Rhizosphere Microbial Community Composition Affects Cadmium and Zinc Uptake by the Metal-Hyperaccumulating Plant Arabidopsis halleri

Abstract

The remediation of metal-contaminated soils by phytoextraction depends on plant growth and plant metal accessibility. Soil microorganisms can affect the accumulation of metals by plants either by directly or indirectly stimulating plant growth and activity or by (im)mobilizing and/or complexing metals. Understanding the intricate interplay of metal-accumulating plants with their rhizosphere microbiome is an important step toward the application and optimization of phytoremediation. We compared the effects of a "native" and a strongly disturbed (gamma-irradiated) soil microbial communities on cadmium and zinc accumulation by the plant Arabidopsis halleri in soil microcosm experiments. A. halleri accumulated 100% more cadmium and 15% more zinc when grown on the untreated than on the gamma-irradiated soil. Gamma irradiation affected neither plant growth nor the 1 M HCl-extractable metal content of the soil. However, it strongly altered the soil microbial community composition and overall cell numbers. Pyrosequencing of 16S rRNA gene amplicons of DNA extracted from rhizosphere samples of A. halleri identified microbial taxa (Lysobacter, Streptomyces, Agromyces, Nitrospira, "Candidatus Chloracidobacterium") of higher relative sequence abundance in the rhizospheres of A. halleri plants grown on untreated than on gamma-irradiated soil, leading to hypotheses on their potential effect on plant metal uptake. However, further experimental evidence is required, and wherefore we discuss different mechanisms of interaction of A. halleri with its rhizosphere microbiome that might have directly or indirectly affected plant metal accumulation. Deciphering the complex interactions between A. halleri and individual microbial taxa will help to further develop soil metal phytoextraction as an efficient and sustainable remediation strategy. E levated metal concentrations in agricultural soils decrease the yield and quality of crops. One of these metals is cadmium (Cd), which is present in the waste materials and waters of many industries (1) and in phosphate fertilizers used in agriculture (2, 3). Besides causing a decrease in crop yield (4), Cd is also a risk to human health if larger quantities (Ͼ2.5 g kg Ϫ1 body weight week Ϫ1 , according to the EFSA [5]) are consumed (6-8). To preserve crop yield and quality, sustainable biotechnologies are urgently needed to relieve agricultural soils of metal contaminants. One promising soil remediation technology is phytoremediation-the use of plants for removing inorganic and organic contaminants from soils (9-11). Phytoremediation is attractive, as it is sustainable and relatively inexpensive compared to other soil cleanup strategies. So far, it has rarely been employed on the field scale (12) due to its low efficiency, slow progress, and the need to develop individual implementation strategies depending on the field site conditions and plant type.Arabidopsis halleri has been studied as a model plant for Cd as well as zinc (Zn) hyperaccumulation in order to apply the plant for phytoremediati...

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