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Applied and Environmental Microbiology
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Environmental Microbiology

Mechanism of Attenuation of Uranyl Toxicity by Glutathione in Lactococcus lactis

Muhammad H. Obeid, Jana Oertel, Marc Solioz, Karim Fahmy
H. Nojiri, Editor
Muhammad H. Obeid
aHelmholtz-Zentrum Dresden-Rossendorf, Institute of Resource Ecology, and Technische Universität Dresden, Dresden, Germany
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Jana Oertel
aHelmholtz-Zentrum Dresden-Rossendorf, Institute of Resource Ecology, and Technische Universität Dresden, Dresden, Germany
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Marc Solioz
bLaboratory of Biochemistry and Molecular Biology, Tomsk State University, Tomsk, Russian Federation
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  • ORCID record for Marc Solioz
Karim Fahmy
aHelmholtz-Zentrum Dresden-Rossendorf, Institute of Resource Ecology, and Technische Universität Dresden, Dresden, Germany
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H. Nojiri
The University of Tokyo
Roles: Editor
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DOI: 10.1128/AEM.00538-16
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ABSTRACT

Both prokaryotic and eukaryotic organisms possess mechanisms for the detoxification of heavy metals, and these mechanisms are found among distantly related species. We investigated the role of intracellular glutathione (GSH), which, in a large number of taxa, plays a role in protection against the toxicity of common heavy metals. Anaerobically grown Lactococcus lactis containing an inducible GSH synthesis pathway was used as a model organism. Its physiological condition allowed study of putative GSH-dependent uranyl detoxification mechanisms without interference from additional reactive oxygen species. By microcalorimetric measurements of metabolic heat during cultivation, it was shown that intracellular GSH attenuates the toxicity of uranium at a concentration in the range of 10 to 150 μM. In this concentration range, no effect was observed with copper, which was used as a reference for redox metal toxicity. At higher copper concentrations, GSH aggravated metal toxicity. Isothermal titration calorimetry revealed the endothermic binding of U(VI) to the carboxyl group(s) of GSH rather than to the reducing thiol group involved in copper interactions. The data indicate that the primary detoxifying mechanism is the intracellular sequestration of carboxyl-coordinated U(VI) into an insoluble complex with GSH. The opposite effects on uranyl and on copper toxicity can be related to the difference in coordination chemistry of the respective metal-GSH complexes, which cause distinct growth phase-specific effects on enzyme-metal interactions.

IMPORTANCE Understanding microbial metal resistance is of particular importance for bioremediation, where microorganisms are employed for the removal of heavy metals from the environment. This strategy is increasingly being considered for uranium. However, little is known about the molecular mechanisms of uranyl detoxification. Existing studies of different taxa show little systematics but hint at a role of glutathione (GSH). Previous work could not unequivocally demonstrate a GSH function in decreasing the presumed uranyl-induced oxidative stress, nor could a redox-independent detoxifying action of GSH be identified. Combining metabolic calorimetry with cell number-based assays and genetics analysis enables a novel and general approach to quantify toxicity and relate it to molecular mechanisms. The results show that GSH-expressing microorganisms appear advantageous for uranyl bioremediation.

FOOTNOTES

    • Received 25 February 2016.
    • Accepted 3 April 2016.
    • Accepted manuscript posted online 8 April 2016.
  • Supplemental material for this article may be found at http://dx.doi.org/10.1128/AEM.00538-16.

  • Copyright © 2016, American Society for Microbiology. All Rights Reserved.
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Mechanism of Attenuation of Uranyl Toxicity by Glutathione in Lactococcus lactis
Muhammad H. Obeid, Jana Oertel, Marc Solioz, Karim Fahmy
Applied and Environmental Microbiology May 2016, 82 (12) 3563-3571; DOI: 10.1128/AEM.00538-16

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Mechanism of Attenuation of Uranyl Toxicity by Glutathione in Lactococcus lactis
Muhammad H. Obeid, Jana Oertel, Marc Solioz, Karim Fahmy
Applied and Environmental Microbiology May 2016, 82 (12) 3563-3571; DOI: 10.1128/AEM.00538-16
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