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

Wenli Tang; Xu Bai; Yang Zhou; Christian Sonne; Mengjie Wu; Su Shiung Lam; Holger Hintelmann; Carl P.J. Mitchell; Alexander Johs; Baohua Gu; Luís Nunes; Cun Liu; Naixian Feng; Sihai Yang; Jörg Rinklebe; Yan Lin; Long Chen; Yanxu Zhang; Yanan Yang; Jiaqi Wang; Shouying Li; Qingru Wu; Yong Sik Ok; Diandou Xu; Hong Li; Xu Xiang Zhang; Hongqiang Ren; Guibin Jiang; Zhifang Chai; Yuxi Gao; Jiating Zhao; Huan Zhong

doi:10.1038/s43016-023-00910-x

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

Wenli Tang
, Xu Bai
, Yang Zhou
, Christian Sonne
, Mengjie Wu
, Su Shiung Lam
, Holger Hintelmann
, Carl P.J. Mitchell
, Alexander Johs
, Baohua Gu
, Luís Nunes
, Cun Liu
, Naixian Feng
, Sihai Yang
, Jörg Rinklebe
, Yan Lin
, Long Chen
, Yanxu Zhang
, Yanan Yang
, Jiaqi Wang

Shouying Li, Qingru Wu, Yong Sik Ok, Diandou Xu, Hong Li, Xu Xiang Zhang, Hongqiang Ren, Guibin Jiang, Zhifang Chai, Yuxi Gao, Jiating Zhao, Huan Zhong

Biogeochemical Dynamics

Research output: Contribution to journal › Article › peer-review

16 Scopus citations

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.

Original language	English
Pages (from-to)	72-82
Number of pages	11
Journal	Nature Food
Volume	5
Issue number	1
DOIs	https://doi.org/10.1038/s43016-023-00910-x
State	Published - Jan 2024

Funding

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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10.1038/s43016-023-00910-x

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Tang, W., Bai, X., Zhou, Y., Sonne, C., Wu, M., Lam, S. S., Hintelmann, H., Mitchell, C. P. J., Johs, A., Gu, B., Nunes, L., Liu, C., Feng, N., Yang, S., Rinklebe, J., Lin, Y., Chen, L., Zhang, Y., Yang, Y., ... Zhong, H. (2024). A hidden demethylation pathway removes mercury from rice plants and mitigates mercury flux to food chains. Nature Food, 5(1), 72-82. https://doi.org/10.1038/s43016-023-00910-x

@article{ffd693d4e97044e88273d3229ba9b63a,

title = "A hidden demethylation pathway removes mercury from rice plants and mitigates mercury flux to food chains",

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.",

author = "Wenli Tang and Xu Bai and Yang Zhou and Christian Sonne and Mengjie Wu and Lam, \{Su Shiung\} and Holger Hintelmann and Mitchell, \{Carl P.J.\} and Alexander Johs and Baohua Gu and Lu{\'i}s Nunes and Cun Liu and Naixian Feng and Sihai Yang and J{\"o}rg Rinklebe and Yan Lin and Long Chen and Yanxu Zhang and Yanan Yang and Jiaqi Wang and Shouying Li and Qingru Wu and Ok, \{Yong Sik\} and Diandou Xu and Hong Li and Zhang, \{Xu Xiang\} and Hongqiang Ren and Guibin Jiang and Zhifang Chai and Yuxi Gao and Jiating Zhao and Huan Zhong",

note = "Publisher Copyright: {\textcopyright} 2024, The Author(s), under exclusive licence to Springer Nature Limited.",

year = "2024",

month = jan,

doi = "10.1038/s43016-023-00910-x",

language = "English",

volume = "5",

pages = "72--82",

journal = "Nature Food",

issn = "2662-1355",

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Tang, W, Bai, X, Zhou, Y, Sonne, C, Wu, M, Lam, SS, Hintelmann, H, Mitchell, CPJ, Johs, A, Gu, B, Nunes, L, Liu, C, Feng, N, Yang, S, Rinklebe, J, Lin, Y, Chen, L, Zhang, Y, Yang, Y, Wang, J, Li, S, Wu, Q, Ok, YS, Xu, D, Li, H, Zhang, XX, Ren, H, Jiang, G, Chai, Z, Gao, Y, Zhao, J & Zhong, H 2024, 'A hidden demethylation pathway removes mercury from rice plants and mitigates mercury flux to food chains', Nature Food, vol. 5, no. 1, pp. 72-82. https://doi.org/10.1038/s43016-023-00910-x

TY - JOUR

T1 - A hidden demethylation pathway removes mercury from rice plants and mitigates mercury flux to food chains

AU - Tang, Wenli

AU - Bai, Xu

AU - Zhou, Yang

AU - Sonne, Christian

AU - Wu, Mengjie

AU - Lam, Su Shiung

AU - Hintelmann, Holger

AU - Mitchell, Carl P.J.

AU - Johs, Alexander

AU - Gu, Baohua

AU - Nunes, Luís

AU - Liu, Cun

AU - Feng, Naixian

AU - Yang, Sihai

AU - Rinklebe, Jörg

AU - Lin, Yan

AU - Chen, Long

AU - Zhang, Yanxu

AU - Yang, Yanan

AU - Wang, Jiaqi

AU - Li, Shouying

AU - Wu, Qingru

AU - Ok, Yong Sik

AU - Xu, Diandou

AU - Li, Hong

AU - Zhang, Xu Xiang

AU - Ren, Hongqiang

AU - Jiang, Guibin

AU - Chai, Zhifang

AU - Gao, Yuxi

AU - Zhao, Jiating

AU - Zhong, Huan

PY - 2024/1

Y1 - 2024/1

N2 - 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.

AB - 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.

UR - https://www.scopus.com/pages/publications/85181438033

U2 - 10.1038/s43016-023-00910-x

DO - 10.1038/s43016-023-00910-x

M3 - Article

C2 - 38177223

AN - SCOPUS:85181438033

SN - 2662-1355

VL - 5

SP - 72

EP - 82

JO - Nature Food

JF - Nature Food

IS - 1

ER -

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

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