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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]
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  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.
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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. https://doi.org/10.1371/journal.pone.0138333
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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. https://doi.org/10.1371/journal.pone.0138333. https://www.osti.gov/servlets/purl/1324975.
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@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 = {Tue Sep 15 00:00:00 EDT 2015},
month = {Tue Sep 15 00:00:00 EDT 2015}
}
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Journal Article:
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Publisher's Version of Record
https://doi.org/10.1371/journal.pone.0138333
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Cited by: 27 works
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Figures / Tables:

Table 1. Table 1.: A list of strains used in this study.
All figures and tables (8 total)
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Works referenced in this record:

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Titration of sulphides and thiols in natural waters
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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
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Potential for Mercury Reduction by Microbes in the High Arctic
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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

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

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

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

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

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

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

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

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

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

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

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

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

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

Effect of Inorganic and Organic Ligands on the Bioavailability of Methylmercury as Determined by Using a mer-lux Bioreporter
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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
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    Works referencing / citing this record:

    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

    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
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