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Characterization of Natural and Affected Environments
Bioavailability, speciation, and phytotoxicity of tungsten (W) in soil affecting growth and molybdoenzyme activity of nodulated soybean Eva Oburger, Carolina Vergara Cid, Julian Preiner, Junjian Hu, Stephan Hann, Wolfgang Wanek, and Andreas Richter Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.7b06500 • Publication Date (Web): 27 Apr 2018 Downloaded from http://pubs.acs.org on April 28, 2018
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Bioavailability, speciation, and phytotoxicity of tungsten (W) in soil affecting
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growth and molybdoenzyme activity of nodulated soybean
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Eva Oburger1,2*, Carolina Vergara Cid3,2, Julian Preiner4,2, Junjian Hu5, Stephan Hann5, Wolfgang Wanek1,
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Andreas Richter1
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1
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Ecosystem Research, Althanstrasse 14, A-1090 Vienna.
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2
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Konrad-Lorenz Strasse 24, A-3430 Tulln, Austria
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University of Vienna, Department of Microbiology and Ecosystem Science, Division of Terrestrial
University of Natural Resources and Life Sciences, BOKU, Department of Forest and Soil Sciences,
National University of Cordoba, Faculty of Physical and Natural Sciences, Multidisciplinary Institute of
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Plant Biology, Pollution and Bioindicator Section, Av. Velez Sarsfield 1611, X5016CGA, Cordoba,
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Argentina.
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4
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Vienna.
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1190 Vienna, Austria
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*corresponding author:
[email protected] University of Vienna, Department of Ecogenomics and Systems Biology, Althanstrasse 14, A-1090
University of Natural Resources and Life Sciences, BOKU, Department of Chemistry, Muthgasse 18, A-
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Abstract
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Increasing use of tungsten (W) based products opened new pathways of W into environmental systems.
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Due to its chemical alikeness with molybdenum (Mo), W is expected to behave similarly to its ‘twin
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element’ Mo; however, our knowledge of the behaviour of W in the plant-soil environment still remains
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sketchy. The aim of this study was to investigate plant growth as well as W and nutrient uptake
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depending on soil chemical properties like soil pH and texture. Soybean (Glycine max cv Primus) was
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grown on two acidic soils differing in soil texture, that were either kept at their natural soil pH (pH 4.5-5)
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or limed (≥ pH 7) and amended with increasing concentration of metallic W (control, 500, 5000 mg kg-1).
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In addition, the activity of molybdoenzymes involved in N assimilation (nitrate reductase) and symbiotic
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N2 fixation (nitrogenase) were also investigated. Our results showed that the risk of W entering the food
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web is significantly greater in high pH soils due to increased solubility of mainly monomeric W. The
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effect of soil texture on W solubility and phytoavailability was less pronounced compared to soil pH.
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Particularly at intermediate W additions (W 500 mg kg-1), symbiotic nitrogen fixation was able to
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compensate for reduced leaf nitrate reductase activity. When W soil solution concentrations became 1 ACS Paragon Plus Environment
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too toxic (W 5000 mg kg-1), nodulation was more strongly inhibited than nitrogenase activity, suggesting
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a more efficient detoxification/ compartmentalization mechanism in nodules than in soybean leaves.
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The increasing presence of polymeric W species observed in low pH soils spiked with high W
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concentrations resulted in decreased W uptake. Simultaneously, polymeric W species had an overall
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negative effect on nutrient assimilation and plant growth, suggesting a greater phytotoxicity of W
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polymers. Our study demonstrates the importance of accounting for soil pH in risk assessment studies of
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W in the plant-soil environment, which has been completely neglected in the past.
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Key words: Tungstate, Nitrate reductase, Nitrogenase, Polymers, Risk assessment, Bradyrhizobium,
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Nodules, Molybdenum, Pollution
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Introduction
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Tungsten (W) is a transition metal that resides in the chromium (Cr) group (Group VI) of the
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periodic table along with Cr and molybdenum (Mo). Compared to other metals, W abundance in the
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earth crust is very low ranking 54th/18th in the overall element/metal abundance lists 1. Nevertheless, a
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variety of W minerals is known with four being of economic importance (wolframite ((Fe, Mn) WO4),
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hübnerite (MnWO4), ferberite (FeWO4) and scheelite (CaWO4)).
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Increasing industrial and military use of W-based products, ranging from household appliances
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to high-end technology goods,2 opened new pathways of W into environmental systems. Main routes of
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entry into the environment include emission and discharge of W-containing waste products by W
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production plants, military activities, W tire stud and road abrasion, coal combustion and soil fertilizer
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application 2-4. Particularly the use of W ammunition has been shown to lead to significantly elevated W
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concentrations in soil (up to 2000 mg kg-1) 5. Recent assessments indicate that the anthropogenic
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contribution to W mobilization in the environment amounts to about 30% of the total global surface
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fluxes but would increase to about 60% if W transport with human-induced soil erosion and Aeolian dust
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is included 6. These numbers clearly show the importance of soil processes in controlling the global
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fluxes of W. Average background concentrations of W in soil range from 0.1 – 2.7 mg kg-1, however
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reported W concentrations in soils near mining or smelting sites, war zones (gulf war region) or military
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firing ranges exceed background thresholds by 10- to 2000-fold
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significant W bioaccumulation in rice grown on agricultural fields adjacent to a W mine,8 further
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highlighting the need for a better understanding of the biogeochemical behaviour of W in the
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environment. 2 ACS Paragon Plus Environment
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. A survey from China revealed
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In environmental systems W occurs as thermodynamically stable oxyanion, tungstate (WO42-),
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with W in its highest oxidation number (6+).
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monomeric W in soil is comparable to that of other oxoanions like molybdate or phosphate (Pi). In a
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leaching column experiment with soil amended with metallic W, Bednar et al. 9 showed that W leaching
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increased with increasing pH of the leachate solution as well as in the presence of competing anions
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(phosphate) and humic acids. Gustafsson
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wide pH range and observed that the decrease in sorption with increasing pH was less pronounced for
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W than for Mo, indicating a higher sorption affinity of W. While knowledge of the chemical and
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environmental behaviour of W in soil still remains limited, these results suggest that solubility and
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consequently plant uptake strongly depend on soil pH.
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Experimental data suggest that the behaviour of
compared W and Mo sorption onto ferrihydrite across a
Recent, but limited, toxicological studies in soil showed that plants and soil organisms are 11
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relatively tolerant to elevated W concentrations. Bamford et al.
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survival and reproduction of earthworms at W concentrations of 586 mg kg-1 soil (artificial soil, pH 6.5),
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while different tolerance levels were observed for different plant species (oat (Avena sativa) > radish
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(Raphanus sativus) > lettuce (Lactuca sativa)). High tolerance often coincides with high biomass
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accumulation comprising a considerable, yet understudied, entry pathway of W into the food web and
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suitable methods to predict W plant uptake from soil have not yet been investigated.
for example found no effect on
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Tungsten is in many ways the twin element of molybdenum (Mo). Both elements, Mo and W,
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belong to the Cr group, but unlike chromium, the two heavier elements possess equal atomic (1.4 x 10-10
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m) and ionic (0.68 x 10-10 m) radii, similar electro negativity (1.4 for W, 1.3 for Mo), and the same range
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of oxidation states (-2 to +6) and coordination numbers (5–9) 1. Consequently, W and Mo also show
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similar redox and coordination chemistries in both structural and functional aspects. In higher plants
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Mo, unlike W, is an essential micronutrient. Being a cofactor of enzymes involved in nitrate assimilation
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(nitrate reductase (NR)) and symbiotic nitrogen (N2) fixation (nitrogenase)12, Mo plays a key role in plant
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N nutrition. It is well-known that certain metalloenzymes are not absolutely metal specific and negative
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effects of W on molybdoenzyme activity in plants and prokaryotes have been repeatedly demonstrated
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13-16
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well understood and there is a lack of studies linking bioavailability of W to plant physiological
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performance.
. Nevertheless, uptake and incorporation of W as well as its effects on plant metabolism are still not
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The aim of this study therefore was to investigate W solubility and plant uptake depending on
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soil chemical properties like soil pH and texture by growing soybean (Glycine max cv Primus) in two
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natural acidic soils differing in soil texture (silt clay loam and sandy loam, World Reference Base of Soil 3 ACS Paragon Plus Environment
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(WRB), Food and Agriculture Organization of the United Nations), that were either kept at their natural
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soil pH or limed (2.5% CaCO3). Each combination of soil pH and texture was spiked with increasing
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concentration of metallic W (control, 500, 5000 mg kg-1). The effect of soil pH dependent W
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phytoavailability and speciation on plant nutrition and growth as well as the activity of molybdoenzymes
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involved in N assimilation (nitrate reductase) and symbiotic N2 fixation (nitrogenase) was investigated.
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Materials and methods
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Experimental soils. Experimental soils were collected from Siebenlinden (N 48° 40.513’, E 14°59.933')
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and Litschau (N 48° 57.37167’ E 15° 3.95167’) in the Waldviertel area in Lower Austria, Austria. Both
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soils evolved from granite rock and are classified as acidic Cambisol. Based on soil texture analysis (Table
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1), the soil from Siebenlinden will from here on be referred to as SAND and the soil originating from
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Litschau will be referred to as CLAY. Soils were air dried at ambient temperature and passed through a 4
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mm sieve. Liming is a common agricultural practice to raise soil pH and improve nutrient availability.
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Half of the soil material was therefore amended with CaCO3 (Calcium carbonate precipitated, puriss.,
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Sigma-Aldrich) to a final concentration of 2.5% to achieve a high (limed) pH treatment, and the other
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half of the soil was directly used as low pH (acidic) counterpart. To simulate anthropogenic driven W
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entries into the environment, e.g via ammunition or abrasion of cutting and drilling tools, metallic W
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powder (Tungsten powder,
