Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

A hidden demethylation pathway removes mercury from rice plants and mitigates mercury flux to food chains

Nature Food volume 5, pages 72–82 (2024)Cite this article

Subjects

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.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Evidence of MeHg demethylation in vivo and Hg release from crops.
Fig. 2: Lines of evidence showing in vivo MeHg demethylation irrespective of microorganisms.
Fig. 3: Lines of evidence showing the dominant role of singlet oxygen in MeHg demethylation in rice plants.
Fig. 4: Health and economic benefits induced by MeHg demethylation in rice plants.

Similar content being viewed by others

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.

References

  1. UNEP. Global Mercury Assessment 2018. (UN Environment Programme, 2018).

  2. Karagas, M. R. et al. Evidence on the human health effects of low-level methylmercury exposure. Environ. Health Perspect. 120, 799–806 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Rice, G. E., Hammitt, J. K. & Evans, J. S. A probabilistic characterization of the health benefits of reducing methyl mercury intake in the United States. Environ. Sci. Technol. 44, 5216–5224 (2010).

    Article  ADS  CAS  PubMed  Google Scholar 

  4. Bellanger, M. et al. Economic benefits of methylmercury exposure control in Europe: monetary value of neurotoxicity prevention. Environ. Health 12, 1–10 (2013).

    Article  Google Scholar 

  5. Grandjean, P., Pichery, C., Bellanger, M. & Budtz-Jørgensen, E. Calculation of mercury’s effects on neurodevelopment. Environ. Health Perspect. 120, 452 (2012).

    Article  Google Scholar 

  6. Zhang, Y. et al. Global health effects of future atmospheric mercury emissions. Nat. Commun. 12, 3035 (2021).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  7. Chen, L. et al. Trans-provincial health impacts of atmospheric mercury emissions in China. Nat. Commun. 10, 1484 (2019).

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  8. Seller, P., Kelly, C. A., Rudd, J. W. M. & Mac Hutchon, A. R. Photodegradation of methylmercury in lakes. Nature 380, 694–697 (1996).

    Article  ADS  Google Scholar 

  9. Klapstein, S. J., Ziegler, S. E., Risk, D. A. & O’Driscoll, N. J. Quantifying the effects of photoreactive dissolved organic matter on methylmercury photodemethylation rates in freshwaters. Environ. Toxicol. Chem. 36, 1493–1502 (2017).

    Article  CAS  PubMed  Google Scholar 

  10. Kronberg, R. M., Schaefer, J. K., Björn, E. & Skyllberg, U. Mechanisms of methyl mercury net degradation in alder swamps: the role of methanogens and abiotic processes. Environ. Sci. Technol. Lett. 5, 220–225 (2018).

    Article  CAS  Google Scholar 

  11. Zhou, X. Q. et al. Microbial communities associated with methylmercury degradation in paddy soils. Environ. Sci. Technol. 54, 7952–7960 (2020).

    Article  ADS  CAS  PubMed  Google Scholar 

  12. Wu, Q. et al. Methanogenesis is an important process in controlling MeHg concentration in rice paddy soils affected by mining activities. Environ. Sci. Technol. 54, 13517–13526 (2020).

    Article  ADS  CAS  PubMed  Google Scholar 

  13. Barkay, T. & Gu, B. Demethylation—the other side of the mercury methylation coin: a critical review. ACS Environ. Au 2, 77–97 (2022).

    Article  CAS  PubMed  Google Scholar 

  14. Feyte, S., Gobeil, C., Tessier, A. & Cossa, D. Mercury dynamics in lake sediments. Geochim Cosmochim Acta 82, 92–112 (2012).

    Article  ADS  CAS  Google Scholar 

  15. Hammerschmidt, C. R. & Fitzgerald, W. F. Photodecomposition of methylmercury in an arctic Alaskan lake. Environ. Sci. Technol. 40, 1212–1216 (2006).

    Article  ADS  CAS  PubMed  Google Scholar 

  16. Lehnherr, I., St. Louis, V. L., Emmerton, C. A., Barker, J. D. & Kirk, J. L. Methylmercury cycling in high arctic wetland ponds: sources and sinks. Environ. Sci. Technol. 46, 10514–10522 (2012).

    Article  ADS  CAS  PubMed  Google Scholar 

  17. Xu, X. et al. Demethylation of methylmercury in growing rice plants: an evidence of self-detoxification. Environ. Pollut. 210, 113–120 (2016).

    Article  CAS  PubMed  Google Scholar 

  18. Li, Y. et al. The influence of iron plaque on the absorption, translocation and transformation of mercury in rice (Oryza sativa L.) seedlings exposed to different mercury species. Plant Soil 398, 87–97 (2016).

    Article  CAS  Google Scholar 

  19. Strickman, R. J. & Mitchell, C. P. J. Accumulation and translocation of methylmercury and inorganic mercury in Oryza sativa: an enriched isotope tracer study. Sci. Total Environ. 574, 1415–1423 (2017).

    Article  ADS  CAS  PubMed  Google Scholar 

  20. Liu, J., Meng, B., Poulain, A. J., Meng, Q. & Feng, X. Stable isotope tracers identify sources and transformations of mercury in rice (Oryza sativa L.) growing in a mercury mining area. Fundam. Res. 1, 259–268 (2021).

    Article  CAS  Google Scholar 

  21. Liu, M. et al. Rice life cycle-based global mercury biotransport and human methylmercury exposure. Nat. Commun. 10, 5164 (2019).

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  22. Gong, Y. et al. Bioaccessibility-corrected risk assessment of urban dietary methylmercury exposure via fish and rice consumption in China. Sci. Total Environ. 630, 222–230 (2018).

    Article  ADS  CAS  PubMed  Google Scholar 

  23. Cui, W. et al. Occurrence of methylmercury in rice-based infant cereals and estimation of daily dietary intake of methylmercury for infants. J. Agric. Food Chem. 65, 9569–9578 (2017).

    Article  CAS  PubMed  Google Scholar 

  24. Zhu, W. et al. Global observations and modeling of atmosphere–surface exchange of elemental mercury: a critical review. Atmos. Chem. Phys. 16, 4451–4480 (2016).

    Article  ADS  CAS  Google Scholar 

  25. Hsu-Kim, H., Kucharzyk, K. H., Zhang, T. & Deshusses, M. A. Mechanisms regulating mercury bioavailability for methylating microorganisms in the aquatic environment: a critical review. Environ. Sci. Technol. 47, 2441–2456 (2013).

    Article  ADS  CAS  PubMed  Google Scholar 

  26. Bishop, K. et al. Recent advances in understanding and measurement of mercury in the environment: terrestrial Hg cycling. Sci. Total Environ. 721, 137647 (2020).

    Article  ADS  CAS  PubMed  Google Scholar 

  27. Zhou, J., Obrist, D., Dastoor, A., Jiskra, M. & Ryjkov, A. Vegetation uptake of mercury and impacts on global cycling. Nat. Rev. Earth Environ. 2, 269–284 (2021).

    Article  ADS  Google Scholar 

  28. Obrist, D. et al. A review of global environmental mercury processes in response to human and natural perturbations: changes of emissions, climate, and land use. Ambio 47, 116–140 (2018).

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  29. Zhang, T. & Hsu-Kim, H. Photolytic degradation of methylmercury enhanced by binding to natural organic ligands. Nat. Geosci. 3, 473–476 (2010).

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  30. Luo, H., Cheng, Q. & Pan, X. Photochemical behaviors of mercury (Hg) species in aquatic systems: a systematic review on reaction process, mechanism, and influencing factor. Sci. Total Environ. 720, 137540 (2020).

    Article  ADS  CAS  PubMed  Google Scholar 

  31. Gill, S. S. & Tuteja, N. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol. Biochem. 48, 909–930 (2010).

    Article  CAS  PubMed  Google Scholar 

  32. Chen, T. & Fluhr, R. Singlet oxygen plays an essential role in the root’s response to osmotic stress. Plant Physiol. 177, 1717–1727 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Koh, E., Carmieli, R., Mor, A. & Fluhr, R. Singlet oxygen-induced membrane disruption and serpin–protease balance in vacuolar-driven cell death. Plant Physiol. 171, 1616–1625 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  34. Taverne, Y. J. et al. Reactive oxygen species: radical factors in the evolution of animal life: a molecular timescale from Earth’s earliest history to the rise of complex life. Bioessays 40, 1–9 (2018).

    Article  Google Scholar 

  35. Sheng, F. et al. A new pathway of monomethylmercury photodegradation mediated by singlet oxygen on the interface of sediment soil and water. Environ. Pollut. 248, 667–675 (2019).

    Article  CAS  PubMed  Google Scholar 

  36. Shapiro, A. M. & Chan, H. M. Characterization of demethylation of methylmercury in cultured astrocytes. Chemosphere 74, 112–118 (2008).

    Article  ADS  CAS  PubMed  Google Scholar 

  37. Yasutake, A. & Hirayama, K. Evaluation of methylmercury biotransformation using rat liver slices. Arch. Toxicol. 75, 400–406 (2001).

    Article  CAS  PubMed  Google Scholar 

  38. Suda, I., Totoki, S. & Takahashi, H. Degradation of methyl and ethyl mercury into inorganic mercury by oxygen free radical-producing systems: involvement of hydroxyl radical. Arch. Toxicol. 65, 129–134 (1991).

    Article  CAS  PubMed  Google Scholar 

  39. Crump, K. S., Kjellström, T., Shipp, A. M., Silvers, A. & Stewart, A. Influence of prenatal mercury exposure upon scholastic and psychological test performance: benchmark analysis of a New Zealand cohort. Risk Anal. 18, 701–713 (1998).

    Article  CAS  PubMed  Google Scholar 

  40. Grandjean, P. et al. Cognitive deficit in 7-year-old children with prenatal exposure to methylmercury. Neurotoxicol. Teratol. 19, 417–428 (1997).

    Article  CAS  PubMed  Google Scholar 

  41. Myers, G. J. et al. Prenatal methylmercury exposure from ocean fish consumption in the Seychelles child development study. Lancet 361, 1686–1692 (2003).

    Article  CAS  PubMed  Google Scholar 

  42. Rothenberg, S. E. et al. Stable mercury isotopes in polished rice (Oryza sativa L.) and hair from rice consumers. Environ. Sci. Technol. 51, 6480–6488 (2017).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  43. Salkever, D. S. Updated estimates of earnings benefits from reduced exposure of children to environmental lead. Environ. Res. 70, 1–6 (1995).

    Article  CAS  PubMed  Google Scholar 

  44. Heckman, J. J., Stixrud, J. & Urzua, S. The effects of cognitive and noncognitive abilities on labor market outcomes and social behavior. J. Labor. Econ. 24, 411–482 (2006).

  45. Zhang, W. et al. Economic evaluation of health benefits of mercury emission controls for China and the neighboring countries in East Asia. Energy Policy 106, 579–587 (2017).

    Article  Google Scholar 

  46. Hasanuzzaman, M. et al. Reactive oxygen species and antioxidant defense in plants under abiotic stress: revisiting the crucial role of a universal defense regulator. Antioxidants 9, 681 (2020).

  47. Rothenberg, S. E. & Feng, X. Mercury cycling in a flooded rice paddy. J. Geophys. Res. Biogeosci. 117, G03003 (2012).

  48. Tang, W. et al. Increased methylmercury accumulation in rice after straw amendment. Environ. Sci. Technol. 53, 6144–6153 (2019).

    Article  ADS  CAS  PubMed  Google Scholar 

  49. Lee, C. S. & Fisher, N. S. Microbial generation of elemental mercury from dissolved methylmercury in seawater. Limnol. Oceanogr. 64, 679–693 (2019).

    Article  ADS  CAS  PubMed  Google Scholar 

  50. Mence Chaintreuil, C. et al. Photosynthetic bradyrhizobia are natural endophytes of the African wild rice Oryza breviligulata. Appl. Environ. Microbiol. 66, 5437–5447 (2000).

    Article  ADS  Google Scholar 

  51. Han, X., Li, Y., Li, D. & Liu, C. Role of free radicals/reactive oxygen species in MeHg photodegradation: importance of utilizing appropriate scavengers. Environ. Sci. Technol. 51, 3784–3793 (2017).

    Article  ADS  CAS  PubMed  Google Scholar 

  52. Štrok, M., Hintelmann, H. & Dimock, B. Development of pre-concentration procedure for the determination of Hg isotope ratios in seawater samples. Anal. Chim. Acta 851, 57–63 (2014).

    Article  PubMed  Google Scholar 

  53. Hintelmann, H. & Ogrinc, N. Determination of stable mercury isotopes by ICP/MS and their application in environmental studies. In Biogeochemistry of Environmentally Important Trace Elements 321–338 (ACS, 2003).

  54. Krieger-Liszkay, A., Trösch, M. & Krupinska, K. Generation of reactive oxygen species in thylakoids from senescing flag leaves of the barley varieties Lomerit and Carina. Planta 241, 1497–1508 (2015).

    Article  CAS  PubMed  Google Scholar 

  55. Ossola, R., Jönsson, O. M., Moor, K. & McNeill, K. Singlet oxygen quantum yields in environmental waters. Chem. Rev. 121, 4100–4146 (2021).

    Article  CAS  PubMed  Google Scholar 

  56. Frisch, M. J. et al. Gaussian 16. (Gaussian, Inc., 2016).

  57. Zhao, Y. & Truhlar, D. G. The M06 suite of density functionals for main group thermochemistry, thermochemical kinetics, noncovalent interactions, excited states, and transition elements: two new functionals and systematic testing of four M06-class functionals and 12 other functionals. Theor. Chem. Acc. 120, 215–241 (2008).

    Article  CAS  Google Scholar 

  58. Andrae, D., Iubermann, U. H., Dolg, M., Stoll, H. & Preub, H. Energy-adjusted ab initio pseudopotentials for the second and third row transition elements. Theor. Chim. Acta 77, 123–141 (1990).

    Article  CAS  Google Scholar 

  59. Marenich, A. V., Cramer, C. J. & Truhlar, D. G. Universal solvation model based on solute electron density and on a continuum model of the solvent defined by the bulk dielectric constant and atomic surface tensions. J. Phys. Chem. B 113, 6378–6396 (2009).

    Article  CAS  PubMed  Google Scholar 

Download references

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).

Author information

Author notes

  1. These authors contributed equally: Wenli Tang, Xu Bai, Yang Zhou.

Authors and Affiliations

  1. School of the Environment, Nanjing University, State Key Laboratory of Pollution Control and Resource Reuse, Nanjing, China

    Wenli Tang, Yang Zhou, Mengjie Wu, Yanan Yang, Jiaqi Wang, Shouying Li, Xu-Xiang Zhang, Hongqiang Ren & Huan Zhong

  2. Key Laboratory for Biomedical Effects of Nanomaterials and Nanosafety, Institute of High Energy Physics (IHEP), Chinese Academy of Sciences (CAS), Beijing, China

    Xu Bai, Diandou Xu, Hong Li, Zhifang Chai, Yuxi Gao & Jiating Zhao

  3. University of Chinese Academy of Sciences, Beijing, China

    Xu Bai

  4. Department of Ecoscience, Arctic Research Centre, Aarhus University, Roskilde, Denmark

    Christian Sonne

  5. Sustainability Cluster, School of Engineering, University of Petroleum and Energy Studies, Dehradun, India

    Christian Sonne

  6. Higher Institution Centre of Excellence (HICoE), Institute of Tropical Aquaculture and Fisheries (AKUATROP), Universiti Malaysia Terengganu, Kuala Nerus, Malaysia

    Su Shiung Lam

  7. Center for Global Health Research (CGHR), Saveetha Institute of Medical and Technical Sciences (SIMATS), Saveetha University, Chennai, India

    Su Shiung Lam

  8. Department of Chemistry and School of the Environment, Trent University, Peterborough, Ontario, Canada

    Holger Hintelmann

  9. Department of Physical and Environmental Sciences, University of Toronto Scarborough, Scarborough, Ontario, Canada

    Carl P. J. Mitchell

  10. Environmental Sciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, USA

    Alexander Johs & Baohua Gu

  11. Faculty of Sciences and Technology, Civil Engineering Research and Innovation for Sustainability Center, University of Algarve, Faro, Portugal

    Luís Nunes

  12. Key Laboratory of Soil Environment and Pollution Remediation, Institute of Soil Science, Chinese Academy of Sciences, Nanjing, China

    Cun Liu

  13. College of Life Science and Technology, Jinan University, Guangzhou, China

    Naixian Feng

  14. State Key Laboratory of Pharmaceutical Biotechnology, School of Life Sciences, Nanjing University, Nanjing, China

    Sihai Yang

  15. School of Architecture and Civil Engineering, Institute of Foundation Engineering, Water and Waste Management, Laboratory of Soil and Groundwater Management, University of Wuppertal, Wuppertal, Germany

    Jörg Rinklebe

  16. Tianjin Key Laboratory of Environmental Technology for Complex Trans-Media Pollution, College of Environmental Science and Engineering, Nankai University, Tianjin, China

    Yan Lin

  17. Key Laboratory of Geographic Information Science (Ministry of Education), School of Geographic Sciences, East China Normal University, Shanghai, China

    Long Chen

  18. School of Atmospheric Sciences, Nanjing University, Nanjing, China

    Yanxu Zhang

  19. State Key Joint Laboratory of Environmental Simulation and Pollution Control, School of Environment, Tsinghua University, Beijing, China

    Qingru Wu

  20. State Environmental Protection Key Laboratory of Sources and Control of Air Pollution Complex, Beijing, China

    Qingru Wu

  21. Korea Biochar Research Center, APRU Sustainable Waste Management Program and Division of Environmental Science and Ecological Engineering, Korea University, Seoul, Republic of Korea

    Yong Sik Ok

  22. State Key Laboratory of Environmental Chemistry and Ecotoxicology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing, China

    Guibin Jiang

  23. State Key Laboratory of Radiation Medicine and Protection, Soochow University, Suzhou, China

    Zhifang Chai

  24. Department of Environmental Science, Zhejiang University, Hangzhou, China

    Jiating Zhao

Authors
  1. Wenli Tang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xu Bai
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yang Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Christian Sonne
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mengjie Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Su Shiung Lam
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Holger Hintelmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Carl P. J. Mitchell
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Alexander Johs
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Baohua Gu
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Luís Nunes
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Cun Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Naixian Feng
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Sihai Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Jörg Rinklebe
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Yan Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

  17. Long Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  18. Yanxu Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  19. Yanan Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  20. Jiaqi Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  21. Shouying Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  22. Qingru Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  23. Yong Sik Ok
    View author publications

    You can also search for this author in PubMed Google Scholar

  24. Diandou Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  25. Hong Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  26. Xu-Xiang Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  27. Hongqiang Ren
    View author publications

    You can also search for this author in PubMed Google Scholar

  28. Guibin Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  29. Zhifang Chai
    View author publications

    You can also search for this author in PubMed Google Scholar

  30. Yuxi Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

  31. Jiating Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  32. Huan Zhong
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

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.

Corresponding authors

Correspondence to Christian Sonne, Yuxi Gao, Jiating Zhao or Huan Zhong.

Ethics declarations

Competing interests

The authors declare no competing interests.

Peer review

Peer review information

Nature Food thanks Kevin Bishop, Xuejun Wang and Ping Li for their contribution to the peer review of this work.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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.

Reporting Summary

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

This .zip file contains the original photos presented in Extended Data Fig. 7b.

Source Data Fig. 4

This file contains the ArcMap files presented in Fig. 4.

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

This .ppt file contains the editable figures and Extended Data figures.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s43016-023-00910-x

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing