DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

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:
 [1];  [2]; ORCiD logo [2];  [3]; ORCiD logo [2]; ORCiD logo [2]; ORCiD logo [3]; ORCiD logo [4]
  1. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Environmental Sciences Division; Chinese Academy of Sciences, Shenyang (China). Key Lab. of Pollution Ecology and Environmental Engineering, Inst. of Applied Ecology
  2. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Environmental Sciences Division
  3. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Division
  4. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Environmental Sciences Division; Univ. of Tennessee, Knoxville, TN (United States). Dept. of Biosystems Engineering and Soil Science
Publication Date:
Research Org.:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
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. https://doi.org/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. https://doi.org/10.1021/acs.est.9b00047. https://www.osti.gov/servlets/purl/1530103.
@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 = {Fri May 10 00:00:00 EDT 2019},
month = {Fri May 10 00:00:00 EDT 2019}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 26 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

The Genetic Basis for Bacterial Mercury Methylation
journal, February 2013


Global prevalence and distribution of genes and microorganisms involved in mercury methylation
journal, October 2015

  • Podar, Mircea; Gilmour, Cynthia C.; Brandt, Craig C.
  • Science Advances, Vol. 1, Issue 9
  • DOI: 10.1126/sciadv.1500675

Site-Directed Mutagenesis of HgcA and HgcB Reveals Amino Acid Residues Important for Mercury Methylation
journal, February 2015

  • Smith, Steven D.; Bridou, Romain; Johs, Alexander
  • Applied and Environmental Microbiology, Vol. 81, Issue 9
  • DOI: 10.1128/AEM.00217-15

Development and Validation of Broad-Range Qualitative and Clade-Specific Quantitative Molecular Probes for Assessing Mercury Methylation in the Environment
journal, July 2016

  • Christensen, Geoff A.; Wymore, Ann M.; King, Andrew J.
  • Applied and Environmental Microbiology, Vol. 82, Issue 19
  • DOI: 10.1128/AEM.01271-16

Mercury Bioavailability and Bioaccumulation in Estuarine Food Webs in the Gulf of Maine
journal, February 2009

  • Chen, Celia Y.; Dionne, Michele; Mayes, Brandon M.
  • Environmental Science & Technology, Vol. 43, Issue 6
  • DOI: 10.1021/es8017122

Mercury as a Global Pollutant: Sources, Pathways, and Effects
journal, May 2013

  • Driscoll, Charles T.; Mason, Robert P.; Chan, Hing Man
  • Environmental Science & Technology, Vol. 47, Issue 10
  • DOI: 10.1021/es305071v

Human Exposure To Methylmercury through Rice Intake in Mercury Mining Areas, Guizhou Province, China
journal, January 2008

  • Feng, Xinbin; Li, Ping; Qiu, Guangle
  • Environmental Science & Technology, Vol. 42, Issue 1
  • DOI: 10.1021/es071948x

Rice methylmercury exposure and mitigation: A comprehensive review
journal, August 2014


Unraveling Microbial Communities Associated with Methylmercury Production in Paddy Soils
journal, October 2018

  • Liu, Yu-Rong; Johs, Alexander; Bi, Li
  • Environmental Science & Technology, Vol. 52, Issue 22
  • DOI: 10.1021/acs.est.8b03052

Aspects of Bioavailability of Mercury for Methylation in Pure Cultures of Desulfobulbus propionicus (1pr3)
journal, January 2001

  • Benoit, J. M.; Gilmour, C. C.; Mason, R. P.
  • Applied and Environmental Microbiology, Vol. 67, Issue 1
  • DOI: 10.1128/AEM.67.1.51-58.2001

Sulfide Controls on Mercury Speciation and Bioavailability to Methylating Bacteria in Sediment Pore Waters
journal, March 1999

  • Benoit, Janina M.; Gilmour, Cynthia C.; Mason, Robert P.
  • Environmental Science & Technology, Vol. 33, Issue 6
  • DOI: 10.1021/es9808200

Estimation of mercury-sulfide speciation in sediment pore waters using octanol-water partitioning and implications for availability to methylating bacteria: Mercury-sulfide speciation
journal, October 1999

  • Benoit, Janina M.; Mason, Robert P.; Gilmour, Cynthia C.
  • Environmental Toxicology and Chemistry, Vol. 18, Issue 10
  • DOI: 10.1002/etc.5620181004

An examination of the factors influencing the flux of mercury, methylmercury and other constituents from estuarine sediment
journal, November 2006


Inorganic mercury (Hg2+) transport through lipid bilayer membranes
journal, February 1981

  • Gutknecht, John
  • The Journal of Membrane Biology, Vol. 61, Issue 1
  • DOI: 10.1007/BF01870753

Mechanisms Regulating Mercury Bioavailability for Methylating Microorganisms in the Aquatic Environment: A Critical Review
journal, February 2013

  • Hsu-Kim, Heileen; Kucharzyk, Katarzyna H.; Zhang, Tong
  • Environmental Science & Technology, Vol. 47, Issue 6
  • DOI: 10.1021/es304370g

Modeling of the Passive Permeation of Mercury and Methylmercury Complexes Through a Bacterial Cytoplasmic Membrane
journal, August 2017

  • Zhou, Jing; Smith, Micholas Dean; Cooper, Sarah J.
  • Environmental Science & Technology, Vol. 51, Issue 18
  • DOI: 10.1021/acs.est.7b02204

Evidence for facilitated uptake of Hg(II) by Vibrio anguillarum and Escherichia coli under anaerobic and aerobic conditions
journal, July 2002

  • Golding, George R.; Kelly, Carol A.; Sparling, Richard
  • Limnology and Oceanography, Vol. 47, Issue 4
  • DOI: 10.4319/lo.2002.47.4.0967

High methylation rates of mercury bound to cysteine by Geobacter sulfurreducens
journal, January 2009

  • Schaefer, Jeffra K.; Morel, François M. M.
  • Nature Geoscience, Vol. 2, Issue 2
  • DOI: 10.1038/ngeo412

Active transport, substrate specificity, and methylation of Hg(II) in anaerobic bacteria
journal, May 2011

  • Schaefer, J. K.; Rocks, S. S.; Zheng, W.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 21
  • DOI: 10.1073/pnas.1105781108

Effect of Divalent Metals on Hg(II) Uptake and Methylation by Bacteria
journal, February 2014

  • Schaefer, Jeffra K.; Szczuka, Aleksandra; Morel, François M. M.
  • Environmental Science & Technology, Vol. 48, Issue 5
  • DOI: 10.1021/es405215v

Effects of Cellular Sorption on Mercury Bioavailability and Methylmercury Production by Desulfovibrio desulfuricans ND132
journal, November 2016

  • Liu, Yu-Rong; Lu, Xia; Zhao, Linduo
  • Environmental Science & Technology, Vol. 50, Issue 24
  • DOI: 10.1021/acs.est.6b04041

Spectroscopic and Microscopic Evidence of Biomediated HgS Species Formation from Hg(II)–Cysteine Complexes: Implications for Hg(II) Bioavailability
journal, August 2018

  • Thomas, Sara A.; Rodby, Kara E.; Roth, Eric W.
  • Environmental Science & Technology, Vol. 52, Issue 17
  • DOI: 10.1021/acs.est.8b01305

Cysteine Inhibits Mercury Methylation by Geobacter sulfurreducens PCA Mutant Δ omcBESTZ
journal, April 2015


Coupled Mercury–Cell Sorption, Reduction, and Oxidation on Methylmercury Production by Geobacter sulfurreducens PCA
journal, October 2014

  • Lin, Hui; Morrell-Falvey, Jennifer L.; Rao, Balaji
  • Environmental Science & Technology, Vol. 48, Issue 20
  • DOI: 10.1021/es502537a

Contrasting Effects of Dissolved Organic Matter on Mercury Methylation by Geobacter sulfurreducens PCA and Desulfovibrio desulfuricans ND132
journal, August 2017

  • Zhao, Linduo; Chen, Hongmei; Lu, Xia
  • Environmental Science & Technology, Vol. 51, Issue 18
  • DOI: 10.1021/acs.est.7b02518

Intracellular Hg(0) Oxidation in Desulfovibrio desulfuricans ND132
journal, October 2016

  • Wang, Yuwei; Schaefer, Jeffra K.; Mishra, Bhoopesh
  • Environmental Science & Technology, Vol. 50, Issue 20
  • DOI: 10.1021/acs.est.6b03299

Sulfate-Reducing Bacterium Desulfovibrio desulfuricans ND132 as a Model for Understanding Bacterial Mercury Methylation
journal, April 2011

  • Gilmour, Cynthia C.; Elias, Dwayne A.; Kucken, Amy M.
  • Applied and Environmental Microbiology, Vol. 77, Issue 12, p. 3938-3951
  • DOI: 10.1128/AEM.02993-10

Mercury Methylation by Novel Microorganisms from New Environments
journal, September 2013

  • Gilmour, Cynthia C.; Podar, Mircea; Bullock, Allyson L.
  • Environmental Science & Technology, Vol. 47, Issue 20
  • DOI: 10.1021/es403075t

Global landscape of cell envelope protein complexes in Escherichia coli
journal, November 2017

  • Babu, Mohan; Bundalovic-Torma, Cedoljub; Calmettes, Charles
  • Nature Biotechnology, Vol. 36, Issue 1
  • DOI: 10.1038/nbt.4024

Molecular Basis of Bacterial Outer Membrane Permeability Revisited
journal, December 2003


Microbial heavy-metal resistance
journal, June 1999


Efflux-mediated heavy metal resistance in prokaryotes
journal, June 2003


Bacterial mercury resistance from atoms to ecosystems
journal, June 2003


Organic and inorganic mercurials have distinct effects on cellular thiols, metal homeostasis, and Fe-binding proteins in Escherichia coli
journal, October 2015

  • LaVoie, Stephen P.; Mapolelo, Daphne T.; Cowart, Darin M.
  • JBIC Journal of Biological Inorganic Chemistry, Vol. 20, Issue 8
  • DOI: 10.1007/s00775-015-1303-1

Effect of the Deletion of qmoABC and the Promoter-Distal Gene Encoding a Hypothetical Protein on Sulfate Reduction in Desulfovibrio vulgaris Hildenborough
journal, June 2010

  • Zane, G. M.; Yen, H. -c. B.; Wall, J. D.
  • Applied and Environmental Microbiology, Vol. 76, Issue 16
  • DOI: 10.1128/AEM.00691-10

Nanomolar Copper Enhances Mercury Methylation by Desulfovibrio desulfuricans ND132
journal, May 2018


Methylmercury uptake and degradation by methanotrophs
journal, May 2017


Detailed Assessment of the Kinetics of Hg-Cell Association, Hg Methylation, and Methylmercury Degradation in Several Desulfovibrio Species
journal, August 2012

  • Graham, Andrew M.; Bullock, Allyson L.; Maizel, Andrew C.
  • Applied and Environmental Microbiology, Vol. 78, Issue 20, p. 7337-7346
  • DOI: 10.1128/AEM.01792-12

Thiol-Facilitated Cell Export and Desorption of Methylmercury by Anaerobic Bacteria
journal, September 2015


Methyl Mercury Contamination and Emission to the Atmosphere from Soil Amended with Municipal Sewage Sludge
journal, November 1997


Anaerobic Mercury Methylation and Demethylation by Geobacter bemidjiensis Bem
journal, April 2016

  • Lu, Xia; Liu, Yurong; Johs, Alexander
  • Environmental Science & Technology, Vol. 50, Issue 8
  • DOI: 10.1021/acs.est.6b00401

The Application and Potential Artifacts of Zeeman Cold Vapor Atomic Absorption Spectrometry in Mercury Stable Isotope Analysis
journal, February 2019


Importance of Dissolved Neutral Mercury Sulfides for Methyl Mercury Production in Contaminated Sediments
journal, April 2007

  • Drott, Andreas; Lambertsson, Lars; Björn, Erik
  • Environmental Science & Technology, Vol. 41, Issue 7
  • DOI: 10.1021/es061724z

Precipitation of Mercuric Sulfide Nanoparticles in NOM-Containing Water: Implications for the Natural Environment
journal, April 2009

  • Deonarine, Amrika; Hsu-Kim, Heileen
  • Environmental Science & Technology, Vol. 43, Issue 7
  • DOI: 10.1021/es803130h

Methylation of Mercury by Bacteria Exposed to Dissolved, Nanoparticulate, and Microparticulate Mercuric Sulfides
journal, January 2012

  • Zhang, Tong; Kim, Bojeong; Levard, Clément
  • Environmental Science & Technology, Vol. 46, Issue 13
  • DOI: 10.1021/es203181m

Effect of Dissolved Organic Matter Source and Character on Microbial Hg Methylation in Hg–S–DOM Solutions
journal, May 2013

  • Graham, Andrew M.; Aiken, George R.; Gilmour, Cynthia C.
  • Environmental Science & Technology, Vol. 47, Issue 11
  • DOI: 10.1021/es400414a

Why Mercury Prefers Soft Ligands
journal, June 2013

  • Riccardi, Demian; Guo, Hao-Bo; Parks, Jerry M.
  • The Journal of Physical Chemistry Letters, Vol. 4, Issue 14
  • DOI: 10.1021/jz401075b

Oxidation and methylation of dissolved elemental mercury by anaerobic bacteria
journal, August 2013

  • Hu, Haiyan; Lin, Hui; Zheng, Wang
  • Nature Geoscience, Vol. 6, Issue 9
  • DOI: 10.1038/ngeo1894

Nuclear magnetic resonance studies of the solution chemistry of metal complexes. 25. Hg(thiol)3 complexes and HG(II)-thiol ligand exchange kinetics
journal, September 1988

  • Cheesman, Bruce V.; Arnold, Alan P.; Rabenstein, Dallas L.
  • Journal of the American Chemical Society, Vol. 110, Issue 19
  • DOI: 10.1021/ja00227a014

Cysteine Addition Promotes Sulfide Production and 4-Fold Hg(II)–S Coordination in Actively Metabolizing Escherichia coli
journal, April 2017

  • Thomas, Sara A.; Gaillard, Jean-François
  • Environmental Science & Technology, Vol. 51, Issue 8
  • DOI: 10.1021/acs.est.6b06400

Works referencing / citing this record:

Optimization of a microplate reader method for the analysis of changes in mitochondrial membrane potential in Chlamydomonas reinhardtii cells using the fluorochrome JC-1
journal, July 2019

  • Harshkova, Darya; Zielińska, Elżbieta; Aksmann, Anna
  • Journal of Applied Phycology, Vol. 31, Issue 6
  • DOI: 10.1007/s10811-019-01860-3