Biogenesis of Mercury–Sulfur Nanoparticles in Plant Leaves from Atmospheric Gaseous Mercury

Abstract

Plant leaves serve both as a sink for gaseous elemental mercury (Hg) from the atmosphere and a source of toxic mercury to terrestrial ecosystems. Litterfall is the primary deposition pathway of atmospheric Hg to vegetated soils, yet the chemical form of this major Hg input remains elusive. We report the first observation of in vivo formation of mercury sulfur nanoparticles in intact leaves of 22 native plants from six different species across two sampling areas from China. The plants grew naturally in soils from a mercury sulfide mining and retorting region at ambient-air gaseous-Hg concentrations ranging from 131 ± 19 to 636 ± 186 ng m and had foliar Hg concentration between 1.9 and 31.1 ng Hg mg dry weight (ppm). High energy resolution X-ray absorption near-edge structure (HR-XANES) spectroscopy shows that up to 57% of the acquired Hg is nanoparticulate, and the remainder speciated as a bis-thiolate complex (Hg(SR)). The fractional amount of nanoparticulate Hg is not correlated with Hg concentration. Variation likely depends on leaf age, plant physiology, and natural variability. Nanoparticulate Hg atoms are bonded to four sulfide or thiolate sulfur atoms arranged in a metacinnabar-type (β-HgS) coordination environment. The nanometer dimension of the mercury-sulfur clusters outmatches the known binding capacity of plant metalloproteins. These findings give rise to challenging questions on their exact nature, how they form, and their biogeochemical reactivity and fate in litterfall, whether this mercury pool is recycled or stored in soils. This study provides new evidence that metacinnabar-type nanoparticles are widespread in oxygenated environments.

Mercury(II) Binding to Metallothionein in Mytilus edulis revealed by High Energy‐Resolution XANES Spectroscopy

“…The geometry of the Hg 4 S 12 ‐α and Hg 3 S 9 ‐β mussel clusters and the Hg 4 S 11 ‐α vertebrate cluster were optimized at the MP2 level using the connectivity of the Cd 4 S 12 ‐α and Cd 3 S 9 ‐β clusters in M. galloprovincialis as structural templates (Figure ). The model thiolate was methanethiolate CH 3 S − , as in our previous computational studies . This substitution marginally changes the geometry of a complex or the effective atomic charge on the sulfur and mercury atoms (Figure S7, Supporting Information).…”

“…The best shape among the tetrahedral compounds from our extended spectral database (ref. and references therein) that best matched peak B was obtained with nanoparticulate metacinnabar (β‐HgS NP ; Figure d). In β‐HgS, Hg II is coordinated to four sulfide atoms at 2.53 Å and surrounded by higher shells of Hg atoms .…”

“…This material has broad β‐HgS X‐ray diffraction peaks and damped HR‐XANES structures (Figures S2 a and S3 b, Supporting Information) characteristic of highly defective material with a wide range of both angles and bond lengths, as commonly observed for metal thiolate clusters in proteins . β‐HgS NP has been identified previously in natural organic matter and soils, in plants, and in pyrite (FeS 2 ) . The β‐HgS NP crystallites imaged by HRTEM are about 5 nm in diameter (Figure S3 b, Supporting Information) …”

“…What is the amino acid sequence of the MT‐10 units (primary structure) and how are they covalently bonded in MT‐40 (quaternary structure)? Do the monomeric units from MT‐40 contain 21 cysteines, as in canonical MT‐10, or 23 cysteines, as in the monomeric MT‐10 units of MT‐20? Lastly, are the biogenic MT clusters more stable than the metallothionein‐like β‐HgS nanoparticles formed naturally in natural organic matter and plant leaves? All these questions could be asked similarly to 4d 10 Ag I and 5d 10 Au I , which, like 5d 10 Hg II , form distorted thiolate clusters in metalloproteins and linear coordination with thiolate ligands when they are embedded in sterically complex and demanding macromolecules. All these important biometals and intriguing questions are now leading to investigations in living matter by HR‐XANES down to, and below, the ppm level …”

“…Here, we show that direct insight into Hg II binding to MTs in living cells is provided by the new application of high energy‐resolution X‐ray absorption near‐edge structure (HR‐XANES) spectroscopy at extreme dilution . Compared to EXAFS, XANES spectroscopy provides geometric information, is less sensitive to structural disorder around the photoabsorbing atom, and has superior elemental sensitivity . Therefore, high spectral resolution allows more precise identification of the plurality of the bonding environments in the α and β domains, either within the same MT molecule, if all molecules are structurally equivalent, or among the MT molecules, if various coordination environments coexist in a mixture.…”