Oxygen intervention in the regulation of gene expression: the photosynthetic bacterial paradigm

Zeilstra-Ryalls, Jill H.; Kaplan, Samuel

doi:10.1007/s00018-003-3242-1

Cited by 79 publications

(93 citation statements)

References 125 publications

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“…The environmental stimuli that affect the formation of photosynthetic complexes in Rhodobacter sphaeroides are oxygen tension and light intensity, and these have been investigated in detail (Bauer et al, 1999;Gregor & Klug, 1999Zeilstra-Ryalls & Kaplan, 2004).…”

Section: Introductionmentioning

confidence: 99%

Photo-oxidative stress in Rhodobacter sphaeroides: protective role of carotenoids and expression of selected genes

2005

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In Rhodobacter sphaeroides, carotenoids are essential constituents of the photosynthetic apparatus and are assumed to prevent the formation of singlet oxygen by quenching of triplet bacteriochlorophyll a (BChl a) in vivo. It was shown that small amounts of singlet oxygen are generated in vivo by incubation of R. sphaeroides under high light conditions. However, growth and survival rates were not affected. Higher amounts of singlet oxygen were generated by BChl a in a carotenoid-deficient strain and led to a decrease in growth and survival rates. The data support earlier results on the pivotal role of carotenoids in the defence against stress caused by singlet oxygen. Results obtained under photo-oxidative stress conditions with strains impaired in carotenoid synthesis suggest that sphaeroidene and neurosporene provide less protection against methylene-blue-generated singlet oxygen than sphaeroidenone in vivo. Despite their protective function against singlet oxygen, relative amounts of carotenoids did not accumulate in R. sphaeroides wild-type cultures under photo-oxidative stress, and relative mRNA levels of phytoene dehydrogenase and sphaeroidene monooxygenase did not increase. In contrast, singlet oxygen specifically induced the expression of glutathione peroxidase and a putative Zn-dependent hydrolase, but mRNA levels of hydrogen-peroxide-degrading catalase E were not significantly affected by photo-oxidative stress. Based on these results, it is suggested that singlet oxygen acts as a specific signal for gene expression in R. sphaeroides. Presumably transcriptional regulators exist to specifically induce the expression of genes involved in the response to stress caused by singlet oxygen.

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Section: Introductionmentioning

confidence: 99%

Photo-oxidative stress in Rhodobacter sphaeroides: protective role of carotenoids and expression of selected genes

2005

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“…These bacteria tightly control the synthesis of their electron transfer proteins involved in each growth mode in response to a specific electron donor, oxygen tension, and light intensity (7,8). Among these regulatory systems, oxygen-and lightsensing mechanisms have been well-studied; however, mechanisms used to sense hydrogen sulfide remain incompletely understood.…”

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confidence: 99%

Sulfide-responsive transcriptional repressor SqrR functions as a master regulator of sulfide-dependent photosynthesis

Shimizu

Shen

Fang

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

113

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Sulfide was used as an electron donor early in the evolution of photosynthesis, with many extant photosynthetic bacteria still capable of using sulfur compounds such as hydrogen sulfide (H 2 S) as a photosynthetic electron donor. Although enzymes involved in H 2 S oxidation have been characterized, mechanisms of regulation of sulfide-dependent photosynthesis have not been elucidated. In this study, we have identified a sulfide-responsive transcriptional repressor, SqrR, that functions as a master regulator of sulfide-dependent gene expression in the purple photosynthetic bacterium Rhodobacter capsulatus. SqrR has three cysteine residues, two of which, C41 and C107, are conserved in SqrR homologs from other bacteria. Analysis with liquid chromatography coupled with an electrospray-interface tandem-mass spectrometer reveals that SqrR forms an intramolecular tetrasulfide bond between C41 and C107 when incubated with the sulfur donor glutathione persulfide. SqrR is oxidized in sulfidestressed cells, and tetrasulfide-cross-linked SqrR binds more weakly to a target promoter relative to unmodified SqrR. C41S and C107S R. capsulatus SqrRs lack the ability to respond to sulfide, and constitutively repress target gene expression in cells. These results establish that SqrR is a sensor of H 2 S-derived reactive sulfur species that maintain sulfide homeostasis in this photosynthetic bacterium and reveal the mechanism of sulfide-dependent transcriptional derepression of genes involved in sulfide metabolism.sulfide sensor | photosynthesis regulation | reactive sulfur species | purple bacteria | Rhodobacter T he discovery of ∼550 deep-sea hydrothermal vents more than 30 y ago (1) has led to the theory that energy metabolism in early ancestral organisms may have arisen from deep-sea hydrothermal vents where simple inorganic molecules such as hydrogen sulfide or hydrogen gas, as well as methane, exist (2-4). Such ancient energy metabolism has been assumed to be similar to that of extant chemolithotrophs, which obtain energy from these molecules. Indeed, various chemolithoautotrophic microbes thrive in deep-sea hydrothermal vents and are capable of oxidizing sulfides, methane, and/or hydrogen gas for use as energy sources and electron donors (5). Some photosynthetic bacteria have also been isolated from deep-sea hydrothermal vents that can grow photosynthetically using sulfide as an electron donor and geothermal radiation as an energy source instead of solar radiation (6), as hypothesized for ancestral phototrophs.Many purple photosynthetic bacteria have remarkable metabolic versatility required to meet the energy demands of sulfidedependent and -independent photosynthesis as well as aerobic and anaerobic respiration. These bacteria tightly control the synthesis of their electron transfer proteins involved in each growth mode in response to a specific electron donor, oxygen tension, and light intensity (7, 8). Among these regulatory systems, oxygen-and lightsensing mechanisms have been well-studied; however, mechanisms used to sen...

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“…Rhodobacter sphaeroides forms photosynthetic complexes only when the oxygen tension in the environment is low. Oxygen-regulated transcription of photosynthesis genes has been extensively studied in the past in different Rhodobacter species, and several redox-dependent regulatory pathways have been investigated in detail (1)(2)(3)(4)(5).…”

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confidence: 99%

“…The AppA protein of R. sphaeroides was originally described as part of a major redox signal chain (9) controlling, together with the PrrB͞PrrA two-component system, Fnr and thioredoxin 1, the oxygen-dependent expression of photosynthesis genes (5). The high puf and puc transcript levels of wild-type cells in the dark and their strong decrease after blue-light irradiation at intermediate oxygen tension depend on AppA (7).…”

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confidence: 99%

A eukaryotic BLUF domain mediates light-dependent gene expression in the purple bacterium Rhodobacter sphaeroides 2.4.1

Han

Braatsch

Osterloh

et al. 2004

Proc. Natl. Acad. Sci. U.S.A.

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The flavin-binding BLUF domain functions as a blue-light receptor in eukaryotes and bacteria. In the photoreceptor protein photoactivated adenylyl cyclase (PAC) from the flagellate Euglena gracilis, the BLUF domain is linked to an adenylyl cyclase domain. The PAC protein mediates a photophobic response. In the AppA protein of Rhodobacter sphaeroides, the BLUF domain is linked to a downstream domain without similarity to known proteins. AppA functions as a transcriptional antirepressor, controlling photosynthesis gene expression in the purple bacterium R. sphaeroides in response to light and oxygen. We fused the PAC␣1-BLUF domain from Euglena to the C terminus of AppA. Our results show that the hybrid protein is fully functional in light-dependent gene repression in R. sphaeroides, despite only Ϸ30% identity between the eukaryotic and the bacterial BLUF domains. Furthermore, the bacterial BLUF domain and the C terminus of AppA can transmit the light signal even when expressed as separated domains. This finding implies that the BLUF domain is fully modular and can relay signals to completely different output domains.

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Oxygen intervention in the regulation of gene expression: the photosynthetic bacterial paradigm

Cited by 79 publications

References 125 publications

Photo-oxidative stress in Rhodobacter sphaeroides: protective role of carotenoids and expression of selected genes

Photo-oxidative stress in Rhodobacter sphaeroides: protective role of carotenoids and expression of selected genes

Sulfide-responsive transcriptional repressor SqrR functions as a master regulator of sulfide-dependent photosynthesis

A eukaryotic BLUF domain mediates light-dependent gene expression in the purple bacterium Rhodobacter sphaeroides 2.4.1

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