Key Points
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Photo-oxidative stress is induced by the formation of the reactive oxygen species singlet oxygen, which is often caused by energy transfer from a light-excited donor to molecular oxygen.
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Carotenoids protect photosynthetic organisms such as Rhodobacter sphaeroides from the photo-oxidative damage that is caused by this energy transfer.
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The alternative σ-factor σE is the master regulator of the photo-oxidative stress response in R. sphaeroides.
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Some known σE target genes are found in many bacteria (forming the core σE regulon), whereas others are predicted to be part of the photo-oxidative stress response in only a subset of species (known as the extended σE regulon).
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The proposed core and extended σE regulons encode few proteins of known or predicted protective function, but how cells respond to photo-oxidative stress is largely unknown, as many target genes have no annotated function as yet.
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Conservation of the proposed core σE regulon suggests that the photo-oxidative stress response is broadly represented both in photosynthetic bacteria and in non-photosynthetic microorganisms that can generate singlet oxygen from light-dependent or light-independent processes.
Abstract
Singlet oxygen is one of several reactive oxygen species that can destroy biomolecules, microorganisms and other cells. Traditionally, the response to singlet oxygen has been termed photo-oxidative stress, as light-dependent processes in photosynthetic cells are major biological sources of singlet oxygen. Recent work identifying a core set of singlet oxygen stress response genes across various bacterial species highlights the importance of this response for survival by both photosynthetic and non-photosynthetic cells. Here, we review how bacterial cells mount a transcriptional response to photo-oxidative stress in the context of what is known about bacterial stress responses to other reactive oxygen species.
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Acknowledgements
Work on the singlet oxygen stress response has been supported by the Department of Energy (DE-FG02-05ER15653) and, more recently, by the National Institutes of General Medical Sciences (GM075273). The authors thank Y.S. Dufour and H.A. Green for allowing us to discuss their unpublished results. We also thank Y. Dufour for advice on the production of Figure 4. Furthermore, we recognize past and current members of the Donohue laboratory for their contribution to the observations summarized in this work.
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FURTHER INFORMATION
Glossary
- Diradical
-
A molecular species with two electrons occupying two degenerate molecular orbitals, typified by high reactivity and a short lifespan.
- Fenton reaction
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The reaction in which free ferrous iron (Fe2+) transfers an electron to hydrogen peroxide (H2O2) to produce a hydroxyl radical (OH·): H2O2 + Fe2+ → OH− + FeO2+ + H+ → Fe3+ + OH− + OH·
- Triplet excited state
-
The higher energy state of a molecule that is characterized by an electron paramagnetic resonance spectrum with three peaks.
- Photosensitizer
-
A chemical compound that readily undergoes photo-excitation and then transfers its energy to other molecules, resulting in a reaction mixture that is sensitive to light.
- Respiratory burst
-
The rapid release of reactive oxygen species from neutrophils and macrophages of the immune system.
- Paraquat
-
A redox cycling agent that can be oxidized by dioxygen, resulting in the production of superoxide; also called methyl viologen.
- Isozymes
-
Any of the electrophoretically distinct forms of an enzyme, which represent different polymeric states but have the same function.
- Carotenoids
-
A class of pigments that are widely distributed in nature; pigments can be yellow, orange, red or purple.
- Photosynthetic reaction centre
-
A site where molecular excitations originating from light are transformed into a series of electron transfer reactions. It is composed of a multiprotein complex containing pigmented cofactors (such as chlorophyll).
- Phototroph
-
An organism that uses light as a source of metabolic energy.
- Dane-Py
-
(3-(N-diethylaminoethyl)-N-dansyl-aminomethyl-2,5-dihydro-2,2,5,5-tetramethyl-1-H-pyrrole.) A fluorescent molecular trap that is specific for singlet oxygen; excitation occurs at 337 nm, with emission at 545 nm.
- Electron paramagnetic resonance spin trapping
-
Experiments in which a particular electron spin state of a molecule is isolated to measure its spectrum.
- σ-factor
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A specificity subunit of prokaryotic RNA polymerase that directs the RNA polymerase holoenzyme to the promoter DNA of specific genes. The primary σ-factor in cells is responsible for the recognition of so-called housekeeping genes, and alternative σ-factors are devoted to specialized functions.
- Methylene blue
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A photosensitizer that is used to generate singlet oxygen when it is exposed to both oxygen and light.
- Rose bengal
-
A widely used stain that also functions as a photosensitizer, specifically to generate singlet oxygen from ground state triplet oxygen.
- Position-specific weighted matrix
-
A statistical representation of patterns in biological sequences, composed of a matrix of score values that gives a weighted match to any given substring of fixed length.
- Photolyase
-
An enzyme that repairs DNA that has been damaged by ultraviolet light exposure by breaking pyrimidine dimers.
- Thylakoid
-
An internal membrane system occupying the main body of a plastid; particularly well-developed in chloroplasts.
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Ziegelhoffer, E., Donohue, T. Bacterial responses to photo-oxidative stress. Nat Rev Microbiol 7, 856–863 (2009). https://doi.org/10.1038/nrmicro2237
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DOI: https://doi.org/10.1038/nrmicro2237
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