytoremediation?

Soil cadmium (Cd) contamination is a widespread problem in Europe, disrupting plant growth, impairing microbial activity, and threatening human health. Phytoextraction using metal hyperaccumulating plants, like Arabidopsis halleri, offers a sustainable approach to mitigate Cd pollution in soils. However, the supply of essential nutrients for plant growth and metal hyperaccumulation is crucial for an efficient application of phytoremediation. Nitrogen (N), a key nutrient undergoing diverse microbially driven transformations in soil, is critical in this context. In addition to Cd contamination, climate change poses an emerging challenge to ecosystem nutrient cycling. While the individual effects of climate change and Cd on soil N-cycling have been studied before, their coupled impacts remain largely unexplored. Thus, this study aims to evaluate the coupled impacts of Cd and climate change on N-cycling in soils under phytoremediation with the metal hyperaccumulating plant A. halleri.

A controlled greenhouse pot experiment was conducted with A. halleri grown in three soils varying naturally in Cd levels under current and future climate conditions, simulated through elevated carbon dioxide concentrations and temperatures reflecting the IPCC SSP3-7 scenario (+3.5 ºC and +400 ppm_v CO₂ predicted to 2100 vs. preindustrial times). Rhizosphere and bulk soil samples were analyzed for metal concentrations, N-pools, and N-cycling functional gene abundances (nifH, chiA, amoA, nirK, nirS, nosZ).

No significant climate effects were found on N-dynamics, with Cd being the dominant factor influencing changes in soil N-cycling. Thus, Cd effects overrode climate effects on soil N-cycling. By stimulating N-mineralization and nitrification but decreasing the denitrification capacity, Cd shifted soil N-cycling towards nitrate. This shift may reflect an increased plant and microbial N-demand for metal detoxification. Furthermore, the higher abundance of the amoA gene of ammonia-oxidizing archaea (AOA) compared to ammonia-oxidizing bacteria (AOB) under Cd stress suggests that archaea, rather than bacteria, dominate nitrification in contaminated soils. A shift in gene abundances in NO₂^- reduction (nirK vs. nirS) was also observed, suggesting a selective advantage for nirK-carrying microorganisms under metal stress. Redundancy analysis revealed that the abundances of N-cycling functional genes were primarily driven by leucine aminopeptidase activity, microbial biomass N, and dissolved organic N, emphasizing the role of soil organic matter degradation and N-mineralization in microbial N-cycling. Understanding the complex interactions between plants, microbes, and N-cycling process under metal stress is crucial for optimizing phytoremediation strategies and promoting sustainable soil management.