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Microbial methylation potential of mercury sulfide particles dictated by surface structure

Nature Geoscience volume 14, pages 409–416 (2021)Cite this article

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Abstract

Environmental contamination by mercury in its organometallic form, methylmercury, remains a major global concern due to its neurotoxicity, environmental persistence and biomagnification through the food chain. Accurate prediction of mercury methylation cannot be achieved based on aqueous speciation alone, and there remains limited mechanistic understanding of microbial methylation of particulate-phase mercury. Here we assess the time-dependent changes in structural properties and methylation potential of nanoparticulate mercury using microscopic and spectroscopic analyses, microcosm bioassays and theoretical calculations. We show that the methylation potential of a mercury sulfide mineral ubiquitous in contaminated soils and sediments (nanoparticulate metacinnabar) is determined by its crystal structure. Methylmercury production increases when more of nano-metacinnabar’s exposed surfaces occur as the (111) facet, due to its large binding affinity to methylating bacteria, likely via the protein transporter responsible for mercury cellular uptake prior to methylation. During nanocrystal growth, the (111) facet diminishes, lessening methylation of nano-metacinnabar. However, natural ligands alleviate this process by preferentially adsorbing to the (111) facet, and consequently hinder natural attenuation of mercury methylation. We show that the methylation potential of nanoparticulate mercury is independent of surface area. Instead, the nano-scale surface structure of nanoparticulate mercury is crucial for understanding the environmental behaviour of mercury and other nutrient or toxic soft elements.

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Fig. 1: Methylation potential and exposed facets of nano-HgS significantly change during ageing while particle size and surface area remain similar.
Fig. 2: Association between methylating bacterial cells and nano-HgS significantly decreases during ageing.
Fig. 3: (111) facet of nano-metacinnabar exhibits higher affinity for the divalent metal transporter of D. desulfuricans ND132 than the other facets.
Fig. 4: (111) facet of nano-metacinnabar preferentially adsorbs natural ligands.
Fig. 5: Conceptual illustration of ageing-induced decrease in bioavailability and methylation potential of nano-metacinnabar due to facet evolution.

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Data availability

The protein sequence and three-dimensional structure of periplasmic solute-binding protein of zinc transport system of D. desulfuricans ND132, ZnuA, are available in the UniProt database (https://www.uniprot.org/uniprot/F0JJA9). All source data are deposited in the Open Science Framework (OSF) at https://doi.org/10.17605/OSF.IO/YXRMF. Source Data files and a Supplementary Data file are provided with this paper.

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Acknowledgements

This research was supported by the National Key Research and Development Program of China under grant 2018YFC1800705 (to T.Z.), the National Natural Science Foundation of China under grants 22020102004 (to W.C.), 21976095 (to T.Z.) and 41603099 (to T.Z.), and the Ministry of Education of China under grant T2017002 (to W.C.). Partial support for P.A. was provided by the NSF Nanosystems Engineering Research Center for Nanotechnology-Enabled Water Treatment (ERC-1449500). The authors thank C. C. Gilmour from the Smithsonian Environmental Research Center for supplying the strain of D. desulfuricans ND132, Q. Yao for help with XRD analysis and H. Hsu-Kim and H. H. Teng for helpful discussions regarding manuscript preparation.

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  1. College of Environmental Science and Engineering, Ministry of Education Key Laboratory of Pollution Processes and Environmental Criteria, Tianjin Key Laboratory of Environmental Remediation and Pollution Control, Nankai University, Tianjin, China

    Li Tian, Wenyu Guan, Yunyun Ji, Xin He, Wei Chen & Tong Zhang

  2. Department of Civil and Environmental Engineering, Rice University, Houston, TX, USA

    Pedro J. J. Alvarez

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Contributions

L.T., W.G., Y.J. and X.H. carried out the experiments and data analysis. T.Z. conceived the study and supervised the research. W.C. and P.J.J.A. contributed intellectual input to the experimental design and data analysis. L.T. and T.Z. drafted the manuscript with input from all authors.

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Tian, L., Guan, W., Ji, Y. et al. Microbial methylation potential of mercury sulfide particles dictated by surface structure. Nat. Geosci. 14, 409–416 (2021). https://doi.org/10.1038/s41561-021-00735-y

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