Demethylation of Methylmercury in Growing Rice Plants: an Evidence of Self-Detoxification

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Demethylation of Methylmercury in Growing Rice Plants: an Evidence of Self-Detoxification Environmental Pollution 210 (2016) 113e120 Contents lists available at ScienceDirect Environmental Pollution journal homepage: www.elsevier.com/locate/envpol Demethylation of methylmercury in growing rice plants: An evidence of self-detoxification Xiaohan Xu a, b, 1, Jiating Zhao a, 1, Yunyun Li a, b, Yuqin Fan c, Nali Zhu d, Yuxi Gao a, Bai Li a, * Hanyu Liu e, Yu-Feng Li a, a State Environmental Protection Engineering Center for Mercury Pollution Prevention and Control, and Laboratory of Metallomics and Nanometallomics, Institute of High Energy Physics, Chinese Academy of Sciences, Beijing 100049, China b University of Chinese Academy of Sciences, Beijing 100049, China c Shandong Maternity and Child Care Hospital, Jinan 250001, China d Laboratory of Proteomics, Protein Science Core Facility Center, Institute of Biophysics, Chinese Academy of Sciences, Beijing 100101, China e Beijing National Day School, Beijing 100049, China article info abstract Article history: Mercury (Hg) is a global pollutant that poses a serious threat to human and the environment. Rice was Received 17 July 2015 found as an important source for human exposure to Hg in some areas. In this study, the transportation Received in revised form and transformation of IHg and MeHg in rice plants exposed to IHg or MeHg were investigated. The IHg 8 December 2015 and MeHg concentrations in rice roots and shoots collected every five days were analyzed by HPLC-ICP- Accepted 8 December 2015 MS and SR-XANES. When exposed to MeHg, the percent of IHg in rice roots and shoots increased while Available online 18 December 2015 MeHg decreased significantly, suggesting prominent demethylation of MeHg occurred. However no Handling editor: Eddy Y. Zeng notable MeHg was found in both roots and shoots of rice plant when exposed to IHg. SR-XANES analysis further confirmed the demethylation of MeHg with rice. This study provides a new finding that deme- Keywords: thylation of MeHg could occur in growing rice, which may be a self-defense process of rice plant. Methylmercury © 2015 Elsevier Ltd. All rights reserved. Inorganic mercury Demethylation Rice SR-XANES 1. Introduction magnify through the food chain. For humans, the primary source of MeHg exposure is the consumption of contaminated foodstuff Mercury (Hg) is a global pollutant that poses a serious threat to (Gilmour et al., 1992; Celo et al., 2006; Harris et al., 2003; human health and the environment. Due to its bioaccumulation, Guimaraes et al., 2000). Once absorbed, MeHg can easily cause long-range transportation, strong neurotoxicity and persistence in permanent damage to central nervous system, especially for the the environment, Hg and its compounds have been regarded as developing fetuses and infants (Clarkson, 1997). priority-controlled pollutants by many agencies (Mastrine et al., Wetlands and the sediment-water interfaces are predominant 1999). As the largest producer, user and emitter of Hg in the sites in the environment where the methylation of Hg usually world, China is faced with great pressure of Hg pollution (Cheng happens (Guimaraes et al., 2000; Driscoll et al., 1998). Microbial and Hu, 2012; Zhang and Wong, 2007). activity is an important way of Hg methylation. Iron-reducing The toxicity of Hg is strongly dependent on its chemical species, bacteria, sulfate reducing bacteria and methanogens are three among which methylmercury (MeHg) is the most poisonous form main MeHg producers (Siciliano and Lean, 2002; King et al., 2001). and more prone to bio-accumulation in organisms. MeHg in the Recent studies found that methylation can also occur in the paddy environment can be generated by methylation of the inorganic field ecosystem and the produced MeHg can be absorbed and mercury (IHg) through biological and chemical processes and can accumulated in rice grain (Galloway and Branfireun, 2004). As is reported in Qingzhen and Wanshan District, Guizhou Province, where acetic acid plants and largest mercury mines exist, the * Corresponding author. concentrations of mercury in the local soils can reach 83.9 mg/kg E-mail address: [email protected] (Y.-F. Li). and 496 mg/kg, respectively. Also in these areas, the total mercury 1 These authors contributed equally to this work. http://dx.doi.org/10.1016/j.envpol.2015.12.013 0269-7491/© 2015 Elsevier Ltd. All rights reserved. 114 X. Xu et al. / Environmental Pollution 210 (2016) 113e120 (THg) concentrations in rice grains can be up to 8.8e569 mg/kg, in days for four times, respectively. Nutrient solutions with different which the concentration of MeHg is 1.20e170 mg/kg (Li et al., 2010a; dosages of IHg or MeHg were collected and renewed every time Qiu et al., 2008; Horvat et al., 2003). after sampling. The culture media was updated every five days with As a staple food for many people around the world, especially in new prepared Hg solutions. East and Southeast Asia, rice has attracted constant attention over the last several decades due to the increasing soil pollution (Horvat et al., 2003; Zhang et al., 2010a). For example, in some Hg mine 2.2. Total Hg (THg) analysis in IHg or MeHg exposed rice plants areas in China, the concentration of Hg in rice is much higher than the national limit of Hg in food, which has restricted the develop- Tissues separated from rice seedlings under Hg exposure were ment of agriculture and caused great damage to residents' health lyophilized at À50C and ground into fine powders after rinsed (Wang et al., 2011; Meng et al., 2014). Our previous work, whatever with deionized water completely. A triplicate of 20e30 mg each for the lab or field studies, indicated that the ratio of MeHg to IHg powdered sample was digested with a freshly prepared mixture of increased gradually from the roots to the grains in rice plants. MeHg 5 mL HNO3 (BV-III) and 0.5 mL H2O2 (MOS) in a digestion tank. The even account for over 50% of the total mercury in the rice grains mixtures were left overnight at room temperature and digested at (Zhao et al., 2014; Li et al., 2015). 160C in a series of sealed pots for 5 h (Zhao et al., 2013a). Subse- Studying the processes of uptake, transportation, trans- quently, the mixtures were volatilized to the volume of approxi- formation and accumulation of different forms of Hg in rice plant is mately 1 mL at the temperature of 90 C and diluted to 4 mL with helpful to understand the mechanism of Hg accumulation in rice 2% (v/v) HNO3 containing 0.1% (v/v) b-mercaptoethanol for Hg grain. Hg demethylation and methylation have ever been found in measurement. lower aquatic plants like unicellular diatom (Deng et al., 2013) and The concentration of total Hg in rice tissues were measured by some kinds of fish (Wang et al., 2013). However, it is still unclear if using ICP-MS (Thermo Elemental X7, USA) in a normal mode. The demethylation and methylation of Hg could also occur in higher running conditions of ICP-MS were listed as following: nebulizer plants like rice plant. Besides, demethylation of MeHg might be a (glass concentric), plasma gas flow (13.0 L/min), auxiliary gas flow self-defense process for organisms when facing Hg stress (Marie (0.70 L/min), nebulizer gas flow (0.72 L/min), collision gas (7.28% (v/ et al., 1995; Collin et al., 2009). v) H2 in He), dwell time (100 ms). A normal tuning solution (Bi In this study, rice plants were exposed to IHg or MeHg under 10 mg/L) was used during the process of optimization every time. hydroponic conditions. The concentrations of both IHg and MeHg Transportation factor (TF), the ratio of THg in rice shoots to that in roots and shoots were investigated using HPLC-ICP-MS in com- in rice roots, is used to express the Hg transportation ability from bination with synchrotron radiation X-ray absorption near-edge roots to aerial parts of rice plants (Meharg and Hartley-Whitaker, structure (SR-XANES) techniques to see if methylation or deme- 2002). thylation could occur or not in growing rice. 2. Materials and methods 2.3. IHg and MeHg analysis in IHg or MeHg exposed rice plants According to previous studies, in typical Hg polluted areas such Forty mg fine powders of roots and shoots were transferred into as Wanshan and Qingzhen Districts, Guizhou province of South- 5 mL centrifuge tubes with 2.5 mL 6 M HCl added to extract IHg and western China, Hg polluted water from abandoned Hg mining and MeHg in the samples. Following 45 min of ultrasonic oscillation, the discharged by chemical factories were used as irrigation sources for mixtures were shaken at 28 C overnight by using an orbital shaker. farmlands and paddy fields (Li et al., 2015; Matsuyama et al., 2009). Subsequently, after 2 extractions, the upper extracts were trans- The Hg concentration in Hg polluted water and soil in the sample ferred into 15 mL centrifuge tubes and pH was adjusted to the value sites of Wanshan District is about 116.2 mg/L and 29.6 mg/kg, of 6.7 by adding ammonium water. 1 mL of freshly adjusted solu- respectively (Zhao et al., 2014). In this study, the exposure dosage of tions were extracted and diluted to 4 mL with previously prepared Hg is set to be 0.5 mg/L and 1 mg/L to roughly simulate the growth mobile phase and filtered by a 0.22 mm microporous membrane conditions of rice in Hg polluted areas. before analysis. The IHg and MeHg concentrations in the nutrient solutions collected were also analyzed following the aforemen- 2.1. Rice cultivation and sample preparation tioned procedure. The IHg stock standard solutions (HgCl2,GBW 08617, National Research Centre for CRMs, China) and MeHg stock Mature and undamaged rice seeds (Oryza sativa L.) selected in standard solutions (CH3HgCl, GBW 08675, National Research advance were sterilized with 10%(V/V) sodium chloride (NaCl) so- Centre for CRMs, China) were diluted with mobile phase to obtain lution for 15 min and washed with running water for 6 h.
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