Abstract
Dietary exposure to methylmercury (MeHg) causes irreversible damage to human cognition and is mitigated by photolysis and microbial demethylation of MeHg. Rice (Oryza sativa L.) has been identified as a major dietary source of MeHg. However, it remains unknown what drives the process within plants for MeHg to make its way from soils to rice and the subsequent human dietary exposure to Hg. Here we report a hidden pathway of MeHg demethylation independent of light and microorganisms in rice plants. This natural pathway is driven by reactive oxygen species generated in vivo, rapidly transforming MeHg to inorganic Hg and then eliminating Hg from plants as gaseous Hg°. MeHg concentrations in rice grains would increase by 2.4- to 4.7-fold without this pathway, which equates to intelligence quotient losses of 0.01–0.51 points per newborn in major rice-consuming countries, corresponding to annual economic losses of US$30.7–84.2 billion globally. This discovered pathway effectively removes Hg from human food webs, playing an important role in exposure mitigation and global Hg cycling.
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Data availability
All the data supporting the findings are included in the main text, Supplementary Information and the Source Data. The databases used in this study are Food and Agriculture Organization (http://www.fao.org/faostat/#en/#dat), World Bank (http://data.worldbank.org/indicator/NY.GDP.PCAP.PP.CD and http://data.worldbank.org/indicator/NY.GDP.PCAP.KD.ZG), World Population Perspective 2019 (https://population.un.org/wpp/) and Natural Earth (https://www.naturalearthdata.com/downloads/10m-cultural-vectors/). Source data are provided with this paper.
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Acknowledgements
The authors gratefully acknowledge L. Gan from Nanjing Agriculture University for the advice on endophytes. Y.G. is supported by National Natural Science Foundation of China (U2032201). W.T. appreciates the financial support from National Natural Science Foundation of China (42107223), Fundamental Research Funds for the Central Universities (021114380175) and Natural Science Foundation of Jiangsu Province (BK20190319). J.Z. is thankful for the support from National Natural Science Foundation of China (12222509). H.H. acknowledges the funding from the NSERC Discovery Grant Program (RGPIN-2018-05421). S.L. appreciates Golden Goose Research Grant Scheme (GGRG) (UMT/RMIC/2-2/25 Jld 5 (64), Vot 55191). A.J. and B.G. are supported by the Office of Biological and Environmental Research within the Office of Science of the US Department of Energy at Oak Ridge National Laboratory, which is managed by UT-Battelle, LLC, under contract number DE-AC05-00OR22725 with the US Department of Energy. H.R. gets support from National Natural Science Foundation of China (52388101).
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H.Z., J.Z. and Y.G. led this project and designed all experiments. W.T. carried out the enriched isotope experiment under the supervision of H.H.; W.T., X.B., Y. Zhou, Y.Y., J.W. and S.L. conducted the crop experiment, rice growth stage experiment, Hg release experiment, homogenate experiment and quencher addition experiment under the supervisions of J.Z., Y.G. and H.Z.; W.T. estimated the avoided IQ decrements/economic benefits and Hg releases; L.N. helped conduct the sensitivity analysis, and C.L. conducted DFT calculations. W.T., H.Z. and C.S. led the manuscript writing and revision, and all coauthors participated in the writing and/or editing.
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Extended data
Extended Data Fig. 1 The design of the enriched isotope experiment (a), and the contents of ambient Hg (b and c) and 200Hg (d and e) in rice tissues.
T0 refers to the time when exposure started (Me202Hg and I200Hg spiked into solutions); T1 refers to the time when exposure ended and plants were transferred (Only notable proportion of I200Hg remained in the solution, Supplementary Text 3); T2 and T3 refer to times when plants were further cultivated in Hg-free solution for 24 h (T2) and 72 h (T3), respectively. The contents of both THg and MeHg are calculated as the total mass (ng) to exclude the effect of biomass variability on concentration (that is, biodilution). For panels (b) to (e), data are shown as mean ± SD, n = 3 replicates. Asterisk (*) indicates significant (p < 0.05, one-way ANOVA) differences between two time points. The number of circles on the left and right margins of each bar correspond to three replicates of MeHg and THg, respectively.
Extended Data Fig. 2 Contents of T202Hg and Me202Hg in solutions of the enriched isotope experiment.
T0 refers to the time when exposure started; T1 refers to the time when exposure ended and plants were transferred; T2 and T3 refer to times when plants were further cultivated in Hg-free solution for 24 h (T2) and 72 h (T3), respectively. Hg in cysteine wash and water wash includes the washing solutions for both roots and shoots. The contents of both THg and MeHg are calculated as the total mass (ng) in solution. Data are presented as Mean ± SD; for the bar of THg in T2+T3 cysteine wash, n = 4 replicates including a duplicate measurement; n = 2 for the bars of THg and MeHg in T2+T3 water wash due to experimental design; n = 3 replicates for the rest bars. Each replicate is depicted as a circle on the bar.
Extended Data Fig. 3 The demethylation ratios (DRs) in rice plants after exposure to different concentrations of MeHg (a) and to 0.8 μg/L MeHg in different matrices (b).
Note that experiments for panels (a) and (b) were conducted separately and thus the slightly lower DR in plants treated with CaCl2 solution (b) compared with that in panel (a) is likely due to differences in the growth condition. Mean ± SD, n = 3 replicates. Noted that in panel a, DR at concentration of 0 was quantified separately and 4 replicates were set. Each replicate is depicted as a circle on the bar.
Extended Data Fig. 4 Experimental design and Hg distribution after 80-h exposure in the Hg release experiment.
It should be noted that this is a conceptual scheme, and details about Hg proportions and the recovery rate can be found in Supplementary Table 9.
Extended Data Fig. 5 The concentrations of MeHg and THg in solution after exposure in the Hg release experiment.
N.S. indicates no significant difference between two parameters (p > 0.05, one-way ANOVA). Mean ± SD, n = 3 replicates. Each replicate is depicted as a circle on the bar.
Extended Data Fig. 6 The effect of light on MeHg demethylation in vivo (a) and in vitro (b).
N.S. indicates no significant difference between two treatments (p > 0.05, one-way ANOVA). Mean ± SD, n = 3 replicates. Each replicate is depicted as a circle on the bar.
Extended Data Fig. 7 The response of MeHg demethylation in root homogenates of rice plants to radical quencher additions (a) and the appearance of singlet oxygen from rice plants (1-, 2- and 4-month-old, left to right in panel b).
THF instead of DMFR was used in 1-month-old plants to scavenge singlet oxygen since the type of quencher has only a minor effect on the DR. In panel (a), data are shown as mean ± SD, n = 3 replicates. Each replicate is depicted as circle on the bar. Original photos in panel b are provided as Source Data.
Extended Data Fig. 8 Lines of evidence supporting the feasibility of using homogenates to detect the production of singlet oxygen.
The EPR signal of singlet oxygen in supernatant fraction (< 0.22 μm) under the light or dark condition (a), and its signal (b) and spin concentrations in homogenates with different degrees of homogenization (c).
Extended Data Fig. 9 Theoretic evidence supporting MeHg demethylation by singlet oxygen.
The optimized geometries for the reactants, transition states and products for reactions of Hg-C bond cleavage in MeHg by the attack of singlet oxygen, or Hg-C bond cleavage in MeHg-GSH in the presence/absence of the attack of singlet oxygen (a) and Gibbs free-energy profiles of Hg-C bond cleavages in all reaction systems (b).
Extended Data Fig. 10 The demethylation ratio of MeHg in the supernatant of root homogenate (< 0.22 μm fraction) without or with singlet oxygen quenched (a) and in singlet oxygen-generating chemical system in the absence or presence of GSH (b).
In (a), data are presented as mean ± SD, n = 3 replicates. In (b), this experiment was repeated 3 times, and 3 replicates were set each time; thus, data are depicted as mean ± SD, n = 9 replicates. Each replicate is depicted as a circle on the bar.
Supplementary information
Supplementary Information
This file contains 2 sections of Methods, 9 sections of Discussion, 63 References and 11 Supplementary Tables.
Source data
Source Data Figs. 1–4
This file contains the raw data plotted in Figs. 1–4 in the main text.
Source Data Extended Data Figs. 1–10
This file contains the raw data plotted in Extended Data Figs. 1–10.
Source Data Fig. 3b and Extended Data Fig. 7b
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Source Data Fig. 4
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Source Data Fig. 4
This file contains all the parameters used in the calculations of IQ decrements and economic benefits for 159 countries, as well as the results.
Source Data All Figures and Extended Data Figures
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Tang, W., Bai, X., Zhou, Y. et al. A hidden demethylation pathway removes mercury from rice plants and mitigates mercury flux to food chains. Nat Food 5, 72–82 (2024). https://doi.org/10.1038/s43016-023-00910-x
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DOI: https://doi.org/10.1038/s43016-023-00910-x
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