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Title: Mercury Uptake by Desulfovibrio desulfuricans ND132: Passive or Active?

Abstract

Recent studies have identified HgcAB proteins as being responsible for mercury [Hg(II)] methylation by certain anaerobic microorganisms. However, it remains controversial whether microbes take up Hg(II) passively or actively. Here, we examine the dynamics of concurrent Hg(II) adsorption, uptake, and methylation by both viable and inactivated cells (heat-killed or starved) or spheroplasts of the sulfate-reducing bacterium Desulfovibrio desulfuricans ND132 in laboratory incubations. We show that, without addition of thiols, >60% of the added Hg(II) (25 nM) was taken up passively in 48 h by live and inactivated cells and also by cells treated with the proton gradient uncoupler, carbonylcyanide-3-chlorophenylhydrazone (CCCP). Inactivation abolished Hg(II) methylation, but the cells continued taking up Hg(II), likely through competitive binding or ligand exchange of Hg(II) by intracellular proteins or thiol-containing cellular components. Similarly, treatment with CCCP impaired the ability of spheroplasts to methylate Hg(II) but did not stop Hg(II) uptake. Spheroplasts showed a greater capacity to adsorb Hg(II) than whole cells, and the level of cytoplasmic membrane-bound Hg(II) correlated well with MeHg production, as Hg(II) methylation is associated with cytoplasmic HgcAB. Our results indicate that active metabolism is not required for cellular Hg(II) uptake, thereby providing an improved understanding of Hg(II) bioavailability for methylation.

Authors:
ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [2]; ORCiD logo [2]; ORCiD logo [2]; ORCiD logo [2]; ORCiD logo [2]; ORCiD logo [3]
  1. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Chinese Academy of Sciences (CAS), Beijing (China)
  2. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
  3. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Univ. of Tennessee, Knoxville, TN (United States)
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1530103
Grant/Contract Number:  
AC05-00OR22725
Resource Type:
Accepted Manuscript
Journal Name:
Environmental Science and Technology
Additional Journal Information:
Journal Volume: 53; Journal Issue: 11; Journal ID: ISSN 0013-936X
Publisher:
American Chemical Society (ACS)
Country of Publication:
United States
Language:
English
Subject:
54 ENVIRONMENTAL SCIENCES

Citation Formats

An, Jing, Zhang, Lijie, Lu, Xia, Pelletier, Dale A., Pierce, Eric M., Johs, Alexander, Parks, Jerry M., and Gu, Baohua. Mercury Uptake by Desulfovibrio desulfuricans ND132: Passive or Active?. United States: N. p., 2019. Web. doi:10.1021/acs.est.9b00047.
An, Jing, Zhang, Lijie, Lu, Xia, Pelletier, Dale A., Pierce, Eric M., Johs, Alexander, Parks, Jerry M., & Gu, Baohua. Mercury Uptake by Desulfovibrio desulfuricans ND132: Passive or Active?. United States. doi:10.1021/acs.est.9b00047.
An, Jing, Zhang, Lijie, Lu, Xia, Pelletier, Dale A., Pierce, Eric M., Johs, Alexander, Parks, Jerry M., and Gu, Baohua. Fri . "Mercury Uptake by Desulfovibrio desulfuricans ND132: Passive or Active?". United States. doi:10.1021/acs.est.9b00047.
@article{osti_1530103,
title = {Mercury Uptake by Desulfovibrio desulfuricans ND132: Passive or Active?},
author = {An, Jing and Zhang, Lijie and Lu, Xia and Pelletier, Dale A. and Pierce, Eric M. and Johs, Alexander and Parks, Jerry M. and Gu, Baohua},
abstractNote = {Recent studies have identified HgcAB proteins as being responsible for mercury [Hg(II)] methylation by certain anaerobic microorganisms. However, it remains controversial whether microbes take up Hg(II) passively or actively. Here, we examine the dynamics of concurrent Hg(II) adsorption, uptake, and methylation by both viable and inactivated cells (heat-killed or starved) or spheroplasts of the sulfate-reducing bacterium Desulfovibrio desulfuricans ND132 in laboratory incubations. We show that, without addition of thiols, >60% of the added Hg(II) (25 nM) was taken up passively in 48 h by live and inactivated cells and also by cells treated with the proton gradient uncoupler, carbonylcyanide-3-chlorophenylhydrazone (CCCP). Inactivation abolished Hg(II) methylation, but the cells continued taking up Hg(II), likely through competitive binding or ligand exchange of Hg(II) by intracellular proteins or thiol-containing cellular components. Similarly, treatment with CCCP impaired the ability of spheroplasts to methylate Hg(II) but did not stop Hg(II) uptake. Spheroplasts showed a greater capacity to adsorb Hg(II) than whole cells, and the level of cytoplasmic membrane-bound Hg(II) correlated well with MeHg production, as Hg(II) methylation is associated with cytoplasmic HgcAB. Our results indicate that active metabolism is not required for cellular Hg(II) uptake, thereby providing an improved understanding of Hg(II) bioavailability for methylation.},
doi = {10.1021/acs.est.9b00047},
journal = {Environmental Science and Technology},
number = 11,
volume = 53,
place = {United States},
year = {2019},
month = {5}
}

Journal Article:
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This content will become publicly available on May 10, 2020
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