The AppA and PpsR Proteins from
            <i>Rhodobacter sphaeroides</i>
            Can Establish a Redox-Dependent Signal Chain but Fail To Transmit Blue-Light Signals in Other Bacteria

Jäger, Andreas; Braatsch, Stephan; Haberzettl, Kerstin; Metz, Sebastian; Osterloh, Lisa; Han, Yuchen; Klug, Gabriele

doi:10.1128/jb.01699-06

Cited by 17 publications

(16 citation statements)

References 52 publications

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“…Interestingly, after illumination with light quantities as high as 20 μmol m −2 s −1 the puc expression increases around 50% in both mutants. As we could show before (8,13), light‐dependent PrrB/PrrA‐mediated regulation of the expression of the photosynthesis genes only sets in after illumination with high‐light quantities. PrrB phosphorylation (through autokinase activity) is regulated in an indirect manner via the electron flow through the respiratory chain (15,41,42).…”

Section: Discussionmentioning

confidence: 52%

In Vivo Effects on Photosynthesis Gene Expression of Base Pair Exchanges in the Gene Encoding the Light‐responsive BLUF Domain of AppA in Rhodobacter Sphaeroides

Metz

Hendriks

Jäger

et al. 2010

Photochem & Photobiology

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The Rhodobacter sphaeroides protein AppA has the unique quality of sensing and transmitting light and redox signals. By acting as antirepressor to the PpsR protein, it acts as a major regulator in photosynthesis gene expression. In this study, we show that by introducing amino acid exchanges into the AppA protein, the in vivo activity as an antirepressor can be greatly altered. The tryptophan 104 to phenylalanine (W104F) base exchange greatly diminished blue-light sensitivity of the BLUF domain. From the obtained in vivo data, the difference in thermal recovery rate of the signaling state of the BLUF domain between the wild type and mutated protein was calculated, predicting an about 10-fold faster recovery in the mutant, which is consistent with in vitro data. Introduction of a tyrosine 21 to phenylalanine (Y21F) or to cysteine (Y21C) mutation led to a complete loss of AppA antirepressor activity, while additionally leading to an increase of photosynthesis gene expression after illumination with high blue-light quantities. Interestingly, this effect is not visible in a W104F/Y21F double mutant that again shows a wild-type-like behavior of the BLUF domain after blue-light illumination, thus restoring the activity of AppA.

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Section: Discussionmentioning

confidence: 52%

In Vivo Effects on Photosynthesis Gene Expression of Base Pair Exchanges in the Gene Encoding the Light‐responsive BLUF Domain of AppA in Rhodobacter Sphaeroides

Metz

Hendriks

Jäger

et al. 2010

Photochem & Photobiology

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“…The expression of appA is dependent on PrrA (38). Such an interplay between the AppA-PpsR and PrrBA systems is likely to be important for global gene regulation responding to oxygen and light, as suggested previously (32,34). The expression level of prrB decreased slightly over time after the shift and then increased over time, but the change was not significant, indicating that prrA and prrB are regulated differently.…”

Section: Discussionmentioning

confidence: 76%

Transcriptome Dynamics during the Transition from Anaerobic Photosynthesis to Aerobic Respiration in Rhodobacter sphaeroides 2.4.1

2008

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Rhodobacter sphaeroides 2.4.1 is a facultative photosynthetic anaerobe that grows by anoxygenic photosynthesis under anaerobic-light conditions. Changes in energy generation pathways under photosynthetic and aerobic respiratory conditions are primarily controlled by oxygen tensions. In this study, we performed time series microarray analyses to investigate transcriptome dynamics during the transition from anaerobic photosynthesis to aerobic respiration. Major changes in gene expression profiles occurred in the initial 15 min after the shift from anaerobic-light to aerobic-dark conditions, with changes continuing to occur up to 4 hours postshift. Those genes whose expression levels changed significantly during the time series were grouped into three major classes by clustering analysis. Class I contained genes, such as that for the aa 3 cytochrome oxidase, whose expression levels increased after the shift. Class II contained genes, such as those for the photosynthetic apparatus and Calvin cycle enzymes, whose expression levels decreased after the shift. Class III contained genes whose expression levels temporarily increased during the time series. Many genes for metabolism and transport of carbohydrates or lipids were significantly induced early during the transition, suggesting that those endogenous compounds were initially utilized as carbon sources. Oxidation of those compounds might also be required for maintenance of redox homeostasis after exposure to oxygen. Genes for the repair of protein and sulfur groups and uptake of ferric iron were temporarily upregulated soon after the shift, suggesting they were involved in a response to oxidative stress. The flagellar-biosynthesis genes were expressed in a hierarchical manner at 15 to 60 min after the shift. Numerous transporters were induced at various time points, suggesting that the cellular composition went through significant changes during the transition from anaerobic photosynthesis to aerobic respiration. Analyses of these data make it clear that numerous regulatory activities come into play during the transition from one homeostatic state to another.

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“…Neglecting the importance of maintaining a wild-type AppA to PpsR ratio, e.g., using heterologous expression of AppA and PpsR from plasmid-borne systems, may easily compromise conclusions regarding the ability of the AppA-PpsR system to respond to environmental stimuli (20). The fact uncovered here that in the prrA null mutant, the AppA/PpsR ratio is greatly increased offers a simple explanation for the observation that light does not affect PS gene expression in this mutant, as observed by Jäger et al (20), who presented a different interpretation.…”

Section: Discussionmentioning

confidence: 99%

“…Genetic inactivation of appA results in phototrophically impaired cells that fail to derepress PS genes in response to oxygen deprivation, which is similar to PpsR overexpression (17). AppA is a unique dual sensor of oxygen and light (3,20,29), sensing oxygen via its SCHIC (sensor containing heme instead of cobalamin) domain (31) and light via the BLUF (sensor of blue light using flavin adenine dinucleotide) domain (13). Both oxygen and light are anticipated to disrupt the AppA-PpsR interaction and thus result in increased DNA binding by PpsR (29,31).…”

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confidence: 99%

Hierarchical Regulation of Photosynthesis Gene Expression by the Oxygen-Responsive PrrBA and AppA-PpsR Systems of Rhodobacter sphaeroides

et al. 2008

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In the facultatively phototrophic proteobacterium Rhodobacter sphaeroides, formation of the photosynthetic apparatus is oxygen dependent. When oxygen tension decreases, the response regulator PrrA of the global two-component PrrBA system is believed to directly activate transcription of the puf, puh, and puc operons, encoding structural proteins of the photosynthetic complexes, and to indirectly upregulate the photopigment biosynthesis genes bch and crt. Decreased oxygen also results in inactivation of the photosynthesis-specific repressor PpsR, bringing about derepression of the puc, bch, and crt operons. We uncovered a hierarchical relationship between these two regulatory systems, earlier thought to function independently. We also more accurately assessed the spectrum of gene targets of the PrrBA system. First, expression of the appA gene, encoding the PpsR antirepressor, is PrrA dependent, which establishes one level of hierarchical dominance of the PrrBA system over AppA-PpsR. Second, restoration of the appA transcript to the wild-type level is insufficient for rescuing phototrophic growth impairment of the prrA mutant, whereas inactivation of ppsR is sufficient. This suggests that in addition to controlling appA transcription, PrrA affects the activity of the AppA-PpsR system via an as yet unidentified mechanism(s). Third, PrrA directly activates several bch and crt genes, traditionally considered to be the PpsR targets. Therefore, in R. sphaeroides, the global PrrBA system regulates photosynthesis gene expression (i) by rigorous control over the photosynthesis-specific AppA-PpsR regulatory system and (ii) by extensive direct transcription activation of genes encoding structural proteins of photosynthetic complexes as well as genes encoding photopigment biosynthesis enzymes.In the facultatively phototrophic alphaproteobacterium Rhodobacter sphaeroides, photosynthesis (PS) operates under anoxic conditions. A decrease in oxygen tension triggers significant upregulation of PS gene transcription (35,38). The photosynthetic apparatus is comprised of the reaction center, encoded by the puh and puf operons, and two light-harvesting complexes, encoded by the puf and puc operons. Enzymes involved in the biosynthesis of photosynthetic pigments, i.e., bacteriochlorophyll a and carotenoids, are encoded by the bch and crt genes, respectively. Most PS-specific genes are located in the R. sphaeroides PS gene cluster, whereas the puc operons are located separately (4, 49). Three major regulatory systems control oxygen-dependent transcription of PS genes. One of these is composed of the antirepressor AppA (15, 17) and the repressor PpsR (7, 36) and is primarily responsible for the regulation of PS genes (30). Two other systems are global regulatory systems, i.e., the redox-responsive two-component system PrrBA (2, 47) and the anaerobic activator FnrL (48).

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The AppA and PpsR Proteins from Rhodobacter sphaeroides Can Establish a Redox-Dependent Signal Chain but Fail To Transmit Blue-Light Signals in Other Bacteria

Cited by 17 publications

References 52 publications

In Vivo Effects on Photosynthesis Gene Expression of Base Pair Exchanges in the Gene Encoding the Light‐responsive BLUF Domain of AppA in Rhodobacter Sphaeroides

In Vivo Effects on Photosynthesis Gene Expression of Base Pair Exchanges in the Gene Encoding the Light‐responsive BLUF Domain of AppA in Rhodobacter Sphaeroides

Transcriptome Dynamics during the Transition from Anaerobic Photosynthesis to Aerobic Respiration in Rhodobacter sphaeroides 2.4.1

Hierarchical Regulation of Photosynthesis Gene Expression by the Oxygen-Responsive PrrBA and AppA-PpsR Systems of Rhodobacter sphaeroides

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