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Impacts of MEtal and CLImate change on NUTrient cycling in the rhizosphere of phytoremediating plants

Periodic Reporting for period 1 - NUTCLIME (Impacts of MEtal and CLImate change on NUTrient cycling in the rhizosphere of phytoremediating plants)

Reporting period: 2022-10-01 to 2024-09-30

Metal pollution in soils remains a significant environmental challenge with far-reaching implications for human health, food security, and ecosystem stability. Heavy metals, such as cadmium (Cd), zinc (Zn), and lead (Pb), are present in soils due to natural processes like the weathering of metal-rich rocks. However, human activities—including mining, industrial emissions, and the use of fertilizers and pesticides—are the primary contributors to soil contamination, releasing toxic metals at unprecedented levels. Metal contamination not only reduces crop yield and food nutritional quality but also poses a significant risk to public health, as toxic metals can enter food and water supplies. The availability and mobility of these metals in soil depend on several factors, including soil pH, organic matter content, redox potential, and microbial activity. These interactions are further influenced by climate change, which alters soil processes and metal dynamics through shifts in temperature, moisture, and plant-soil interactions.

Despite advances in remediation strategies, such as phytoremediation using metal-accumulating plants, the combined effects of metal contamination and climate change on nutrient cycling, soil microbial communities, and plant growth remain poorly understood. This knowledge gap limits the development of effective, sustainable solutions for managing contaminated soils under changing environmental conditions. To address this gap, the project aimed to investigate the interplay between metal contamination, climate change, and rhizosphere processes in soils. Specifically, it focused on understanding how these factors influence nutrient cycling, microbial dynamics, and plant-soil interactions, using the hyperaccumulator plant Arabidopsis halleri as a model system. By integrating innovative methodologies, including advanced imaging techniques and molecular analyses, the project aimed to provide new insights for improving soil health, advancing phytoremediation, and ensuring agricultural sustainability under future climate scenarios.
The research was structured into three key work packages (WPs), each addressing specific aspects of plant-soil-microbe interactions and nutrient cycling.

WP1: Assessment of nutrient dynamics. A controlled greenhouse experiment was conducted to study the combined effects of metal contamination and climate change on plant growth, nutrient dynamics, and microbial activity. Experimental soils with low, medium, and high metal content were subjected to current and future climate scenarios (RCP 8.5 IPCC 2021). Advanced techniques such as isotope pool dilution assays, enzymatic activity, and microbial metabolic determinations were implemented to assess biogeochemical processes. The results showed future climatic conditions enhanced plant growth and Cd accumulation, particularly in moderately contaminated soils. Though climate change increased organic matter decomposition in low-metal soils, this was not observed in soils with increased metal levels. This indicated that climate change effects on microbial dynamics and biogeochemical processes were overridden in soils with increased metal levels. Metal contamination significantly reduced the microbial biomass and decreased the soil nutrient storage capacity. The microbial metabolism in the rhizosphere increased to meet plant nutrient demands at higher metal levels in soils at the expense of a higher maintenance cost (stress) for microorganisms. Importantly, the results suggested that phytoremediation efficiency could improve under future climatic conditions, particularly in soils with moderate metal contamination.

WP2: Spatial distribution of enzymes, nutrients and metals. To understand the spatial distribution of enzymatic activity in the rhizosphere, advanced imagining techniques such as zymography and planar optodes were used to visualize microbial activity and pH gradients around roots. Micro-XRF mapping further revealed the spatial distribution of metals in the rhizosphere. Soil areas of particularly high and low microbial activity were sampled to evaluate nutrient and metal fluxes, enzyme kinetics, and microbial community. Enzymatic activity mapping showed that β-glucosidase (indicative of microbial carbon decomposition) activity was concentrated near roots, while acid phosphatase (indicative of phosphorus acquisition) was more uniformly distributed throughout the soil-plant system. Future climatic conditions enhanced enzymatic activity in contaminated soils, suggesting increased nutrient mobilization under metal stress. Zn clustering around roots was more pronounced under future climatic conditions, likely due to increased plant demand for water. Roots with higher Zn storage exhibited reduced enzymatic activity, highlighting a trade-off between metal storage and nutrient acquisition. A spin-off experiment was conducted to explore oxidative enzyme activity, further expanding the scope of the project and resulting in additional insights into microbial functional responses.

WP3: Active and total microbial community composition. The microbial community composition, both active and total, was studied using amplicon sequencing. Nitrogen functional genes were quantified to assess nitrogen cycling dynamics under different metal contamination levels and climatic conditions. Soil metal content and root activity were the primary drivers of microbial diversity and community composition. Active microbial diversity decreased at higher metal concentrations in soils, with a larger portion of the microbial community remaining dormant. Nitrogen cycling pathways shifted with increased metal levels, favoring nitrate accumulation in high-metal soils, which could enhance plant nitrogen availability but increase the risk of nitrate leaching.
Overall, NUTCLIME advanced our understanding of phytoremediation potential under future climatic scenarios and the interactions between nutrient fluxes, microbial communities, and soil metal content in phytoremediation systems. The outcomes of this project will contribute significantly to optimizing phytoremediation strategies, enabling better prediction and management of nutrient fluxes in contaminated environments. This project also provides fundamental mechanistic knowledge on which future field-scale research can be conducted to further test and implement the findings. The delivered actionable insights will also aid agencies and research institutes working on designing sustainable soil remediation practices, food security, and mitigating environmental pollution in agricultural and urban systems. Scientific papers, conference presentations, public outreach, networking, open data management, and other knowledge transfer activities have ensured the exploitation and dissemination of the results and their accessibility to the broader scientific community, which will facilitate future research efforts.
Experiments and advanced imaging methods