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Impact of Root-Induced Mobilization of Zinc on Stable Zn Isotope Variation in the Soil−Plant System David Houben,*,†,‡ Philippe Sonnet,† Guillaume Tricot,† Nadine Mattielli,§ Eléonore Couder,§ and Sophie Opfergelt† †

Earth and Life Institute, Université catholique de Louvain, Croix du Sud 2/L7.05.10, 1348 Louvain-la-Neuve, Belgium HydrISE, Institut Polytechnique LaSalle Beauvais, rue Pierre Waguet 19, 60026 Beauvais Cedex, France § Laboratoire G-Time (Geochemistry: Tracing by Isotopes, Minerals and Elements), Université Libre de Bruxelles, CP 160-02, 50, Avenue FD Roosevelt, 1050 Brussels, Belgium ‡

S Supporting Information *

ABSTRACT: Stable Zn isotopes are increasingly used to trace the source of metal pollution in the environment and to gain a better understanding of the biogeochemical cycle of Zn. In this work, we investigated the effect of plants on Zn isotope fractionation in the soil−plant system of the surface horizon of two Zn-rich Technosols (pH 6.73−7.51, total Zn concentration = 9470−56600 mg kg−1). In a column experiment, the presence of Agrostis capillaris L. significantly increased the mobilization of Zn from soil to leachate, predominantly as a result of root-induced soil acidification. The zinc isotope compositions of plants and leachates indicated that the Zn uptake by A. capillaris did not fractionate Zn isotopes as compared to the leachates. Within the plant, heavier Zn isotopes were preferentially retained in roots (Δ66Znroot − shoot = +0.24 to +0.40 ‰). More importantly, the Zn released in leachates due to root-induced mobilization was isotopically heavier than the Zn released in the absence of plants (Δ66Zn = +0.16 to +0.18 ‰). This indicates that the rhizosphere activity of A. capillaris mobilized Zn from another pool than the one that spontaneously releases Zn upon contact with the percolating solution. Mobilization of Zn by the roots might thus exert a stronger influence on the Zn isotope composition in the soil solution than the Zn uptake by the plant. This study highlights the key role of the rhizosphere activity in Zn release in soil and demonstrates that stable Zn isotopes provide a useful proxy for the detection of Zn mobilization in soil−plant systems.

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INTRODUCTION

interactions with soil and subsequent control of Zn release is thus required to fully assess the biogeochemistry of Zn and the ecological risks associated with its presence in soils. Stable Zn isotopes provide new insights into the biotic and abiotic processes that control Zn release from Earth’s critical zone.14 Recently, a number of studies have investigated Zn isotopes as potential tracers for Zn fluxes in the anthroposphere.15,16 Black et al.17 suggested that Zn leaching from industrial sites could lead to the observed heavy isotopic signature in rivers downstream of the contamination source, the magnitude of which would be dependent on the source material and on the aqueous species of Zn. According to Borrok et al.,18 the relative abundance of Zn isotopes in natural waters can be used to probe biogeochemical reactions and to fingerprint and track sources of Zn. However, an understanding of Zn isotope

Zinc is a metal that plays a dual role in the environment. For most living organisms, Zn is a vital micronutrient, notably because it acts as a key element in the structure of all six enzyme classes.1 In contrast, an excess of Zn causes deleterious effects on organisms. For instance, high levels of Zn in soil inhibit many plant metabolic functions, result in retarded plant growth, and cause senescence.2 Although Zn deficiency is the most common crop micronutrient deficiency,3 numerous soils have been contaminated by Zn worldwide. Large Zn inputs to soil are caused, for instance, by atmospheric emission fallouts4 or by deposition of pyrometallurgical wastes, such as slag, which often have a high residual Zn content.5 There is increasing evidence that plant-induced chemical changes can dramatically alter the release of metals in soils,6−8 even though studies have shown divergent results. For instance, in column experiments, where the soil solution was collected at the bottom of the column9−11 or at various depths12,13 using suction cups, plants were found to both mobilize and immobilize Zn. A comprehensive understanding of plant © 2014 American Chemical Society

Received: Revised: Accepted: Published: 7866

January 17, 2014 June 16, 2014 June 23, 2014 June 23, 2014 dx.doi.org/10.1021/es5002874 | Environ. Sci. Technol. 2014, 48, 7866−7873

Environmental Science & Technology

Article

variations in the environment depends on the determination of Zn isotope ratios in the various compartments and materials on Earth and on the isotope fractionations associated with biogeochemical processes that drive the Zn speciation in the environment.19 Because biogeochemical processes are important mechanisms that affect isotope fractionation during Zn cycling in the environment,20 they need to be carefully assessed before Zn isotopes can be used for the identification of Zn sources.21,22 In particular, plant uptake has been recognized as a key process affecting Zn isotopes during the Zn biogeochemical cycle. During Zn plant uptake, the enrichment of heavy Zn isotopes in the roots compared to the nutrient solution and the depletion of heavy Zn isotopes in the shoots compared to the roots have been reported.23−25 Arnold et al.26 observed heavy Zn isotope enrichment in rice genotypes relative to the plantavailable Zn. This observation was explained by the preferential complexation of heavy Zn isotopes by phytosiderophores released by roots and the subsequent uptake of this complex. However, thus far, the understanding of the mechanisms controlling Zn isotope variations that are associated with plant uptake is still limited.27 Existing studies on the effects of plants on Zn isotopes generally consider only plant uptake, disregarding additional plant effects such as root-induced Zn mobilization.8 In the present study, a column experiment was conducted to gain better insight into the effects of plants on the isotope composition of Zn released from the soil−plant system. By considering both plant uptake and root mobilization of Zn, the experimental setup aimed at better constraining the mechanisms that control plant-induced Zn isotope variations. Agrostis capillaris L. (= A. tenuis Sibth.) was chosen as the model plant because it is a metal-tolerant plant that can, in a temperate climate, successfully cover any Pb-/Zn-contaminated soil and metallurgical or mining waste disposal site, irrespective of whether it is calcareous or acidic.28,29

The study soil was collected from the A horizon of a sandy loam slag-derived Technosol located in a bare area. Collection and Characterization of Soil Samples. A composite bulk (20 kg) surface soil sample (0−10 cm) was collected in each site, by mixing subsamples taken according to a random design. After homogenization and 2 weeks of airdrying in the laboratory, the soil was crushed and dry sieved to a particle size between 100 and 500 μm. The relative percentage (by weight) of this fraction within the fine earth (0−2 mm) was about 45% for both soils. All experiments in this study were conducted on the 100−500-μm fraction, for which selected properties and mineralogy are given in Tables S1 and S2, respectively (Supporting Information). Design of Leaching Column and Growth Conditions. A column experiment was conducted with 12 columns in total: the two soils (Sclaigneaux and Angleur) were considered under two vegetal cover conditions (A. capillaris and plant-free soil) with three replicates for each treatment. The design of the experimental device was adapted from Gommers et al.33 The columns were made from poly(vinyl chloride) (PVC) tubes, with a length of 300 mm and a diameter of 75 mm, with multiple holes drilled in the bottom end cap covered by a polyamide mesh (mesh size = 20 μm). Each column was connected to a funnel channeling the leachates into a high-density polyethylene (HDPE) collection bottle. All apparatus components were acid-washed (pH 3, HCl) and abundantly rinsed with deionized water. Columns were filled with a mixture consisting of 100 g of soil particles (100−500 μm) and 1900 g of washed quartz (500−1000 μm), representing a length of soil-filled column of 250 mm. Prior to sowing, the columns were arranged according to a randomized pattern in a controlled-climate room (temperature of 20 °C, relative humidity of 80%, 16-h photoperiod, and mean light intensity varying from 120 to 180 μmol m−2 s−1). The columns were also slowly saturated with a nutrient solution whose chemical composition, expressed in mM, was 1 Ca(NO3)2.4H2O, 0.5 KCl, 0.25 K2SO4, 0.05 MgCl2, 0.05 MgSO4, 0.05 NaH2PO4, and 0.08 H3BO3. Then, 0.5 ± 0.01 g of sterilized seeds (10 min in 2 M H2O2) of Agrostis capillaris L. (= A. tenuis Sibth.) was sown in each column, and the surface of the soil was covered with a thin layer (2 mm) of polyethylene beads to protect it from drying out, prevent soil destructuration by drop impact, and ensure watering flow homogeneity. Control experiments were also conducted following the same procedure but without plants. One week after sowing, each column was connected by an opaque inlet tubing to its own nutrient solution reservoir, and irrigation from above was started. The nutrient solution was delivered from the reservoir to the column using a multichannel peristaltic pump, which ensured that each column received the same volume of solution. However, according to the growth rate of the plants and corresponding transpiration, the irrigation flow was modified during the course of the experiment so that the percolated volume from each column was at least 80−100 mL week−1. Leachates were collected weekly for 7 weeks. At the completion of the experiment, shoots were cut using ceramic scissors. The material filling the tube was then extruded, and the core was cut into 5-cm-thick slices. The contrasting grain size of the quartz and the soil particles made it possible to recover the soil by sieving the soil−quartz mixture, whereas the coarse grain size of the soil (>100 μm) eased the separation of adhering solid particles from the roots. Briefly, after carefully separating and gathering the roots, the material remaining from

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MATERIALS AND METHODS Description of Sites. Two Technosols30 with different sources of metal contamination were collected in Belgium. Site 1 is located at Sclaigneaux near the city of Andenne along the valley of the Meuse River (hereafter referred to as Sclaigneaux). Although this 80-ha site is now a natural reserve accessible to the public, it was intensively subjected to heavy-metal contamination from the 1850s to the 1970s due to atmospheric fallout and slag deposition originating from the adjacent lead and zinc smelting plant (“Société Dumont”). A detailed description of the site and associated slag can be found in ref 31. The studied soil was collected from the A horizon of a sandy loam slag-derived Technosol. Although the site is partly spontaneously revegetated by grass and birch trees, the soil was sampled in a bare area. Site 2 is an industrial dump site located at Angleur near the city of Liège (hereafter referred to as Angleur). The total site area covers ∼1.9 ha, and a major part of the waste pile is adjacent to the Ourthe River and to the Canal of the Ourthe. The dump contains waste material originating from a zinc smelting plant that was operated between 1837 and 1905 by the “Société des Mines et Fonderies de Zinc de la VieilleMontagne”. A detailed description of the site is available in ref 32. Although several parts of the site are still bare, it has been spontaneously colonized by a (pseudo-) metallophyte flora including Armeria maritima ssp. halleri and A. capillaris.29 7867

dx.doi.org/10.1021/es5002874 | Environ. Sci. Technol. 2014, 48, 7866−7873


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by successive additions of acids (HCl/HNO3/HBr) according to the methodology described by Smolders et al.43 Zinc recovery was quantitatively monitored to circumvent problems associated with potential isotopic fractionation on microcolumns. The yield values were higher than 98%. Total procedural blanks (digestion and chromatography) were less than 10 ng of Zn. Zinc isotopic ratios were measured on an HR Nu Plasma MC-ICP-MS (multicollector inductively coupled plasma mass spectrometer, Nu Instruments, Wrexham, U.K.) in wet-plasma mode at Université Libre de Bruxelles, Brussels, Belgium. Mass discrimination effects were corrected by using simultaneously external normalization (Cu-doping method) and standard-sample bracketing with 400 ppb in-house Merck Zn and Cu standard solutions (calibrated against the JMC 30749L Zn and NIST SRM 976 Cu reference standards, both supplied by F. Albarède, ENS, Lyon, France).44 Nickel contributions were systematically corrected by monitoring mass 62 (62Ni). Nevertheless, the 64Ni beam intensity was less than 1.5 μV (i.e., less than the background signal) (for complementary information, see Mattielli et al.15). The Zn isotopic compositions in this study are expressed as δ66Zn = [(66Zn/64Zn)sample/(66Zn/64Zn)JMC Lyon − 1] × 1000 (in ‰). During the period of data collection, repeated analyses of our in-house Zn and Cu standards gave a mean δ66Zn value of +0.01 ± 0.03 ‰ (2SD) (n = 24). In addition, repeated analyses of the IRMM 3702 Zn certified standard solution45 (relative to our in-house standard) gave a mean δ66Zn value of +0.39 ± 0.02 ‰ (n = 5), well in the range of the reported values.45,46 For comparison with previous publications, the current batch of the JMC 3-0749L Zn standard used at ULB gave +(0.11 ± 0.03) ‰ (n = 17) relative to our in-house standard, which is consistent with the long-term repeated analyses performed on this standard in the laboratory. Finally, the ryegrass BCR281 reference material was measured and provided a δ66Zn value of +0.49 ± 0.04 ‰ (n = 9) relative to our in-house standard, which is well in agreement with the published values.43,47 The Zn isotope composition of the whole plant, δ66Znplant, was estimated by a method similar to that used by Aucour et al.,48 according to the equation

each slice was air-dried, and the soil was separated from quartz by sieving at 0.05) higher in the presence of plants (Figure S3, Supporting Information), suggesting that root-derived DOC was negligible. Moreover, model calculations of the metal speciation (using Visual MINTEQ 3.0) indicated no increase in organo-Zn complexes in the presence of plants and predicted free Zn2+ to be the dominant species in both cases (Figure 3). Therefore, the heavier Zn isotope composition of leachates from planted soils can be explained only by the release of Zn from a pool that is characterized by enrichment in heavy Zn isotopes compared to the pool that spontaneously supplied Zn to leachates in the absence of plants. This highlights the ability of plants to induce the mobilization of Zn from a less soluble pool. We hypothesize that this pool

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ASSOCIATED CONTENT

S Supporting Information *

Selected soil properties (Table S1), soil mineralogy (Table S2), Zn isotope ratios (Table S3), speciation results using different DOM compositions (Figures S1 and S2), time evolution of dissolved organic carbon concentration (Figure S3). This material is available free of charge via the Internet at http:// pubs.acs.org.

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AUTHOR INFORMATION

Corresponding Author

*Phone: 0033 (0)3 44 06 93 45; fax: 0033 (0)3 44 06 25 26; email: [email protected], david.houben@ outlook.com. Notes

The authors declare no competing financial interest. 7871



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ACKNOWLEDGMENTS We thank P. Populaire for his technical assistance and C. Givron, A. Iserentant, W. Debouge, and I. Petrov for their analytical assistance. C. Rozewicz is gratefully acknowledged for proofreading the manuscript as a native English speaker. D.H. was supported by the “Fonds pour la formation à la Recherche dans l’Industrie et dans l’Agriculture” (FRIA) of Belgium. S.O. was funded by the “Fonds National de la Recherche Scientifique” (FNRS, Belgium). This work was also supported by the FNRS, Belgium (FRFC Contract 2.4599.11).

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