Redox signaling through zinc activates the radiation response in Deinococcus bacteria

Abstract Deinococcus bacteria are extremely resistant to radiation and other DNA damage- and oxidative stress-generating conditions. An efficient SOS-independent response mechanism inducing expression of several DNA repair genes is essential for this resistance, and is controlled by metalloprotease...

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Autores principales:	Romaric Magerand, Pascal Rey, Laurence Blanchard, Arjan de Groot
Formato:	article
Lenguaje:	EN
Publicado:	Nature Portfolio 2021
Materias:	Medicine R Science Q
Acceso en línea:	https://doaj.org/article/63b07dd551b24d8eb9535cd4c5acd400
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spelling	oai:doaj.org-article:63b07dd551b24d8eb9535cd4c5acd4002021-12-02T13:19:22ZRedox signaling through zinc activates the radiation response in Deinococcus bacteria10.1038/s41598-021-84026-x2045-2322https://doaj.org/article/63b07dd551b24d8eb9535cd4c5acd4002021-02-01T00:00:00Zhttps://doi.org/10.1038/s41598-021-84026-xhttps://doaj.org/toc/2045-2322Abstract Deinococcus bacteria are extremely resistant to radiation and other DNA damage- and oxidative stress-generating conditions. An efficient SOS-independent response mechanism inducing expression of several DNA repair genes is essential for this resistance, and is controlled by metalloprotease IrrE that cleaves and inactivates transcriptional repressor DdrO. Here, we identify the molecular signaling mechanism that triggers DdrO cleavage. We show that reactive oxygen species (ROS) stimulate the zinc-dependent metalloprotease activity of IrrE in Deinococcus. Sudden exposure of Deinococcus to zinc excess also rapidly induces DdrO cleavage, but is not accompanied by ROS production and DNA damage. Further, oxidative treatment leads to an increase of intracellular free zinc, indicating that IrrE activity is very likely stimulated directly by elevated levels of available zinc ions. We conclude that radiation and oxidative stress induce changes in redox homeostasis that result in IrrE activation by zinc in Deinococcus. We propose that a part of the zinc pool coordinated with cysteine thiolates is released due to their oxidation. Predicted regulation systems involving IrrE- and DdrO-like proteins are present in many bacteria, including pathogens, suggesting that such a redox signaling pathway including zinc as a second messenger is widespread and participates in various stress responses.Romaric MagerandPascal ReyLaurence BlanchardArjan de GrootNature PortfolioarticleMedicineRScienceQENScientific Reports, Vol 11, Iss 1, Pp 1-12 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Medicine R Science Q
spellingShingle	Medicine R Science Q Romaric Magerand Pascal Rey Laurence Blanchard Arjan de Groot Redox signaling through zinc activates the radiation response in Deinococcus bacteria
description	Abstract Deinococcus bacteria are extremely resistant to radiation and other DNA damage- and oxidative stress-generating conditions. An efficient SOS-independent response mechanism inducing expression of several DNA repair genes is essential for this resistance, and is controlled by metalloprotease IrrE that cleaves and inactivates transcriptional repressor DdrO. Here, we identify the molecular signaling mechanism that triggers DdrO cleavage. We show that reactive oxygen species (ROS) stimulate the zinc-dependent metalloprotease activity of IrrE in Deinococcus. Sudden exposure of Deinococcus to zinc excess also rapidly induces DdrO cleavage, but is not accompanied by ROS production and DNA damage. Further, oxidative treatment leads to an increase of intracellular free zinc, indicating that IrrE activity is very likely stimulated directly by elevated levels of available zinc ions. We conclude that radiation and oxidative stress induce changes in redox homeostasis that result in IrrE activation by zinc in Deinococcus. We propose that a part of the zinc pool coordinated with cysteine thiolates is released due to their oxidation. Predicted regulation systems involving IrrE- and DdrO-like proteins are present in many bacteria, including pathogens, suggesting that such a redox signaling pathway including zinc as a second messenger is widespread and participates in various stress responses.
format	article
author	Romaric Magerand Pascal Rey Laurence Blanchard Arjan de Groot
author_facet	Romaric Magerand Pascal Rey Laurence Blanchard Arjan de Groot
author_sort	Romaric Magerand
title	Redox signaling through zinc activates the radiation response in Deinococcus bacteria
title_short	Redox signaling through zinc activates the radiation response in Deinococcus bacteria
title_full	Redox signaling through zinc activates the radiation response in Deinococcus bacteria
title_fullStr	Redox signaling through zinc activates the radiation response in Deinococcus bacteria
title_full_unstemmed	Redox signaling through zinc activates the radiation response in Deinococcus bacteria
title_sort	redox signaling through zinc activates the radiation response in deinococcus bacteria
publisher	Nature Portfolio
publishDate	2021
url	https://doaj.org/article/63b07dd551b24d8eb9535cd4c5acd400
work_keys_str_mv	AT romaricmagerand redoxsignalingthroughzincactivatestheradiationresponseindeinococcusbacteria AT pascalrey redoxsignalingthroughzincactivatestheradiationresponseindeinococcusbacteria AT laurenceblanchard redoxsignalingthroughzincactivatestheradiationresponseindeinococcusbacteria AT arjandegroot redoxsignalingthroughzincactivatestheradiationresponseindeinococcusbacteria
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Redox signaling through zinc activates the radiation response in Deinococcus bacteria

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