Trade-offs and adaptation to metalliferous soils: The role of soil microbiome in metal tolerance and uptake in Arabidopsis halleri ecotypes from a reciprocal transplant experiment

Soil contamination with trace metal elements is a worldwide issue, prompting research on plant species capable of hyperaccumulating metals to reduce soil toxicity. Previous research suggests that both plant species and their populations can affect soil microbial communities, yet little is known about how different populations of hyperaccumulator species influence these microbial communities to enhance metal-uptake and tolerance. This study evaluated the effect of soil origin, soil microbiome, and plant population on phytoextraction efficiencies of Cd and Zn among four A. halleri populations: two each from metalliferous and non-metalliferous sites. In a controlled transplant experiment, clonal replicates of A. halleri were grown in native and three non-native soils for six months. Biogeochemical analyses of plants and soils were conducted, alongside sequencing of root-associated soil bacterial/archaeal and fungal DNA. Soil treatments primarily differed in pH, total Cd, Pb, and Zn, as well as acid and alkaline phosphatase enzyme activities. A combined effect of soil origin and population was noted for arylsulfatase and β-glucosidase activities, as well as ammonium and nitrate concentrations. Both non-metallicolous and metallicolous populations accumulated high levels of Cd and Zn in metalliferous soils with the non-metallicolous population NM_PL14 outperforming the metallicolous populations in Zn hyperaccumulation. Interestingly, non-metallicolous populations grown in metalliferous soils exhibited no trade-offs in plant performance despite higher Cd and Zn accumulation. Soil origin had a stronger effect on the bacterial/archaeal and fungal community composition than plant ecotype. Partial least square regression models explained 66 % and 79 % of the variability in A. halleri Cd and Zn hyperaccumulation. There was a positive association between Zn-uptake and specific microbial taxa (e.g., Cornebacteriales, Microbacteriaceae, Propionibacteriales, Rhizobiaceae, Basidiomycota, Oidiodendron, Phallaceae) and functional activity (e.g., arylsulfatase, S oxidation) in metalliferous soils. Taken together, our findings suggest that non-metallicolous A. halleri populations may be better suited for Zn phytoextraction applications.