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Interaction of two photoreceptors in the regulation of bacterial photosynthesis genes.

Metz S, Haberzettl K, Frühwirth S, Teich K, Hasewinkel C, Klug G - Nucleic Acids Res. (2012)

Bottom Line: Here we show that CryB interacts with the C-terminal domain of AppA and modulates the binding of AppA to the transcriptional repressor PpsR in a light-dependent manner.Consequently, binding of the transcription factor PpsR to its DNA target is affected by CryB.These results elucidate for the first time how a bacterial cryptochrome affects gene expression.

View Article: PubMed Central - PubMed

Affiliation: Institut für Mikrobiologie und Molekularbiologie, Universität Giessen, Heinrich-Buff-Ring 26-32, D-35392 Giessen, Germany.

ABSTRACT
The expression of photosynthesis genes in the facultatively photosynthetic bacterium Rhodobacter sphaeroides is controlled by the oxygen tension and by light quantity. Two photoreceptor proteins, AppA and CryB, have been identified in the past, which are involved in this regulation. AppA senses light by its N-terminal BLUF domain, its C-terminal part binds heme and is redox-responsive. Through its interaction to the transcriptional repressor PpsR the AppA photoreceptor controls expression of photosynthesis genes. The cryptochrome-like protein CryB was shown to affect regulation of photosynthesis genes, but the underlying signal chain remained unknown. Here we show that CryB interacts with the C-terminal domain of AppA and modulates the binding of AppA to the transcriptional repressor PpsR in a light-dependent manner. Consequently, binding of the transcription factor PpsR to its DNA target is affected by CryB. In agreement with this, all genes of the PpsR regulon showed altered expression levels in a CryB deletion strain after blue-light illumination. These results elucidate for the first time how a bacterial cryptochrome affects gene expression.

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Simplified model of AppA/PpsR dependent gene regulation. Under high oxygen (>4 mg l−1 dissolved O2) AppA (grey rectangle) is unable to bind PpsR (black circle) due to its oxidized heme and the free PpsR repressor inhibits photosynthesis gene expression. With decreasing oxygen levels AppA binds to PpsR thus photosynthesis gene expression is restored. At intermediate oxygen levels, however, illumination results in release of PpsR from AppA and consequently repression of photosynthesis genes (modified from 9). The arrows indicate transcription of photosynthesis genes.
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gks243-F1: Simplified model of AppA/PpsR dependent gene regulation. Under high oxygen (>4 mg l−1 dissolved O2) AppA (grey rectangle) is unable to bind PpsR (black circle) due to its oxidized heme and the free PpsR repressor inhibits photosynthesis gene expression. With decreasing oxygen levels AppA binds to PpsR thus photosynthesis gene expression is restored. At intermediate oxygen levels, however, illumination results in release of PpsR from AppA and consequently repression of photosynthesis genes (modified from 9). The arrows indicate transcription of photosynthesis genes.

Mentions: Rhodobacter sphaeroides harbors a set of different photoreceptors including two phytochromes, a LOV domain protein, three BLUF (Blue Light sensing Using FAD) domain proteins and a cryptochrome. Both phytochromes are composed of the PAS–GAF–PHY photosensory module, typically present in phytochromes, but linked to GGDEF–EAL output modules. One of the phytochromes, BphG1, was shown to be involved in the turn-over of c-di-GMP (6). The short LOV domain protein of R. sphaeroides lacks an output module and undergoes a photocycle but its biological function remains to be elucidated (7). Similarly, two of the BLUF domain proteins of R. sphaeroides lack an output domain (8) and their biological function is not known. The BLUF domain was first discovered in the AppA protein of R. sphaeroides (4,8,9), which was intensively studied in regard to its biological function, the mechanisms of signal transduction and its photocycle. The AppA protein was initially identified as a redox regulator of photosynthesis genes, which functions as antagonist of the PpsR protein (10,11). PpsR represses photosynthesis genes at high oxygen tension by binding to target promoters (11). Binding to PpsR is mediated by the C-terminal part of AppA (12), which was shown to bind heme (13,14). The novel type of heme-binding domain was named SCHIC (Sensor Containing Heme Instead of Cobalamin) domain (14). AppA also functions as photoreceptor through its BLUF domain, which interferes with PpsR binding at intermediate oxygen concentrations in response to blue light (4,9,12,13). Figure 1 shows a simplified schematic model for photosynthesis gene regulation by AppA/PpsR. Recently we demonstrated the involvement of the cryptochrome CryB in the regulation of photosynthesis genes in R. sphaeroides (15). The promoter of cryB is recognized by the RpoE-dependent alternative sigma factor RpoHII, both sigma factors have a major role in the response of R. sphaeroides to photooxidative stress (16–19).Figure 1.


Interaction of two photoreceptors in the regulation of bacterial photosynthesis genes.

Metz S, Haberzettl K, Frühwirth S, Teich K, Hasewinkel C, Klug G - Nucleic Acids Res. (2012)

Simplified model of AppA/PpsR dependent gene regulation. Under high oxygen (>4 mg l−1 dissolved O2) AppA (grey rectangle) is unable to bind PpsR (black circle) due to its oxidized heme and the free PpsR repressor inhibits photosynthesis gene expression. With decreasing oxygen levels AppA binds to PpsR thus photosynthesis gene expression is restored. At intermediate oxygen levels, however, illumination results in release of PpsR from AppA and consequently repression of photosynthesis genes (modified from 9). The arrows indicate transcription of photosynthesis genes.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3401432&req=5

gks243-F1: Simplified model of AppA/PpsR dependent gene regulation. Under high oxygen (>4 mg l−1 dissolved O2) AppA (grey rectangle) is unable to bind PpsR (black circle) due to its oxidized heme and the free PpsR repressor inhibits photosynthesis gene expression. With decreasing oxygen levels AppA binds to PpsR thus photosynthesis gene expression is restored. At intermediate oxygen levels, however, illumination results in release of PpsR from AppA and consequently repression of photosynthesis genes (modified from 9). The arrows indicate transcription of photosynthesis genes.
Mentions: Rhodobacter sphaeroides harbors a set of different photoreceptors including two phytochromes, a LOV domain protein, three BLUF (Blue Light sensing Using FAD) domain proteins and a cryptochrome. Both phytochromes are composed of the PAS–GAF–PHY photosensory module, typically present in phytochromes, but linked to GGDEF–EAL output modules. One of the phytochromes, BphG1, was shown to be involved in the turn-over of c-di-GMP (6). The short LOV domain protein of R. sphaeroides lacks an output module and undergoes a photocycle but its biological function remains to be elucidated (7). Similarly, two of the BLUF domain proteins of R. sphaeroides lack an output domain (8) and their biological function is not known. The BLUF domain was first discovered in the AppA protein of R. sphaeroides (4,8,9), which was intensively studied in regard to its biological function, the mechanisms of signal transduction and its photocycle. The AppA protein was initially identified as a redox regulator of photosynthesis genes, which functions as antagonist of the PpsR protein (10,11). PpsR represses photosynthesis genes at high oxygen tension by binding to target promoters (11). Binding to PpsR is mediated by the C-terminal part of AppA (12), which was shown to bind heme (13,14). The novel type of heme-binding domain was named SCHIC (Sensor Containing Heme Instead of Cobalamin) domain (14). AppA also functions as photoreceptor through its BLUF domain, which interferes with PpsR binding at intermediate oxygen concentrations in response to blue light (4,9,12,13). Figure 1 shows a simplified schematic model for photosynthesis gene regulation by AppA/PpsR. Recently we demonstrated the involvement of the cryptochrome CryB in the regulation of photosynthesis genes in R. sphaeroides (15). The promoter of cryB is recognized by the RpoE-dependent alternative sigma factor RpoHII, both sigma factors have a major role in the response of R. sphaeroides to photooxidative stress (16–19).Figure 1.

Bottom Line: Here we show that CryB interacts with the C-terminal domain of AppA and modulates the binding of AppA to the transcriptional repressor PpsR in a light-dependent manner.Consequently, binding of the transcription factor PpsR to its DNA target is affected by CryB.These results elucidate for the first time how a bacterial cryptochrome affects gene expression.

View Article: PubMed Central - PubMed

Affiliation: Institut für Mikrobiologie und Molekularbiologie, Universität Giessen, Heinrich-Buff-Ring 26-32, D-35392 Giessen, Germany.

ABSTRACT
The expression of photosynthesis genes in the facultatively photosynthetic bacterium Rhodobacter sphaeroides is controlled by the oxygen tension and by light quantity. Two photoreceptor proteins, AppA and CryB, have been identified in the past, which are involved in this regulation. AppA senses light by its N-terminal BLUF domain, its C-terminal part binds heme and is redox-responsive. Through its interaction to the transcriptional repressor PpsR the AppA photoreceptor controls expression of photosynthesis genes. The cryptochrome-like protein CryB was shown to affect regulation of photosynthesis genes, but the underlying signal chain remained unknown. Here we show that CryB interacts with the C-terminal domain of AppA and modulates the binding of AppA to the transcriptional repressor PpsR in a light-dependent manner. Consequently, binding of the transcription factor PpsR to its DNA target is affected by CryB. In agreement with this, all genes of the PpsR regulon showed altered expression levels in a CryB deletion strain after blue-light illumination. These results elucidate for the first time how a bacterial cryptochrome affects gene expression.

Show MeSH
Related in: MedlinePlus