Thiolated arsenic species observed in rice paddy pore waters

Abstract

The accumulation of carcinogenic arsenic in rice, the world’s main staple crop, represents a health threat to millions of people. The speciation of arsenic controls its mobility and bioavailability and therefore its entry into the food chain. Inorganic and methylated oxyarsenic species have been a focus of research, but arsenic characterization in the field has largely ignored thioarsenates, in which sulfur takes the place of oxygen. Here, on the basis of field, mesocosm and soil incubation studies across multiple paddy soils from rice cultivation areas in Italy, France and China, we find that thioarsenates are important arsenic species in paddy-soil pore waters. We observed thioarsenates throughout the cropping season, with concentrations comparable to the much-better-investigated methylated oxyarsenates. Anaerobic soil incubations confirmed a large potential for thiolation across a wide diversity of paddy soil types in different climate zones and with different parent materials. In these incubations, inorganic thioarsenates occurred predominantly where soil pH exceeded 6.5 and in the presence of zero-valent sulfur. Methylated thioarsenates occurred predominantly at soil pH below 7 and in the presence of their precursors, methylated oxyarsenates. High concentrations of dissolved iron limited arsenic thiolation. Sulfate fertilization increased thioarsenate formation. It is currently unclear whether thiolation is good or bad for rice consumption safety. Nevertheless, we highlight thiolation as an important factor to arsenic biogeochemistry in rice paddies.

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Fig. 1: Conceptual model for the formation of thioarsenates in paddy soils coupled to a cryptic S cycle.
Fig. 2: Pore-water As thiolation, methylation and total As concentrations over time during rice cultivation.
Fig. 3: Proportions of inorganic, methylated and total thioarsenates, as well as methylated oxyarsenates, integrated over time.
Fig. 4: Parameters that determine occurrence of inorganic and methylated thioarsenates in anaerobic soil incubations.

Data availability

The datasets generated during and/or analysed during the current study are also available from the corresponding author on reasonable request.

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Acknowledgements

We acknowledge financial support for a PhD stipend to J. Wang from the China Scholarship Council (CSC), mobility grants within the Bavarian Funding Programme for travels to France (BFHZ FK-40-15), Italy (BayIntAn2016), China (BayCHINA2018), as well as from the National Key Research and Development Project of China (2016YFE0106400) and the National Natural Science Foundation of China (41325003) for paddy soils survey, sampling and determination in China. We acknowledge data support from the Soil Data Center, National Earth System Science Data Sharing Service Infrastructure, National Science & Technology Infrastructure of China (http://soil.geodata.cn) and Ente Regionale per i Servizi all’Agricoltura e alle Foreste—Regione Lombardia of Italy (https://www.ersaf.lombardia.it/). We are indebted to the staff at the Rice Research Centre in Castello d’Agogna (Pavia, Italy) for help with soil sampling and mesocosm rice cultivation, including S. Feccia, F. Mazza, U. Rolla, E. Miniotti, G. Beltarre, A. Iuzzolino, F. Bonassi, L. Pizzin, D. Tenni, A. Zanellato, F. Massara, E. Magnani, G. Bertone and M. Zini. We thank C. Thomas and A. Boisnard from the Centre Français du Riz (Arles, Italy) for assistance with soil sampling in France. We are grateful to M. T. F. Wagner, C. Lerda, S. Will, J. M. Leon, J. Besold, L. Wegner and S. Zhang for help with field sampling and laboratory assistance, to Y. Yang for help with map design, and to J. Mehlhorn for help with statistical analyses.

Author information

J.W. initiated DTPA method development, conceived and performed all mesocosm and incubation experiments including analyses, evaluated the results and contributed to manuscript preparation; C.F.K. contributed to field survey, sample analyses, data evaluation and manuscript preparation; L.B. contributed to DTPA method development; P.H. and L.W. initiated the Chinese soil survey and advised on incubation experiments; P.H., T.M., G.W. and L.W. sampled and characterized the Chinese soils; M.R. assisted in design, setup and operation of mesocosms and sample collection; M.M. and D.S.-P. assisted in analyses of aqueous parameters from mesocosms; M.M. contributed to field survey and data discussion; B.P.-F. initiated and supervised the project, carried out the field survey, conceived experiments and wrote the manuscript; all authors contributed to revising the manuscript.

Correspondence to Britta Planer-Friedrich.

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Peer review information Primary Handling Editors: Xujia Jiang; Rebecca Neely.

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Supplementary information

Supplementary Information

Supplementary methods, Figs. 1–20 and Tables 1–9

Supplementary Table 1

Pore water chemistry including As speciation

Supplementary Table 2

Soil classification and basic chemical parameters

Supplementary Table 3

Pore water chemistry in the mesocosm experiments

Supplementary Table 4

Mean values for thiolation and methylation

Supplementary Table 5

Location, parent material, and soil classification

Supplementary Table 6

Spearman’s correlation analyses for soil and pore water parameters

Supplementary Table 7

Relative importance of predictor values

Supplementary Table 8

Quantitative Recovery of As species in a fresh model pore water

Supplementary Table 9

Characteristics of irrigation water for mesocosm experiments

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Wang, J., Kerl, C.F., Hu, P. et al. Thiolated arsenic species observed in rice paddy pore waters. Nat. Geosci. (2020). https://doi.org/10.1038/s41561-020-0533-1

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