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Title: The use of a mercury biosensor to evaluate the bioavailability of mercury-thiol complexes and mechanisms of mercury uptake in bacteria

Abstract

As mercury (Hg) biosensors are sensitive to only intracellular Hg, they are useful in the investigation of Hg uptake mechanisms and the effects of speciation on Hg bioavailability to microbes. In this study, bacterial biosensors were used to evaluate the roles that several transporters such as the glutathione, cystine/cysteine, and Mer transporters play in the uptake of Hg from Hg-thiol complexes by comparing uptake rates in strains with functioning transport systems to strains where these transporters had been knocked out by deletion of key genes. The Hg uptake into the biosensors was quantified based on the intracellular conversion of inorganic mercury (Hg(II)) to elemental mercury (Hg(0)) by the enzyme MerA. It was found that uptake of Hg from Hg-cysteine (Hg(CYS)2) and Hg-glutathione (Hg(GSH)2) complexes occurred at the same rate as that of inorganic complexes of Hg(II) into Escherichia coli strains with and without intact Mer transport systems. However, higher rates of Hg uptake were observed in the strain with a functioning Mer transport system. These results demonstrate that thiol-bound Hg is bioavailable to E. coli and that this bioavailability is higher in Hg-resistant bacteria with a complete Mer system than in non-resistant strains. No difference in the uptake rate ofmore » Hg from Hg(GSH)2 was observed in E. coli strains with or without functioning glutathione transport systems. There was also no difference in uptake rates between a wildtype Bacillus subtilis strain with a functioning cystine/cysteine transport system, and a mutant strain where this transport system had been knocked out. These results cast doubt on the viability of the hypothesis that the entire Hg-thiol complex is taken up into the cell by a thiol transporter. It is more likely that the Hg in the Hg-thiol complex is transferred to a transport protein on the cell membrane and is subsequently internalized.« less

Authors:
 [1];  [2];  [3];  [4];  [5];  [2];  [2];  [6]
  1. Rutgers Univ., New Brunswick, NJ (United States); Duke Univ., Durham, NC (United States)
  2. Rutgers Univ., New Brunswick, NJ (United States)
  3. Univ. of Connecticut, Groton, CT (United States)
  4. Harvard School of Public Health, Boston, MA (United States)
  5. King Abdul-Aziz Univ., Jeddah (Saudi Arabia)
  6. Cornell Univ., Ithaca, NY (United States)
Publication Date:
Research Org.:
Rutgers Univ., New Brunswick, NJ (United States); Rutgers Univ., Piscataway, NJ (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1324975
Alternate Identifier(s):
OSTI ID: 1454700
Grant/Contract Number:  
SC0007051; sc0007051
Resource Type:
Accepted Manuscript
Journal Name:
PLoS ONE
Additional Journal Information:
Journal Volume: 10; Journal Issue: 9; Journal ID: ISSN 1932-6203
Publisher:
Public Library of Science
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; bacillus stubtilis; glutathione; cysteine; thiols; biosensors; biological transport; synport proteins; cell membranes

Citation Formats

Ndu, Udonna, Barkay, Tamar, Mason, Robert P., Schartup, Amina Traore, Al-Farawati, Radwan, Liu, Jie, Reinfelder, John R., and Chang, Yung -Fu. The use of a mercury biosensor to evaluate the bioavailability of mercury-thiol complexes and mechanisms of mercury uptake in bacteria. United States: N. p., 2015. Web. doi:10.1371/journal.pone.0138333.
Ndu, Udonna, Barkay, Tamar, Mason, Robert P., Schartup, Amina Traore, Al-Farawati, Radwan, Liu, Jie, Reinfelder, John R., & Chang, Yung -Fu. The use of a mercury biosensor to evaluate the bioavailability of mercury-thiol complexes and mechanisms of mercury uptake in bacteria. United States. doi:10.1371/journal.pone.0138333.
Ndu, Udonna, Barkay, Tamar, Mason, Robert P., Schartup, Amina Traore, Al-Farawati, Radwan, Liu, Jie, Reinfelder, John R., and Chang, Yung -Fu. Tue . "The use of a mercury biosensor to evaluate the bioavailability of mercury-thiol complexes and mechanisms of mercury uptake in bacteria". United States. doi:10.1371/journal.pone.0138333. https://www.osti.gov/servlets/purl/1324975.
@article{osti_1324975,
title = {The use of a mercury biosensor to evaluate the bioavailability of mercury-thiol complexes and mechanisms of mercury uptake in bacteria},
author = {Ndu, Udonna and Barkay, Tamar and Mason, Robert P. and Schartup, Amina Traore and Al-Farawati, Radwan and Liu, Jie and Reinfelder, John R. and Chang, Yung -Fu},
abstractNote = {As mercury (Hg) biosensors are sensitive to only intracellular Hg, they are useful in the investigation of Hg uptake mechanisms and the effects of speciation on Hg bioavailability to microbes. In this study, bacterial biosensors were used to evaluate the roles that several transporters such as the glutathione, cystine/cysteine, and Mer transporters play in the uptake of Hg from Hg-thiol complexes by comparing uptake rates in strains with functioning transport systems to strains where these transporters had been knocked out by deletion of key genes. The Hg uptake into the biosensors was quantified based on the intracellular conversion of inorganic mercury (Hg(II)) to elemental mercury (Hg(0)) by the enzyme MerA. It was found that uptake of Hg from Hg-cysteine (Hg(CYS)2) and Hg-glutathione (Hg(GSH)2) complexes occurred at the same rate as that of inorganic complexes of Hg(II) into Escherichia coli strains with and without intact Mer transport systems. However, higher rates of Hg uptake were observed in the strain with a functioning Mer transport system. These results demonstrate that thiol-bound Hg is bioavailable to E. coli and that this bioavailability is higher in Hg-resistant bacteria with a complete Mer system than in non-resistant strains. No difference in the uptake rate of Hg from Hg(GSH)2 was observed in E. coli strains with or without functioning glutathione transport systems. There was also no difference in uptake rates between a wildtype Bacillus subtilis strain with a functioning cystine/cysteine transport system, and a mutant strain where this transport system had been knocked out. These results cast doubt on the viability of the hypothesis that the entire Hg-thiol complex is taken up into the cell by a thiol transporter. It is more likely that the Hg in the Hg-thiol complex is transferred to a transport protein on the cell membrane and is subsequently internalized.},
doi = {10.1371/journal.pone.0138333},
journal = {PLoS ONE},
number = 9,
volume = 10,
place = {United States},
year = {2015},
month = {9}
}

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Cited by: 5 works
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Figures / Tables:

Table 1. Table 1.: A list of strains used in this study.

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Works referenced in this record:

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Effect of Inorganic and Organic Ligands on the Bioavailability of Methylmercury as Determined by Using a mer-lux Bioreporter
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Aspects of Bioavailability of Mercury for Methylation in Pure Cultures of Desulfobulbus propionicus (1pr3)
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Construction of two lux-tagged Hg2+-specific biosensors and their luminescence performance
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The yliA, -B, -C, and -D Genes of Escherichia coli K-12 Encode a Novel Glutathione Importer with an ATP-Binding Cassette
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Simple and simultaneous determination of glutathione, thioacetamide and refractory organic matter in natural waters by DP-CSV
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Bioluminescence Biosensor for the Detection of Organomercury Contamination
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Three Different Systems Participate in L-Cystine Uptake in Bacillus subtilis
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Dissolved Organic Carbon Thresholds Affect Mercury Bioaccumulation in Arctic Lakes
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Mercury reduction and complexation by natural organic matter in anoxic environments
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Data from: The use of a mercury biosensor to evaluate the bioavailability of mercury-thiol complexes and mechanisms of mercury uptake in bacteria
dataset, September 2015

  • Ndu, Udonna; Barkay, Tamar; Mason, Robert P.
  • Dryad Digital Repository-Supplementary information for journal article at DOI: 10.1371/journal.pone.0138333, 2 XLSX files
  • DOI: 10.5061/dryad.bc4gk

Organomercurials removal by heterogeneous merB genes harboring bacterial strains
journal, July 2010

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A GFP-based bacterial biosensor with chromosomally integrated sensing cassette for quantitative detection of Hg(II) in environment
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Adaptation of chemosynthetic microorganisms to elevated mercury concentrations in deep-sea hydrothermal vents
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Evidence for facilitated uptake of Hg(II) by Vibrio anguillarum and Escherichia coli under anaerobic and aerobic conditions
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Role of MerT and MerP from Pseudomonas K-62 Plasmid pMR26 in the Transport of Phenylmercury.
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Factors influencing the oxidation, reduction, methylation and demethylation of mercury species in coastal waters
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Roles of the Tn21 merT, merP, and merC gene products in mercury resistance and mercury binding.
journal, October 1992


Oxidation of Dissolved Elemental Mercury by Thiol Compounds under Anoxic Conditions
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Changes in the non-protein thiol pool and production of dissolved gaseous mercury in the marine diatom Thalassiosira weissflogii under mercury exposure
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Effects of dissolved organic carbon and salinity on bioavailability of mercury.
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Cell-density-dependent sensitivity of a mer-lux bioassay.
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Bacterial Oxidation of Mercury Metal Vapor, Hg(0)
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    Works referencing / citing this record:

    Three Different Systems Participate in L-Cystine Uptake in Bacillus subtilis
    journal, July 2004


    Stimulation of elemental mercury oxidation by SH compounds
    journal, March 1995

    • Yamamoto, M.; Hou, H.; Nakamura, K.
    • Bulletin of Environmental Contamination and Toxicology, Vol. 54, Issue 3
    • DOI: 10.1007/bf00195113

    Bacterial mercury resistance from atoms to ecosystems
    journal, June 2003


    Factors influencing the oxidation, reduction, methylation and demethylation of mercury species in coastal waters
    journal, December 2007


    Role of MerT and MerP from Pseudomonas K-62 Plasmid pMR26 in the Transport of Phenylmercury.
    journal, January 2000

    • Kiyono, Masako; Uno, Yoshio; Omura, Tomoko
    • Biological & Pharmaceutical Bulletin, Vol. 23, Issue 3
    • DOI: 10.1248/bpb.23.279

    A GFP-based bacterial biosensor with chromosomally integrated sensing cassette for quantitative detection of Hg(II) in environment
    journal, May 2012


    Construction of two lux-tagged Hg2+-specific biosensors and their luminescence performance
    journal, April 2008

    • Fu, Ya-Juan; Chen, Wen-Li; Huang, Qiao-Yun
    • Applied Microbiology and Biotechnology, Vol. 79, Issue 3
    • DOI: 10.1007/s00253-008-1442-1

    Changes in the non-protein thiol pool and production of dissolved gaseous mercury in the marine diatom Thalassiosira weissflogii under mercury exposure
    journal, December 2009


    Inorganic and Organic Sulfur Cycling in Salt-Marsh Pore Waters
    journal, May 1986


    Roles of the Tn21 merT, merP, and merC gene products in mercury resistance and mercury binding.
    journal, October 1992


    The role of cysteine and sulfide in the interplay between microbial Hg( ii ) uptake and sulfur metabolism
    journal, January 2019

    • Thomas, Sara A.; Catty, Patrice; Hazemann, Jean-Louis
    • Metallomics, Vol. 11, Issue 7
    • DOI: 10.1039/c9mt00077a

    Data from: The use of a mercury biosensor to evaluate the bioavailability of mercury-thiol complexes and mechanisms of mercury uptake in bacteria
    dataset, September 2015

    • Ndu, Udonna; Barkay, Tamar; Mason, Robert P.
    • Dryad Digital Repository-Supplementary information for journal article at DOI: 10.1371/journal.pone.0138333, 2 XLSX files
    • DOI: 10.5061/dryad.bc4gk

    Mercury Reduction and Oxidation by Reduced Natural Organic Matter in Anoxic Environments
    journal, November 2011

    • Zheng, Wang; Liang, Liyuan; Gu, Baohua
    • Environmental Science & Technology, Vol. 46, Issue 1
    • DOI: 10.1021/es203402p

    Thiols in Coastal Waters of the Western North Sea and English Channel
    journal, May 2001

    • Al-Farawati, Radwan; van den Berg, Constant M. G.
    • Environmental Science & Technology, Vol. 35, Issue 10
    • DOI: 10.1021/es000073i

    Potential for Mercury Reduction by Microbes in the High Arctic
    journal, February 2007

    • Poulain, A. J.; Ni Chadhain, S. M.; Ariya, P. A.
    • Applied and Environmental Microbiology, Vol. 73, Issue 7
    • DOI: 10.1128/aem.02701-06

    Versatile biosensor vectors for detection and quantification of mercury
    journal, December 2000


    Oxidation of Dissolved Elemental Mercury by Thiol Compounds under Anoxic Conditions
    journal, November 2013

    • Zheng, Wang; Lin, Hui; Mann, Benjamin F.
    • Environmental Science & Technology, Vol. 47, Issue 22
    • DOI: 10.1021/es402697u

    The role of cysteine and sulfide in the interplay between microbial Hg( ii ) uptake and sulfur metabolism
    journal, January 2019

    • Thomas, Sara A.; Catty, Patrice; Hazemann, Jean-Louis
    • Metallomics, Vol. 11, Issue 7
    • DOI: 10.1039/c9mt00077a

    Titration of sulphides and thiols in natural waters
    journal, January 1986


    Mercury reduction and complexation by natural organic matter in anoxic environments
    journal, January 2011

    • Gu, B.; Bian, Y.; Miller, C. L.
    • Proceedings of the National Academy of Sciences, Vol. 108, Issue 4
    • DOI: 10.1073/pnas.1008747108

    Effect of Inorganic and Organic Ligands on the Bioavailability of Methylmercury as Determined by Using a mer-lux Bioreporter
    journal, August 2012

    • Ndu, Udonna; Mason, Robert P.; Zhang, Huan
    • Applied and Environmental Microbiology, Vol. 78, Issue 20
    • DOI: 10.1128/aem.00362-12

    Data from: The use of a mercury biosensor to evaluate the bioavailability of mercury-thiol complexes and mechanisms of mercury uptake in bacteria
    dataset, September 2015

    • Ndu, Udonna; Barkay, Tamar; Mason, Robert P.
    • Dryad Digital Repository-Supplementary information for journal article at DOI: 10.1371/journal.pone.0138333, 2 XLSX files
    • DOI: 10.5061/dryad.bc4gk

    Simple and simultaneous determination of glutathione, thioacetamide and refractory organic matter in natural waters by DP-CSV
    journal, October 2013


    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

    The yliA, -B, -C, and -D Genes of Escherichia coli K-12 Encode a Novel Glutathione Importer with an ATP-Binding Cassette
    journal, August 2005


    Organomercurials removal by heterogeneous merB genes harboring bacterial strains
    journal, July 2010

    • Chien, Mei-Fang; Narita, Masaru; Lin, Kuo-Hsing
    • Journal of Bioscience and Bioengineering, Vol. 110, Issue 1
    • DOI: 10.1016/j.jbiosc.2010.01.010

    Bioluminescence Biosensor for the Detection of Organomercury Contamination
    journal, July 2003


    Dissolved Organic Carbon Thresholds Affect Mercury Bioaccumulation in Arctic Lakes
    journal, February 2014

    • French, Todd D.; Houben, Adam J.; Desforges, Jean-Pierre W.
    • Environmental Science & Technology, Vol. 48, Issue 6
    • DOI: 10.1021/es403849d

    Adaptation of chemosynthetic microorganisms to elevated mercury concentrations in deep-sea hydrothermal vents
    journal, January 2009

    • Crepo-Medina, Melitza; Chatziefthimiou, Aspassia D.; Bloom, Nicolas S.
    • Limnology and Oceanography, Vol. 54, Issue 1
    • DOI: 10.4319/lo.2009.54.1.0041

    The role of cysteine residues in the transport of mercuric ions by the Tn501 MerT and MerP mercury-resistance proteins
    journal, July 1995


    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

      Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.