Superoxide Dismutase and Pseudocatalase Increase Tolerance to Hg(II) in <named-content content-type="genus-species">Thermus thermophilus</named-content> HB27 by Maintaining the Reduced Bacillithiol Pool

ABSTRACT Mercury (Hg) is a widely distributed, toxic heavy metal with no known cellular role. Mercury toxicity has been linked to the production of reactive oxygen species (ROS), but Hg does not directly perform redox chemistry with oxygen. How exposure to the ionic form, Hg(II), generates ROS is un...

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Autores principales:	Javiera Norambuena, Thomas E. Hanson, Tamar Barkay, Jeffrey M. Boyd
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	Thermus thermophilus bacillithiol iron mercury pseudocatalase reactive oxygen species Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/cec60033bb854a0ab31edf2130818690
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spelling	oai:doaj.org-article:cec60033bb854a0ab31edf21308186902021-11-15T15:55:25ZSuperoxide Dismutase and Pseudocatalase Increase Tolerance to Hg(II) in <named-content content-type="genus-species">Thermus thermophilus</named-content> HB27 by Maintaining the Reduced Bacillithiol Pool10.1128/mBio.00183-192150-7511https://doaj.org/article/cec60033bb854a0ab31edf21308186902019-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00183-19https://doaj.org/toc/2150-7511ABSTRACT Mercury (Hg) is a widely distributed, toxic heavy metal with no known cellular role. Mercury toxicity has been linked to the production of reactive oxygen species (ROS), but Hg does not directly perform redox chemistry with oxygen. How exposure to the ionic form, Hg(II), generates ROS is unknown. Exposure of Thermus thermophilus to Hg(II) triggered ROS accumulation and increased transcription and activity of superoxide dismutase (Sod) and pseudocatalase (Pcat); however, Hg(II) inactivated Sod and Pcat. Strains lacking Sod or Pcat had increased oxidized bacillithiol (BSH) levels and were more sensitive to Hg(II) than the wild type. The ΔbshA Δsod and ΔbshA Δpcat double mutant strains were as sensitive to Hg(II) as the ΔbshA strain that lacks bacillithiol, suggesting that the increased sensitivity to Hg(II) in the Δsod and Δpcat mutant strains is due to a decrease of reduced BSH. Treatment of T. thermophilus with Hg(II) decreased aconitase activity and increased the intracellular concentration of free Fe, and these phenotypes were exacerbated in Δsod and Δpcat mutant strains. Treatment with Hg(II) also increased DNA damage. We conclude that sequestration of the redox buffering thiol BSH by Hg(II), in conjunction with direct inactivation of ROS-scavenging enzymes, impairs the ability of T. thermophilus to effectively metabolize ROS generated as a normal consequence of growth in aerobic environments. IMPORTANCE Thermus thermophilus is a deep-branching thermophilic aerobe. It is a member of the Deinococcus-Thermus phylum that, together with the Aquificae, constitute the earliest branching aerobic bacterial lineages; therefore, this organism serves as a model for early diverged bacteria (R. K. Hartmann, J. Wolters, B. Kröger, S. Schultze, et al., Syst Appl Microbiol 11:243–249, 1989, https://doi.org/10.1016/S0723-2020(89)80020-7) whose natural heated habitat may contain mercury of geological origins (G. G. Geesey, T. Barkay, and S. King, Sci Total Environ 569-570:321–331, 2016, https://doi.org/10.1016/j.scitotenv.2016.06.080). T. thermophilus likely arose shortly after the oxidation of the biosphere 2.4 billion years ago. Studying T. thermophilus physiology provides clues about the origin and evolution of mechanisms for mercury and oxidative stress responses, the latter being critical for the survival and function of all extant aerobes.Javiera NorambuenaThomas E. HansonTamar BarkayJeffrey M. BoydAmerican Society for MicrobiologyarticleThermus thermophilusbacillithiolironmercurypseudocatalasereactive oxygen speciesMicrobiologyQR1-502ENmBio, Vol 10, Iss 2 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	Thermus thermophilus bacillithiol iron mercury pseudocatalase reactive oxygen species Microbiology QR1-502
spellingShingle	Thermus thermophilus bacillithiol iron mercury pseudocatalase reactive oxygen species Microbiology QR1-502 Javiera Norambuena Thomas E. Hanson Tamar Barkay Jeffrey M. Boyd Superoxide Dismutase and Pseudocatalase Increase Tolerance to Hg(II) in <named-content content-type="genus-species">Thermus thermophilus</named-content> HB27 by Maintaining the Reduced Bacillithiol Pool
description	ABSTRACT Mercury (Hg) is a widely distributed, toxic heavy metal with no known cellular role. Mercury toxicity has been linked to the production of reactive oxygen species (ROS), but Hg does not directly perform redox chemistry with oxygen. How exposure to the ionic form, Hg(II), generates ROS is unknown. Exposure of Thermus thermophilus to Hg(II) triggered ROS accumulation and increased transcription and activity of superoxide dismutase (Sod) and pseudocatalase (Pcat); however, Hg(II) inactivated Sod and Pcat. Strains lacking Sod or Pcat had increased oxidized bacillithiol (BSH) levels and were more sensitive to Hg(II) than the wild type. The ΔbshA Δsod and ΔbshA Δpcat double mutant strains were as sensitive to Hg(II) as the ΔbshA strain that lacks bacillithiol, suggesting that the increased sensitivity to Hg(II) in the Δsod and Δpcat mutant strains is due to a decrease of reduced BSH. Treatment of T. thermophilus with Hg(II) decreased aconitase activity and increased the intracellular concentration of free Fe, and these phenotypes were exacerbated in Δsod and Δpcat mutant strains. Treatment with Hg(II) also increased DNA damage. We conclude that sequestration of the redox buffering thiol BSH by Hg(II), in conjunction with direct inactivation of ROS-scavenging enzymes, impairs the ability of T. thermophilus to effectively metabolize ROS generated as a normal consequence of growth in aerobic environments. IMPORTANCE Thermus thermophilus is a deep-branching thermophilic aerobe. It is a member of the Deinococcus-Thermus phylum that, together with the Aquificae, constitute the earliest branching aerobic bacterial lineages; therefore, this organism serves as a model for early diverged bacteria (R. K. Hartmann, J. Wolters, B. Kröger, S. Schultze, et al., Syst Appl Microbiol 11:243–249, 1989, https://doi.org/10.1016/S0723-2020(89)80020-7) whose natural heated habitat may contain mercury of geological origins (G. G. Geesey, T. Barkay, and S. King, Sci Total Environ 569-570:321–331, 2016, https://doi.org/10.1016/j.scitotenv.2016.06.080). T. thermophilus likely arose shortly after the oxidation of the biosphere 2.4 billion years ago. Studying T. thermophilus physiology provides clues about the origin and evolution of mechanisms for mercury and oxidative stress responses, the latter being critical for the survival and function of all extant aerobes.
format	article
author	Javiera Norambuena Thomas E. Hanson Tamar Barkay Jeffrey M. Boyd
author_facet	Javiera Norambuena Thomas E. Hanson Tamar Barkay Jeffrey M. Boyd
author_sort	Javiera Norambuena
title	Superoxide Dismutase and Pseudocatalase Increase Tolerance to Hg(II) in <named-content content-type="genus-species">Thermus thermophilus</named-content> HB27 by Maintaining the Reduced Bacillithiol Pool
title_short	Superoxide Dismutase and Pseudocatalase Increase Tolerance to Hg(II) in <named-content content-type="genus-species">Thermus thermophilus</named-content> HB27 by Maintaining the Reduced Bacillithiol Pool
title_full	Superoxide Dismutase and Pseudocatalase Increase Tolerance to Hg(II) in <named-content content-type="genus-species">Thermus thermophilus</named-content> HB27 by Maintaining the Reduced Bacillithiol Pool
title_fullStr	Superoxide Dismutase and Pseudocatalase Increase Tolerance to Hg(II) in <named-content content-type="genus-species">Thermus thermophilus</named-content> HB27 by Maintaining the Reduced Bacillithiol Pool
title_full_unstemmed	Superoxide Dismutase and Pseudocatalase Increase Tolerance to Hg(II) in <named-content content-type="genus-species">Thermus thermophilus</named-content> HB27 by Maintaining the Reduced Bacillithiol Pool
title_sort	superoxide dismutase and pseudocatalase increase tolerance to hg(ii) in <named-content content-type="genus-species">thermus thermophilus</named-content> hb27 by maintaining the reduced bacillithiol pool
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/cec60033bb854a0ab31edf2130818690
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Superoxide Dismutase and Pseudocatalase Increase Tolerance to Hg(II) in <named-content content-type="genus-species">Thermus thermophilus</named-content> HB27 by Maintaining the Reduced Bacillithiol Pool

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