Proteins Needed to Activate a Transcriptional Response to the Reactive Oxygen Species Singlet Oxygen

ABSTRACT Singlet oxygen (1O2) is a reactive oxygen species generated by energy transfer from one or more excited donors to molecular oxygen. Many biomolecules are prone to oxidation by 1O2, and cells have evolved systems to protect themselves from damage caused by this compound. One way that the pho...

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Autores principales: Tae-Wook Nam, Eva C. Ziegelhoffer, Rachelle A. S. Lemke, Timothy J. Donohue
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Publicado: American Society for Microbiology 2013
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spelling oai:doaj.org-article:7f0d5f68631e475482453fef480b774a2021-11-15T15:40:22ZProteins Needed to Activate a Transcriptional Response to the Reactive Oxygen Species Singlet Oxygen10.1128/mBio.00541-122150-7511https://doaj.org/article/7f0d5f68631e475482453fef480b774a2013-03-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00541-12https://doaj.org/toc/2150-7511ABSTRACT Singlet oxygen (1O2) is a reactive oxygen species generated by energy transfer from one or more excited donors to molecular oxygen. Many biomolecules are prone to oxidation by 1O2, and cells have evolved systems to protect themselves from damage caused by this compound. One way that the photosynthetic bacterium Rhodobacter sphaeroides protects itself from 1O2 is by inducing a transcriptional response controlled by ChrR, an anti-σ factor which releases an alternative sigma factor, σE, in the presence of 1O2. Here we report that induction of σE-dependent gene transcription is decreased in the presence of 1O2 when two conserved genes in the σE regulon are deleted, including one encoding a cyclopropane fatty acid synthase homologue (RSP2144) or one encoding a protein of unknown function (RSP1091). Thus, we conclude that RSP2144 and RSP1091 are each necessary to increase σE activity in the presence of 1O2. In addition, we found that unlike in wild-type cells, where ChrR is rapidly degraded when 1O2 is generated, turnover of this anti-σ factor is slowed when cells lacking RSP2144, RSP1091, or both of these proteins are exposed to 1O2. Further, we demonstrate that the organic hydroperoxide tert-butyl hydroperoxide promotes ChrR turnover in both wild-type cells and mutants lacking RSP2144 or RSP1091, suggesting differences in the ways different types of oxidants increase σE activity. IMPORTANCE Oxygen serves many crucial functions on Earth; it is produced during photosynthesis and needed for other pathways. While oxygen is relatively inert, it can be converted to reactive oxygen species (ROS) that destroy biomolecules, cause disease, or kill cells. When energy is transferred to oxygen, the ROS singlet oxygen is generated. To understand how singlet oxygen impacts cells, we study the stress response to this ROS in Rhodobacter sphaeroides, a bacterium that, like plants, generates this compound as a consequence of photosynthesis. This paper identifies proteins that activate a stress response to singlet oxygen and shows that they act in a specific response to this ROS. The identified proteins are found in many free-living, symbiotic, or pathogenic bacteria that can encounter singlet oxygen in nature. Thus, our findings provide new information about a stress response to a ROS of broad biological, agricultural, and biomedical importance.Tae-Wook NamEva C. ZiegelhofferRachelle A. S. LemkeTimothy J. DonohueAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 4, Iss 1 (2013)
institution DOAJ
collection DOAJ
language EN
topic Microbiology
QR1-502
spellingShingle Microbiology
QR1-502
Tae-Wook Nam
Eva C. Ziegelhoffer
Rachelle A. S. Lemke
Timothy J. Donohue
Proteins Needed to Activate a Transcriptional Response to the Reactive Oxygen Species Singlet Oxygen
description ABSTRACT Singlet oxygen (1O2) is a reactive oxygen species generated by energy transfer from one or more excited donors to molecular oxygen. Many biomolecules are prone to oxidation by 1O2, and cells have evolved systems to protect themselves from damage caused by this compound. One way that the photosynthetic bacterium Rhodobacter sphaeroides protects itself from 1O2 is by inducing a transcriptional response controlled by ChrR, an anti-σ factor which releases an alternative sigma factor, σE, in the presence of 1O2. Here we report that induction of σE-dependent gene transcription is decreased in the presence of 1O2 when two conserved genes in the σE regulon are deleted, including one encoding a cyclopropane fatty acid synthase homologue (RSP2144) or one encoding a protein of unknown function (RSP1091). Thus, we conclude that RSP2144 and RSP1091 are each necessary to increase σE activity in the presence of 1O2. In addition, we found that unlike in wild-type cells, where ChrR is rapidly degraded when 1O2 is generated, turnover of this anti-σ factor is slowed when cells lacking RSP2144, RSP1091, or both of these proteins are exposed to 1O2. Further, we demonstrate that the organic hydroperoxide tert-butyl hydroperoxide promotes ChrR turnover in both wild-type cells and mutants lacking RSP2144 or RSP1091, suggesting differences in the ways different types of oxidants increase σE activity. IMPORTANCE Oxygen serves many crucial functions on Earth; it is produced during photosynthesis and needed for other pathways. While oxygen is relatively inert, it can be converted to reactive oxygen species (ROS) that destroy biomolecules, cause disease, or kill cells. When energy is transferred to oxygen, the ROS singlet oxygen is generated. To understand how singlet oxygen impacts cells, we study the stress response to this ROS in Rhodobacter sphaeroides, a bacterium that, like plants, generates this compound as a consequence of photosynthesis. This paper identifies proteins that activate a stress response to singlet oxygen and shows that they act in a specific response to this ROS. The identified proteins are found in many free-living, symbiotic, or pathogenic bacteria that can encounter singlet oxygen in nature. Thus, our findings provide new information about a stress response to a ROS of broad biological, agricultural, and biomedical importance.
format article
author Tae-Wook Nam
Eva C. Ziegelhoffer
Rachelle A. S. Lemke
Timothy J. Donohue
author_facet Tae-Wook Nam
Eva C. Ziegelhoffer
Rachelle A. S. Lemke
Timothy J. Donohue
author_sort Tae-Wook Nam
title Proteins Needed to Activate a Transcriptional Response to the Reactive Oxygen Species Singlet Oxygen
title_short Proteins Needed to Activate a Transcriptional Response to the Reactive Oxygen Species Singlet Oxygen
title_full Proteins Needed to Activate a Transcriptional Response to the Reactive Oxygen Species Singlet Oxygen
title_fullStr Proteins Needed to Activate a Transcriptional Response to the Reactive Oxygen Species Singlet Oxygen
title_full_unstemmed Proteins Needed to Activate a Transcriptional Response to the Reactive Oxygen Species Singlet Oxygen
title_sort proteins needed to activate a transcriptional response to the reactive oxygen species singlet oxygen
publisher American Society for Microbiology
publishDate 2013
url https://doaj.org/article/7f0d5f68631e475482453fef480b774a
work_keys_str_mv AT taewooknam proteinsneededtoactivateatranscriptionalresponsetothereactiveoxygenspeciessingletoxygen
AT evacziegelhoffer proteinsneededtoactivateatranscriptionalresponsetothereactiveoxygenspeciessingletoxygen
AT rachelleaslemke proteinsneededtoactivateatranscriptionalresponsetothereactiveoxygenspeciessingletoxygen
AT timothyjdonohue proteinsneededtoactivateatranscriptionalresponsetothereactiveoxygenspeciessingletoxygen
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