Mechanism of Accumulation of Methylmercury in Rice (Oryza sativa L

Article Cite This: Environ. Sci. Technol. XXXX, XXX, XXX−XXX

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Mechanism of Accumulation of Methylmercury in Rice (Oryza sativa L.) in a Mercury Mining Area Zhangwei Wang,†,‡ Ting Sun,†,‡ Charles T. Driscoll,§ Yongguang Yin,†,‡ and Xiaoshan Zhang*,†,‡ †

Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, No. 18 Shuangqing Road, Beijing 100085, China University of Chinese Academy of Sciences, Beijing 100049, China § Department of Civil and Environmental Engineering, Syracuse University, 151 Link Hall, Syracuse, New York 13244, United States Environ. Sci. Technol. Downloaded from pubs.acs.org by QUEEN MARY UNIV OF LONDON on 08/22/18. For personal use only.

‡

S Supporting Information *

ABSTRACT: Rice consumption is the primary pathway for methylmercury (MeHg) exposure at inland mercury (Hg) mining areas of China. The sources and processes of formation and translocation for MeHg in rice plant are complex and remain largely unknown. In this study, rice (Oryza sativa L.) was exposed to isotopically labeled dimethylmercury (DMe199Hg) in field experiments using open top chambers to explore the response of MeHg accumulation in rice tissues to different levels of DMe199Hg in air. Rice leaves assimilated DMeHg from air, which was subsequently largely stored in aboveground tissues, including the rice grain, with only a small amount reaching the root. Combining these experimental results with field investigations of DMeHg concentrations in air beneath the rice canopy in a Hg mining area, we estimate that 15.5%, 10.8%, and 8.50% MeHg in the brown rice, the leaf, and the upper stalk, respectively, could be derived from atmospheric sources of DMeHg, while 99.5% of MeHg in rice root originated from the rice soil−water system. These findings help refine the mechanism of MeHg accumulation in rice that, in addition to soil, a fraction of MeHg in rice plants can be derived from DMeHg emissions from flooded rice paddies in Hg mining areas.

1. INTRODUCTION Mercury (Hg) is a persistent and highly toxic trace metal. The ecological and toxicological effects of Hg are strongly dependent on its chemical speciation.1,2 Organic compounds of Hg, such as methylmercury (MeHg), are of particular concern because of their bioaccumulation in food webs and their role in exposure and toxicity.3 In aquatic food webs, fish and marine mammals at the top of aquatic food chains readily bioaccumulate and biomagnify MeHg to high concentrations. Seafood consumption is the primary pathway of MeHg exposure for most people globally.4−8 However, MeHg can also be bioaccumulated along terrestrial food chains.9 Recent field investigations from Hg mining and nonmining areas have also shown that rice plant, especially the grain, has the higher MeHg concentrations compared to other cereals.10−12 Human exposure to MeHg through consumption of harvested rice was assessed by comparing the estimated MeHg dietary intake with the provisional tolerable weekly intake established by the Joint FAO/WHO Expert Committee on Food Additives, and with the MeHg reference dose (RfD) of the United States Environmental Protection Agency (USEPA).13−15 Isotope signatures of MeHg in diet (rice and fish) and human hair have been used to quantify human exposure.16,17 Rice consumption is a major pathway for MeHg exposure in inland regions polluted by Hg where rice is a large portion of the diet.11,13,18−24 © XXXX American Chemical Society

The sources and processes of formation and translocation for MeHg in rice plant are complex and remain largely unknown. MeHg in rice plant is thought to largely originate from soil.12,25−28 The mobility and methylation of soil Hg is determined by a range of factors, such as redox potential, pH, dissolved organic carbon, sulfur, iron, and dissolved Hg content, and microbial communities (methanogens, sulfatereducing, and iron-reducing bacteria and archea).1,29−33 The physiochemical conditions of flooded paddy soils promote the formation of MeHg, which can then be assimilated by rice root and combined with protein, polysaccharides, and nucleic acids.26,34 With rice plant growth, MeHg in rice roots is translocated to other parts of the plant, including grain as the rice seed begins to develop.26,29,35 Rice cultivars and farming strategies, selenium and phosphorus effect MeHg assimilation and translocation from root to grains.30,36−38 However, variation in stable Hg isotopes in different tissues of rice39 and controlled field experiments using cereals and grass40−43 clearly demonstrate that plants, such as rice, can also assimilate atmospheric Hg through stomata of leaves. The pathway plays a crucial role in Hg accumulation in aboveReceived: April 4, 2018 Revised: July 27, 2018 Accepted: August 6, 2018

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DOI: 10.1021/acs.est.8b01783 Environ. Sci. Technol. XXXX, XXX, XXX−XXX

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Environmental Science & Technology

L−1 199HgCl2 solution was incubated with an excess of MeCo (MeCo:199Hg2+ = 10:1) at pH 4.0 and 9 °C in 0.01 mol L−1 NaCl. For incubations, all reagents were added in 200 mL Pyrex glass bubble wrapped with aluminum foil in the dark space of a water bath. The 2.0 L min−1 highly pure N2 (99.999%) carried the gaseous methylmercury into the 1.0 L buffer bottle (Pyrex glass) with multioutlets for air flow. A gas flowmeter was used to adjust the airflow rate and control the DMe199Hg concentration in the OTCs (see Figure S1, Supporting Information). Enriched 199HgO (atomic percentage 91.09 ± 0.05) was purchased from Oak Ridge National Laboratory (Oak Ridge, TN, USA) and dissolved in 10% HCl as a stock solution (1.0 g of 199Hg(II) L−1) for the experiment. MeCo (CH3B12, 99.5%, Sinopaharm Chemical Reagent Co., Ltd. in China) and other reagents used were ultrapure quality. To reduce the risk associated with use of DMeHg, ventilation devices were used in this generation system, and operators used gas masks and chemical-resistant gloves. CAUTION: Dimethylmercury is volatile and extremely toxic, causing neurological damage and death. Absorption by the skin and inhalation of the vapors must be avoided by using adequate ventilation and proper personal protection gear. 2.2. OTCs Experiment with Gaseous DMe199Hg Treatments. Field OTCs experiments using stable Hg isotopes were performed to trace DMeHg assimilation and translocation in rice plants. The OTCs were constructed following the design of Heagle et al.72 A schematic illustration of this design is shown in Figure S1. The total volume of the chamber of OTCs was 0.6 m3, with the air turnover time of about 50 s. All fixtures and tubing for the experiments were made or wrapped with Teflon to minimize the absorption of gaseous DMeHg. DMeHg is the dominant product in aqueous media of abiotic methylation of Hg(II) by MeCo.68 More importantly, DMeHg has a high vapor pressure (8.30 × 103 Pa), which is at least 3 and 4 orders of magnitude higher than those of monomethylmercury (MMeHg) and elemental mercury, respectively. Consequently, we established four different DMe199Hg concentrations in air for the OTCs, including reference condition (0 pg m−3), 16 ± 9, 137 ± 92, and 329 ± 182 pg m−3. Note that the Hg isotope was not spiked in potted soil of the OTCs. A single replicate was used for each concentration level. Additionally, to compare atmospheric and soil pathways of MeHg accumulation in rice tissues, two soil amendment treatments (45 μg of 199Hg(II) kgdry_soil−1) were established by adding extrinsic diluted 199 HgCl2 solution (pH ≈ 6.5) to soil. Note that for these soil experiments Hg isotope was not spiked in exposure air. Intrinsic total Hg of these experimental soils were 52.6 ± 8.92 μg of Hg kgdry soil−1. The OTCs experiments were conducted during the rice growing season from July 10 to October 10, 2016. A rice cultivar widely grown by local farmers, Zhongqingyou No. 2, was cultivated for our experiments. The management of rice for this experiment followed local agronomic practices. 2.3. Sampling and Analysis for Field Measurements and OTCs Experiments. Field measurements of DMeHg in air and MeHg in rice tissues were conducted August 15−25, 2016, at a rice paddy in Shujing (27.5° N, 109.2° E). This site is located near an inactive smelter with an abandoned Hg mine in Wangshan in Southwest China. These measurements were made to help put the results of OTCs experiments in the context of field conditions. Sampling of DMeHg in surface air beneath a rice canopy was conducted by the pumping of

ground parts of the plant. Furthermore, some researchers have suggested that MeHg in plant leaves could be derived from in vivo transformation of inorganic Hg species from the atmosphere.44,45 So far, there is a limited understanding of the atmospheric pathway of MeHg to rice tissues. Further research is needed to fill this knowledge gap. There are three operationally defined forms of atmospheric Hg, including gaseous elemental mercury (GEM), gaseous oxidized mercury (GOM), and particulate bound mercury (PBM). Gustin and co-workers have shown that GOM concentrations measured by a KCl-coated denuder can underestimate concentrations by a factor of 1.6−12, and the composition of GOM is poorly understood.46−48 Dissolved gaseous dimethylmercury (DMeHg) has been reported in upwelling marine environments and can be an important form of methylated Hg in the deep ocean.49−52 A few measurements of dissolved DMeHg have been reported for nonmarine environments, including anoxic waters of Onondaga Lake, NY, USA,53 mangrove and salt marsh sediments,54,55 and river floodplain soil.56 In rice paddies, oxic soils become completely anoxic upon flooding,57 and the waterlogged soil provides suitable conditions for methanogens, sulfate-reducing and ironreducing bacteria, and archea.58 In this study, we hypothesize that DMeHg could be formed in soil-water system of flooded rice paddy in Hg-contaminated area, and subsequently evaded to air beneath the rice canopy, and assimilated by the rice plant and translocated to tissues. To test this hypothesis, we first used methylcobalamin (MeCo) and isotopic 199Hg(II) to produce DMe199Hg, and then exposed rice (Oryza sativa L.) to DMe199Hg using field open top chambers (OTCs) to explore the response of MeHg accumulation in rice tissues to different levels of DMe199Hg in air. We also confirmed DMeHg concentrations in air beneath the rice canopy from field measurements in a Hg mining area and estimated its contribution to MeHg in rice plant tissues. Finally, based on the results of this work, we posit pathways of MeHg accumulation in rice plant.

2. EXPERIMENTAL SECTION 2.1. Gaseous DMe199Hg Generation. The highly volatile DMeHg can be produced by biotic and abiotic pathways.59−61 Known abiotic pathways include reaction of CH3Hg+(aq) with H2S62 or selenoamino acids63 and methylation with methylcobalamin (CH3−B12, MeCo).64 The number of bacterial strains tested for their ability to methylate Hg(II) to DMeHg is limited and the main biological process for DMeHg formation in the environment remains to be identified.65 In this study, DMe199Hg was generated based on the following reactions: CH3−B12 + Hg 2 + + H 2O → CH3Hg + + H 2O−B12

(1)

CH3−B12 + CH3Hg + → CH3HgCH3 + H 2O−B12

(2)

Previous studies have shown that pH, temperature, salinity, initial concentrations of reagents, and the ratio of MeCo to Hg(II) all have a strong influence on the relative efficiency of Me199Hg and DMe199Hg production by the above reactions. The optimal experimental conditions used to enhance DMe199Hg formation was pH 4.0 and MeCo/199Hg(II) molar ratio of 10 in 20 °C.66−70 To avoid the possible interference by acetate buffer in the formation of Hg compounds,70 sulfuric acid and sodium hydroxide were used to adjust pH.70,71 Therefore, in this study 100 mL of 0.035 mg B


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Environmental Science & Technology approximately 120 L of air (2 L min−1 airflow rate) through a sodalime trap (4−8 mesh sodalime ACS, Alfa Aesar) to an absorbent trap (quartz tube with 8.0 cm long and 0.7 cm inside diameter) packed with Bond Elut ENV (BE) absorbent (125 μm, Varian Inc.). The sodalime trap was used to remove water in the airflow, while the BE trap was used to absorb DMeHg.49,73 All traps and tubes were tightly covered with aluminum foil to prevent photolytic reactions. After sample collection, BE traps were sealed with Teflon endcaps and transported to the laboratory for analysis. A determination of DMeHg on BE traps was performed by isothermal gas chromatography separation and detection by cold vapor atomic fluorescence spectrometry (GC-CVAFS, Methylmercury Manual System, Brooks Rand Co., USA). BE absorption is the most suitable approach for simultaneous trapping of gaseous MMeHg and DMeHg because of high absorption capacity and excellent chromatographic properties.73 In GC-CVAFS method, methylmercury species were pyrolyzed to elemental mercury and thus the peak responses are the same for unit molar values of DMeHg and MMeHg. Because of the extreme toxicity of DMeHg, MMeHg standards (National Research Centre for Certified Reference Materials, China) were used to produce calibration curves for DMeHg quantification, an approach previously used in investigations of DMeHg in seawater.50,74 Note that we corrected the DMeHg mass with the coefficient of γ = 230.6/215.6 to obtain DMeHg concentration. Ultratrace Hg clean techniques75 were applied during the field study. The DMeHg field blanks were conducted every day in the same manner (handle, store, transport, and analysis) as the field samples collection, but did not draw air through the BE trap. In addition, whole rice plants were sampled and cleaned with drinking water in the field and then transported to the laboratory for further preparation and analysis for MeHg concentrations like those used in OTCs experiments. In OTCs experiments, the whole rice plant was sampled at the tillering stage, elongation stage, heading stage, milk stage, and ripening stage at intervals of about 20 days, that is, July 20 (0720), August 10 (0810), August 31 (0831), September 18 (0918), and October 10 (1010). All samples from OTCs experiments were cleaned with drinking water in situ followed by a deionized water rinse after being transported to the laboratory. Rice root, upper and bottom stalks with the sheath removed, and foliage were segmented, and brown rice was separated from the hull in the milk and ripening stages using a dehuller machine (JLG-1, China). Soils (0−20 cm) were sampled coincident with the rice plant sampling using a shovel to avoid roots, leaves, and stones in OTCs experiments. Plant and soil samples were freeze-dried and then ground, homogenized, and stored at −4 °C for analysis. For MeHg analysis, rice samples (approximately 0.1 g) were prepared using KOH−methanol/solvent extraction,76 and soil samples (approximately 1.0 g) were extracted using CuSO4− methanol/solvent extraction.77 The concentrations of MeHg were then determined using aqueous ethylation, purging, trapping, and GC-CVAFS detection following the USEPA 1630 method.75 Me202Hg and Me199Hg were determined by gas chromatography separation followed by inductively coupled mass spectrometry detection (GC-ICPMS) as detailed by Ma et al.78 To ensure the quality of analysis, in triplicate samples were conducted for each sample. Analysis of two procedure blanks, matrix spikes, and certified reference material (CRM, IAEA-405) were performed for each batch

of samples. The method detection limits (3δ) were 0.001 ng g−1 for MeHg in soil and rice tissues. All procedure blanks were below the method detection limits. The recovery of MeHg was 85−113% for all matrix spikes and CRM, and the precision for in triplicate samples were estimated as less than 7.0%. 2.4. Data Analysis. The transient signals recorded by ICPMS were processed by Origin 8.0 software (Microcal Software Inc., MA). Quantification of Hg isotopes was conducted using peak areas of the corresponding species. Me199Hg concentrations in samples were derived from both ambient Hg and spiked Me199Hg, while the Me202Hg originated from the ambient Hg. Thus, concentrations of MeHg originating from ambient Hg were calculated using the concentrations of Me202Hg and natural abundance of 202Hg (eq 3). The Me199Hg from ambient Hg can be calculated using the concentrations of Me202Hg and the ratio of natural abundance of 199Hg to 202Hg (P199/P202). Concentrations of Me199Hg originating from the spiked 199Hg tracer can be calculated by subtracting the Me199Hg originating from ambient Hg from the measured concentration of Me199Hg (eq 4). CMeHg(ambient) = CMe202 Hg /P202

(3)

CMeHg(tracer) = C Me199 Hg − P199C Me202 Hg /P202

(4)

where CMe202Hg and CMe199Hg are the measured concentrations of Me202Hg and Me199Hg (ng g−1), P202 and P199 are the natural isotopic abundances of 202Hg and 199Hg. CMeHg(ambient) and CMeHg(tracer)are the concentrations of MeHg (ng g−1) in samples originating from the ambient and from the spiked tracer.

3. RESULTS AND DISCUSSION 3.1. High Ambient DMeHg Concentrations in Flooded Rice Paddy. A field investigation of DMeHg was conducted at a rice paddy in Shujing located near an inactive smelter with an abandoned Hg mine in Wangshan in Southwest China. The mean DMeHg concentration in air beneath the rice canopy was 10.1 ± 7.06 pg m−3 with a range from 1.27 to 25.7 pg m−3, which is higher than values reported in urban air79,80 and the arctic marine boundary layer,49 but about 3 orders of magnitude lower than those in landfill gas81−84 (Figure 1). DMeHg concentrations in air beneath the rice canopy decreased by a factor of 10 from early morning (25.7 pg m−3) to midday (2.80 pg m−3) and then increased by a factor of 5 after sunset (10.2 pg m−3) (Figure 2). These patterns imply photolytic degradation of DMeHg in the daytime despite the shading of solar radiation by the rice canopy. High planting density of mature rice can form a “canopy”, increasing resistance and restricting gas exchange from below to above the rice canopy. This condition likely limits dilution of DMeHg emissions from paddy water, allowing for accumulation beneath the rice canopy. Note that experimental devegetation in flooded rice fields has been shown to decrease pore water MeHg production by 64%.85 Diel studies of MeHg concentrations in pore water (0−2 cm) in rice milk stage showed a peak around midnight and low levels during daytime, which was attributed to change in biotic methylation process resulting from competition between sulfate-reducing bacteria and methanogens.86,87 In our study, the highest DMeHg levels were observed in early morning, with the lowest at midday in air beneath the rice canopy despite missing data at midnight. This pattern could reflect the C


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rice tissues. In contrast, CMeHg(tracer) in leaves and grains increased with DMe199Hg concentrations in air, showing a quadratic linear relationship (R2 = 0.846−0.999, p < 0.05) during the stages of rice growth (Figure 3C,D). Although CMeHg(tracer) was low in rice bottom stalks and roots (several ng g−1), the quadratic linear correlations remained significant (Figure S2D−F). Changes in CMeHg(ambient) and CMeHg(tracer) differed during the five stages of rice growth (tillering stage, elongation stage, heading stage, milk stage, and ripening stage). The CMeHg(ambient) was highest in the tillering stage, while CMeHg(tracer) was greatest in the elongation and heading stages, with both ambient and tracer concentrations decreasing with prolonged plant growth (Figure 3 and Figure S2). This pattern suggests differences in the mechanism of MeHg accumulation derived from the tracer and ambient Hg. In OTCs experiments, to some extent, CMeHg(ambient) and CMeHg(tracer) represent rice MeHg derived from soil and air, respectively. The patterns of decreasing concentrations during the later stages of rice growth could be attributed to the dilution of MeHg with biomass production associated with rice growth and/or the demethylation process. Furthermore, CMeHg(ambient) and CMeHg(tracer) were significantly higher in brown rice than values in the hull during the milk stage and ripening stage, indicating that the edible portion of rice tends to accumulate elevated MeHg. This finding is consistent with results from soil Hg simulation experiments and field surveys.11,12,25,26,28 3.3. Translocation of Me199Hg in the Rice Plant. The use of Hg stable isotope ratios coupled with improvements in analytical methods have facilitated the identification of sources and processes of Hg in the environment.88,89 In the OTCs experiments, the ratios of Me202Hg to Me199Hg in soil ranged from 1.66 to 1.82, with average 1.74 ± 0.0400. No difference in Me202Hg to Me199Hg ratios was evident in soil during the growing season among the reference and three DMe199Hg treatments (Figure 4A−C). However, the ratios of Me202Hg to Me199Hg in leaves sharply decreased from 1.68 to 0.153, 1.54 to 0.0492, and 1.32 to 0.0447 from the tillering stage (0720) to the ripening stage (1010) for the three DMe199Hg treatment concentrations (16 ± 9,137 ± 92, and 329 ± 182 pg m−3), respectively. These corresponding ratios in rice roots decreased by only 23.1%, 36.2%, and 48.4% from the tillering stage to the ripening stage for three DMe199Hg treatments. Similar decreasing trends were found in rice upper and bottom stalks. The amplitude of the MeHg response increased with rice growth. For example, the percentage difference for leaves (between DMeHg treatment and reference; see Figure 4) was 16.8% between the tillering stage and elongation stage, and increased to 54.4%, 85.6%, and 90.9% from the tillering stage to the heading stage, milk stage, and ripening stage, respectively, in the 16 ± 9 pg m−3 DMeHg treatment. These reductions followed the order of leaf > upper stalk > bottom stalk > root for a given treatment in OTCs experiments. Note that a reduction in the amplitude of the temporal response of the tracer concentrations in different tissues suggests translocation of MeHg in rice from the atmospheric source to the rice leaf, to the upper stalk, to the bottom stalk, and finally to the rice root. In contrast, in reference OTCs, the Me202Hg/ Me199Hg ratios of rice tissues were stable, with mean values of 1.71 ± 0.120 for leaves, 1.70 ± 0.00500 for upper stalks, and 1.69 ± 0.00500 for bottom stalks during the entire growth period (Figure 4E). Although fractionation of stable isotopes of Hg have been observed for a variety of natural processes,

Figure 1. DMeHg concentrations in air beneath the rice canopy in this study, compared with values in urban air,79,80 the arctic marine boundary layer,49 and landfill gas.81−84 The boxes extend from 25 to 75% quartiles with the middle line and black solid square representing the median and average values, respectively; the whiskers extend from minimum to maximum values.

Figure 2. Diurnal variation of DMeHg concentrations in air (pg m−3) beneath the rice canopy.

dynamics of microbial methylation on DMeHg formation in flooded paddies. However, more research is needed to confirm the mechanism driving diel patterns in DMeHg. High MeHg concentrations were also evident in rice tissues during rice milk stage at the Shujing site (Figure S3). 3.2. Experimental Assimilation of DMe199Hg by Rice Tissues. The results of the field OTCs experiments using stable Hg isotopes revealed that rice plant is capable of assimilating gaseous organic Hg from air. Time series of CMeHg(ambient) and CMeHg(tracer) in rice leaves and grains from the OTCs experiments are shown in Figure 3. During the growing season, CMeHg(ambient) of rice leaves ranged from 0.700 to 46.6 ng g−1. The highest MeHg concentrations in leaves were evident during the tillering stage and concentrations subsequently decreased exponentially during later rice plant development (Figure 3A). CMeHg(ambient) in rice grains ranged from 2.60 to 56.2 ng g−1, with the highest values occurring during the milk stage and then decreasing exponentially (Figure 3B). A similar pattern of CMeHg(ambient) was found in other rice tissues (Figure S2A−C). Note that during each vegetation stage CMeHg(ambient) was consistent among the references and the three DMe199Hg treatments, implying that DMe199Hg in ambient air did not influence CMeHg(ambient) in D


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Figure 3. CMeHg(ambient)(A and B) and CMeHg(tracer)(C and D) in rice leaves and grains during different stages of growth in open top chamber experiments.

this variation is generally very small in plants with a Δ value of a few parts per thousand.35,90−92 Therefore, from the variation in Me202Hg/Me199Hg ratios in rice tissues, we can conclude that assimilation of DMeHg from air by the rice leaf is transferred to the bottom stalk, with only a small amount of this source reaching the rice root. The Me202Hg/Me199Hg ratios in grains with hull during the heading stage, and in brown rice during the milk stage and the ripening stage, all declined sharply with the increasing of DMe 199 Hg concentrations (Figure 4A−C), which was accompanied by decreasing concentrations in the leaves and the upper stalks. In contrast, in the reference OTCs, Me202Hg/ Me199Hg ratios of grain with hull and brown rice were stable (Figure 4E). The percentage difference of the ratio of Me202Hg/Me199Hg in rice grains and hulls between the DMeHg treatments and the reference is shown in Figure 4F, and for brown rice values were 30.5%, 40.9%, and 74.1% in the milk stage and 40.3%, 65.6%, and 76.9% in the ripening stage for 16 ± 9, 137 ± 92, and 329 ± 182 pg m−3 DMeHg treatments, respectively. These data indicate that brown rice accumulated Me199Hg with increasing of DMe199Hg levels in air during the growth seasons. Note that only a small increase (2.8%) in the percentage difference was evident from the milk stage to the ripening stage in the highest DMeHg treatment. In the soil 199Hg(II) amended treatment, the lowest ratios Me202Hg/Me199Hg among rice tissues were observed in roots and bottom stalks (Figure 4D), which contrasts with the pattern observed in OTCs experiments. In OTCs experiments, the ratios of Me202Hg/Me199Hg in hulls were significantly lower than those in brown rice during the milk and ripening stages, and yet this pattern was not evident in reference OTCs (Figure 4E) or the soil 199Hg(II) amended treatment (Figure 4D). These patterns indicate that assimilation and transfer pathways of MeHg from air are different from those of soil.

DMeHg assimilated by rice leaves from air is mostly stored in aboveground plant parts, including the human edible rice grain. Only a small amount of this DMeHg input reaches the rice root. 3.4. Mechanism of Methylmercury Accumulation in Rice in a Mercury Mining Area. In this study, stable Hg isotope field OTCs experiments validate that rice leaf can assimilate gaseous organic Hg from the atmosphere, and that this MeHg is mainly stored in aboveground parts including human edible rice grains. Previous GEM OTCs experiments, stable isotope tracer experiments, and field investigations have revealed that total/inorganic Hg in aboveground parts of crops, grasses, and leaves of trees largely originates from atmospheric sources through stomatal assimilation of GEM.40,42,93−95 A similar assimilation mechanism (i.e., stomatal assimilation of atmospheric DMeHg) could explain MeHg accumulation in rice plant. However, more detailed field research is needed to confirm this mechanism. High DMeHg concentrations (1.27−25.7 pg m−3) were observed in air beneath the rice canopy from our field investigation (in section 3.1). We applied these DMeHg levels to the response function developed from the DMe199Hg OTCs experiments (in section 3.2) to estimate the fraction of MeHg that could be derived from atmospheric DMeHg at the Shujing site in the Wanshan Hg mining area. Using this approach, we estimate that a mean concentration of 1.58 μg kg−1 with a range from 0.200 to 3.94 μg kg−1 MeHg in brown rice and 0.340 μg kg−1 with range from 0.0500 to 0.860 μg kg−1 MeHg in rice leaves could originate from atmospheric sources. Combining these values with the measured MeHg concentrations in rice plant sampled from the Shujing site (Figure S3), it is estimated that 15.5%, 10.8%, and 8.50% of the MeHg concentration in the brown rice, the leaf, and the upper stalk, respectively, could be attributed to atmospheric sources of E


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Figure 4. Ratios of Me202Hg to Me199Hg in soil and rice tissues during the growing season in open top chamber experiments (A, 16 ± 9; B, 137 ± 92; C, 329 ± 182 pg m−3 of DMeHg), soil 199Hg(II) treatment (D), and reference (E), and percentage difference of the ratios in rice grain and hull between DMeHg treatment and the reference (F). See the following equation: percentage difference (%) ÄÅ Å = 100 × ÅÅÅ(Me202Hg/Me199)(reference) ÅÇ ÉÑ Ñ 202 − (Me Hg/Me199Hg)(DMeHg treatment)ÑÑÑ ÑÖ

{

/(Me202Hg/Me199Hg)(reference)

}

DMeHg, while 99.5% of the MeHg in the root appears to be derived from the rice soil−water system (Figure 5). These observations potentially refine the mechanism of MeHg accumulation in rice that, in addition to soil, a fraction of

MeHg in rice plants can be derived from DMeHg emissions from flooded rice paddies in Hg mining areas and potentially systems contaminated by atmospheric Hg deposition. These findings provide a foundation for the remediation of MeHgpolluted rice paddies. Research should be undertaken to better understand the factors controlling DMeHg production and accumulation in rice paddies. With this mechanistic information, practices might be implemented to mitigate DMeHg production and decrease MeHg accumulation in rice grains.

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ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.est.8b01783. Figures and text detailing the assimilation of DMe199Hg by rice stalks and roots (PDF)

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AUTHOR INFORMATION

Corresponding Author

*Phone: +86 10 62849168; Fax number: +86 10-62849369; email: [email protected] (X.Z.).

Figure 5. Percentages of MeHg in rice derived from air and soil at the Shujing site in the Wanshan mercury mining area. F


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Zhangwei Wang: 0000-0002-0516-4536 Charles T. Driscoll: 0000-0003-2692-2890 Xiaoshan Zhang: 0000-0001-6124-7806 Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This research was funded by the Natural Science Foundation of China (No. 41373124, 41673113, and 41371461), and “Strategic Priority Research Program” of the Chinese Academy of Sciences (Grant No. XDB14020205). The authors would like to thank Jinsong Xiao from Guizhou Institute of Environmental Sciences Research and Design for his assistance in field works.

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Mechanism of Accumulation of Methylmercury in Rice (Oryza sativa L

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