Spectroscopic and Microscopic Evidence of Biomediated HgS Species Formation from Hg(II)-Cysteine Complexes: Implications for Hg(II) Bioavailability

Sara A. Thomas; Kara E. Rodby; Eric W. Roth; Jinsong Wu; Jean François Gaillard

doi:10.1021/acs.est.8b01305

Spectroscopic and Microscopic Evidence of Biomediated HgS Species Formation from Hg(II)-Cysteine Complexes: Implications for Hg(II) Bioavailability

Sara A. Thomas^*, Kara E. Rodby, Eric W. Roth, Jinsong Wu, Jean François Gaillard

^*Corresponding author for this work

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

50 Scopus citations

Abstract

We investigated the chemistry of Hg(II) during exposure of exponentially growing bacteria (Escherichia coli, Bacillus subtilis, and Geobacter sulfurreducens) to 50 nM, 500 nM, and 5 μM total Hg(II) with and without added cysteine. With X-ray absorption spectroscopy, we provide direct evidence of the formation of cell-associated HgS for all tested bacteria. The addition of cysteine (100-1000 μM) promotes HgS formation (>70% of total cell-associated Hg(II)) as a result of the biodegradation of added cysteine to sulfide. Cell-associated HgS species are also detected when cysteine is not added as a sulfide source. Two phases of HgS, cinnabar (α-HgS) and metacinnabar (β-HgS), form depending on the total concentration of Hg(II) and sulfide in the exposure medium. However, α-HgS exclusively forms in assays that contain an excess of cysteine. Scanning transmission electron microscopy images reveal that nanoparticulate HgS_(s) is primarily located at the cell surface/extracellular matrix of Gram-negative E. coli and G. sulfurreducens and in the cytoplasm/cell membrane of Gram-positive B. subtilis. Intracellular Hg(II) was detected even when the predominant cell-associated species was HgS. This study shows that HgS species can form from exogenous thiol-containing ligands and endogenous sulfide in Hg(II) biouptake assays under nondissimilatory sulfate reducing conditions, providing new considerations for the interpretation of Hg(II) biouptake results.

Original language	English (US)
Pages (from-to)	10030-10039
Number of pages	10
Journal	Environmental Science and Technology
Volume	52
Issue number	17
DOIs	https://doi.org/10.1021/acs.est.8b01305
State	Published - Sep 4 2018

Funding

We are grateful to Qing Ma for his beamline assistance at the APS. We thank Dr. Isabelle Michaud-Soret for helpful discussions regarding this study. This work is supported by the National Science Foundation under grant CHE-1308504 and a grant to K.E.R. from the Undergraduate Research Grant Program administered by Northwestern University’s Office of the Provost. Portions of this work were performed at the DND-CAT Synchrotron Research Center located at Sector 5 of the APS. DND-CAT is supported by the E.I. DuPont de Nemours & Co., The Dow Chemical Company, the U.S. National Science Foundation through Grant DMR-9304725, and the State of Illinois through the Department of Commerce and the Board of Higher Education Grant IBHE HECA NWU 96. The STEM and TEM work made use of the BioCryo and EPIC facility of Northwestern University’s NUANCE Center, which has received support from the Soft and Hybrid Nanotechnology Experimental (SHyNE) Resource (NSF ECCS-1542205); the MRSEC program (NSF DMR-1121262) at the Materials Research Center; the International Institute for Nanotechnology (IIN); the Keck Foundation; and the State of Illinois, through the IIN. Finally, we thank four anonymous reviewers for their helpful suggestions.

ASJC Scopus subject areas

General Chemistry
Environmental Chemistry

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10.1021/acs.est.8b01305

Cite this

@article{fb589a7787ce4f3087277c4fa4de42c2,

title = "Spectroscopic and Microscopic Evidence of Biomediated HgS Species Formation from Hg(II)-Cysteine Complexes: Implications for Hg(II) Bioavailability",

abstract = "We investigated the chemistry of Hg(II) during exposure of exponentially growing bacteria (Escherichia coli, Bacillus subtilis, and Geobacter sulfurreducens) to 50 nM, 500 nM, and 5 μM total Hg(II) with and without added cysteine. With X-ray absorption spectroscopy, we provide direct evidence of the formation of cell-associated HgS for all tested bacteria. The addition of cysteine (100-1000 μM) promotes HgS formation (>70% of total cell-associated Hg(II)) as a result of the biodegradation of added cysteine to sulfide. Cell-associated HgS species are also detected when cysteine is not added as a sulfide source. Two phases of HgS, cinnabar (α-HgS) and metacinnabar (β-HgS), form depending on the total concentration of Hg(II) and sulfide in the exposure medium. However, α-HgS exclusively forms in assays that contain an excess of cysteine. Scanning transmission electron microscopy images reveal that nanoparticulate HgS(s) is primarily located at the cell surface/extracellular matrix of Gram-negative E. coli and G. sulfurreducens and in the cytoplasm/cell membrane of Gram-positive B. subtilis. Intracellular Hg(II) was detected even when the predominant cell-associated species was HgS. This study shows that HgS species can form from exogenous thiol-containing ligands and endogenous sulfide in Hg(II) biouptake assays under nondissimilatory sulfate reducing conditions, providing new considerations for the interpretation of Hg(II) biouptake results.",

author = "Thomas, {Sara A.} and Rodby, {Kara E.} and Roth, {Eric W.} and Jinsong Wu and Gaillard, {Jean Fran{\c c}ois}",

note = "Funding Information: We are grateful to Qing Ma for his beamline assistance at the APS. We thank Dr. Isabelle Michaud-Soret for helpful discussions regarding this study. This work is supported by the National Science Foundation under grant CHE-1308504 and a grant to K.E.R. from the Undergraduate Research Grant Program administered by Northwestern University{\textquoteright}s Office of the Provost. Portions of this work were performed at the DND-CAT Synchrotron Research Center located at Sector 5 of the APS. DND-CAT is supported by the E.I. DuPont de Nemours & Co., The Dow Chemical Company, the U.S. National Science Foundation through Grant DMR-9304725, and the State of Illinois through the Department of Commerce and the Board of Higher Education Grant IBHE HECA NWU 96. The STEM and TEM work made use of the BioCryo and EPIC facility of Northwestern University{\textquoteright}s NUANCE Center, which has received support from the Soft and Hybrid Nanotechnology Experimental (SHyNE) Resource (NSF ECCS-1542205); the MRSEC program (NSF DMR-1121262) at the Materials Research Center; the International Institute for Nanotechnology (IIN); the Keck Foundation; and the State of Illinois, through the IIN. Finally, we thank four anonymous reviewers for their helpful suggestions. Publisher Copyright: {\textcopyright} 2018 American Chemical Society.",

year = "2018",

month = sep,

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doi = "10.1021/acs.est.8b01305",

language = "English (US)",

volume = "52",

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T1 - Spectroscopic and Microscopic Evidence of Biomediated HgS Species Formation from Hg(II)-Cysteine Complexes

T2 - Implications for Hg(II) Bioavailability

AU - Thomas, Sara A.

AU - Rodby, Kara E.

AU - Roth, Eric W.

AU - Wu, Jinsong

AU - Gaillard, Jean François

N1 - Funding Information: We are grateful to Qing Ma for his beamline assistance at the APS. We thank Dr. Isabelle Michaud-Soret for helpful discussions regarding this study. This work is supported by the National Science Foundation under grant CHE-1308504 and a grant to K.E.R. from the Undergraduate Research Grant Program administered by Northwestern University’s Office of the Provost. Portions of this work were performed at the DND-CAT Synchrotron Research Center located at Sector 5 of the APS. DND-CAT is supported by the E.I. DuPont de Nemours & Co., The Dow Chemical Company, the U.S. National Science Foundation through Grant DMR-9304725, and the State of Illinois through the Department of Commerce and the Board of Higher Education Grant IBHE HECA NWU 96. The STEM and TEM work made use of the BioCryo and EPIC facility of Northwestern University’s NUANCE Center, which has received support from the Soft and Hybrid Nanotechnology Experimental (SHyNE) Resource (NSF ECCS-1542205); the MRSEC program (NSF DMR-1121262) at the Materials Research Center; the International Institute for Nanotechnology (IIN); the Keck Foundation; and the State of Illinois, through the IIN. Finally, we thank four anonymous reviewers for their helpful suggestions. Publisher Copyright: © 2018 American Chemical Society.

PY - 2018/9/4

Y1 - 2018/9/4

N2 - We investigated the chemistry of Hg(II) during exposure of exponentially growing bacteria (Escherichia coli, Bacillus subtilis, and Geobacter sulfurreducens) to 50 nM, 500 nM, and 5 μM total Hg(II) with and without added cysteine. With X-ray absorption spectroscopy, we provide direct evidence of the formation of cell-associated HgS for all tested bacteria. The addition of cysteine (100-1000 μM) promotes HgS formation (>70% of total cell-associated Hg(II)) as a result of the biodegradation of added cysteine to sulfide. Cell-associated HgS species are also detected when cysteine is not added as a sulfide source. Two phases of HgS, cinnabar (α-HgS) and metacinnabar (β-HgS), form depending on the total concentration of Hg(II) and sulfide in the exposure medium. However, α-HgS exclusively forms in assays that contain an excess of cysteine. Scanning transmission electron microscopy images reveal that nanoparticulate HgS(s) is primarily located at the cell surface/extracellular matrix of Gram-negative E. coli and G. sulfurreducens and in the cytoplasm/cell membrane of Gram-positive B. subtilis. Intracellular Hg(II) was detected even when the predominant cell-associated species was HgS. This study shows that HgS species can form from exogenous thiol-containing ligands and endogenous sulfide in Hg(II) biouptake assays under nondissimilatory sulfate reducing conditions, providing new considerations for the interpretation of Hg(II) biouptake results.

AB - We investigated the chemistry of Hg(II) during exposure of exponentially growing bacteria (Escherichia coli, Bacillus subtilis, and Geobacter sulfurreducens) to 50 nM, 500 nM, and 5 μM total Hg(II) with and without added cysteine. With X-ray absorption spectroscopy, we provide direct evidence of the formation of cell-associated HgS for all tested bacteria. The addition of cysteine (100-1000 μM) promotes HgS formation (>70% of total cell-associated Hg(II)) as a result of the biodegradation of added cysteine to sulfide. Cell-associated HgS species are also detected when cysteine is not added as a sulfide source. Two phases of HgS, cinnabar (α-HgS) and metacinnabar (β-HgS), form depending on the total concentration of Hg(II) and sulfide in the exposure medium. However, α-HgS exclusively forms in assays that contain an excess of cysteine. Scanning transmission electron microscopy images reveal that nanoparticulate HgS(s) is primarily located at the cell surface/extracellular matrix of Gram-negative E. coli and G. sulfurreducens and in the cytoplasm/cell membrane of Gram-positive B. subtilis. Intracellular Hg(II) was detected even when the predominant cell-associated species was HgS. This study shows that HgS species can form from exogenous thiol-containing ligands and endogenous sulfide in Hg(II) biouptake assays under nondissimilatory sulfate reducing conditions, providing new considerations for the interpretation of Hg(II) biouptake results.

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Spectroscopic and Microscopic Evidence of Biomediated HgS Species Formation from Hg(II)-Cysteine Complexes: Implications for Hg(II) Bioavailability

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