High soil metal contents override climate impacts on biogeochemical dynamics in bulk and rhizosphere soils of a metal-hyperaccumulating plant

Plant roots can modify soil organic matter decomposition, regulating carbon (C) and nitrogen (N) fluxes and storage. Several biotic (e.g., plant species, soil microbiome) and abiotic factors (e.g., nutrient availability, temperature, environmental stressors) can influence the extent of changes in nutrient cycling driven by roots. For instance, metal contamination and climate change can trigger changes in plant and microbial growth and activity, impacting soil biogeochemical processes. Given that future climatic conditions may boost metal mobility in soils and root exudation, the coupling of both disturbances may likely impact nutrient cycling more severely than either single factor. However, little is known about the impacts of coupled climate change and soil contamination on nutrient cycling facilitated by the rhizosphere of a metal hyperaccumulating plant, which is especially relevant in phytoremediation.

To investigate whether and to which extent climate induces modifications of nutrient and metal availability affecting microbiome dynamics and functioning in bulk and rhizosphere soils, we set up a greenhouse pot study with the model metal hyperaccumulating plant Arabidopsis halleri. Three agricultural soils with natural contents of the common non-metabolically useful heavy metal Cd (low 0.2 ppm Cd, medium 1 ppm Cd, and high 14 ppm Cd) were exposed to today’s and future climatic conditions (according to IPCC RCP 8.5: +4º C and +400 ppmv CO₂). 

Future climatic conditions enhanced plant growth in all soils producing between 1.6 to 2.8 times more shoot, with plants growing overall less on the high-Cd soil. Future climatic conditions increased shoot Cd accumulation only in soil with medium-Cd content but not low and high-Cd. Increased organic matter decomposition indicated by higher hydrolytic enzyme activity and N mineralization was found in the low-Cd soil under future conditions. Nevertheless, root activity was the main driver in producing changes in soil nutrient fluxes and metal availability in metal contaminated soils. Overall, increasing metal concentration negatively affected soil carbon microbial biomass and the microbial metabolic quotient; however, the decline was significantly more pronounced in the rhizosphere of medium-Cd and high-Cd soils. In addition, hydrolytic enzyme activities involved in C and N cycling were higher in medium-Cd and high-Cd soils, as well as the plant metal content and metal availability in the rhizospheres. These findings indicate a higher maintenance cost for microorganisms in the rhizosphere of contaminated soils, which may respond to higher nutrient demand from plants and a higher portion of assimilated C allocated to alleviate heavy metal toxicity. As soil metal contamination increased, less microbial N biomass and higher N mineralization were found in the rhizosphere, suggesting an adjustment in microbial activity to plant needs and lower capacity for N immobilization in soils.

We conclude that although climate change can significantly affect overall plant responses and boost organic matter decomposition in soils with low metal content, climate impacts on soil microbial community dynamics and biogeochemical processes are overridden in soils with high metal contents, which trigger higher C and N demand by plant and stressed microorganisms and may imply a decrease in C and N soil storage.