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Global analysis of photosynthesis transcriptional regulatory networks.

Imam S, Noguera DR, Donohue TJ - PLoS Genet. (2014)

Bottom Line: PrrA regulates ∼34 operons encoding mainly photosynthesis and electron transport functions, while CrpK, a previously uncharacterized Crp-family protein, regulates genes involved in photosynthesis and maintenance of iron homeostasis.Furthermore, CrpK and FnrL share similar DNA binding determinants, possibly explaining our observation of the ability of CrpK to partially compensate for the growth defects of a ΔFnrL mutant.We show that the Rrf2 family protein, MppG, plays an important role in photopigment biosynthesis, as part of an incoherent feed-forward loop with PrrA.

View Article: PubMed Central - PubMed

Affiliation: Program in Cellular and Molecular Biology, University of Wisconsin - Madison, Madison, Wisconsin, United States of America; Department of Bacteriology, University of Wisconsin - Madison, Wisconsin Energy Institute, Madison, Wisconsin, United States of America; DOE Great Lakes Bioenergy Research Center, University of Wisconsin - Madison, Madison, Wisconsin, United States of America.

ABSTRACT
Photosynthesis is a crucial biological process that depends on the interplay of many components. This work analyzed the gene targets for 4 transcription factors: FnrL, PrrA, CrpK and MppG (RSP_2888), which are known or predicted to control photosynthesis in Rhodobacter sphaeroides. Chromatin immunoprecipitation followed by high-throughput sequencing (ChIP-seq) identified 52 operons under direct control of FnrL, illustrating its regulatory role in photosynthesis, iron homeostasis, nitrogen metabolism and regulation of sRNA synthesis. Using global gene expression analysis combined with ChIP-seq, we mapped the regulons of PrrA, CrpK and MppG. PrrA regulates ∼34 operons encoding mainly photosynthesis and electron transport functions, while CrpK, a previously uncharacterized Crp-family protein, regulates genes involved in photosynthesis and maintenance of iron homeostasis. Furthermore, CrpK and FnrL share similar DNA binding determinants, possibly explaining our observation of the ability of CrpK to partially compensate for the growth defects of a ΔFnrL mutant. We show that the Rrf2 family protein, MppG, plays an important role in photopigment biosynthesis, as part of an incoherent feed-forward loop with PrrA. Our results reveal a previously unrealized, high degree of combinatorial regulation of photosynthetic genes and significant cross-talk between their transcriptional regulators, while illustrating previously unidentified links between photosynthesis and the maintenance of iron homeostasis.

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Related in: MedlinePlus

Photosynthetic gene regulatory network.An overview of the R. sphaeroides photosynthetic gene regulatory network, showing known transcriptional regulators and their photosynthesis-related direct target genes. Grey nodes and edges indicate inactive genes and interactions. The top panel (Aerobic) depicts the regulatory control mechanism of photosynthesis genes under aerobic respiratory conditions in the dark. Under this condition the anti-repressor protein AppA, which has been proposed to be sensitive to oxygen and light, is inactivated. This allows its cognate repressor, PpsR, to downregulate the expression of several photosynthesis related genes including the gene encoding the transcription factor PrrA. This results in the inhibition of photosynthesis by preventing the production of photopigments. Molecular oxygen also inhibits the activity of the transcription factors FnrL and potentially MppG (the uncertain nature of effect is indicated by a dashed edge). Under anoxygenic photosynthetic conditions (bottom panel), AppA becomes active and directly interacts with PpsR(depicted by the white circle above ppsR) inhibiting its activity. In addition, the activators of photosynthesis, PrrA, FnrL and CrpK, become active under these conditions and induce the expression of photosynthetic genes. Under these conditions, the photopigment gene repressors MppG and the sRNA PcrZ are also active, negatively modulating photopigment gene expression. The expression of appA and the activity of its gene product is dependent on regulatory inputs from PrrA, MppG, PcrZ and oxygen. Biotapestry was used for network visualization [91].
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pgen-1004837-g005: Photosynthetic gene regulatory network.An overview of the R. sphaeroides photosynthetic gene regulatory network, showing known transcriptional regulators and their photosynthesis-related direct target genes. Grey nodes and edges indicate inactive genes and interactions. The top panel (Aerobic) depicts the regulatory control mechanism of photosynthesis genes under aerobic respiratory conditions in the dark. Under this condition the anti-repressor protein AppA, which has been proposed to be sensitive to oxygen and light, is inactivated. This allows its cognate repressor, PpsR, to downregulate the expression of several photosynthesis related genes including the gene encoding the transcription factor PrrA. This results in the inhibition of photosynthesis by preventing the production of photopigments. Molecular oxygen also inhibits the activity of the transcription factors FnrL and potentially MppG (the uncertain nature of effect is indicated by a dashed edge). Under anoxygenic photosynthetic conditions (bottom panel), AppA becomes active and directly interacts with PpsR(depicted by the white circle above ppsR) inhibiting its activity. In addition, the activators of photosynthesis, PrrA, FnrL and CrpK, become active under these conditions and induce the expression of photosynthetic genes. Under these conditions, the photopigment gene repressors MppG and the sRNA PcrZ are also active, negatively modulating photopigment gene expression. The expression of appA and the activity of its gene product is dependent on regulatory inputs from PrrA, MppG, PcrZ and oxygen. Biotapestry was used for network visualization [91].

Mentions: Our analyses have provided new information on the TRN controlling bacterial photosynthesis in R. sphaeroides. We confirmed the predicted involvement of two previously uncharacterized TFs, CrpK and MppG, in the regulation of photosynthesis related genes. We also extended the regulons of PrrA and FnrL, which had previously been implicated in regulation of the photosynthetic lifestyle of R. sphaeroides. Our analyses, combined with previous analyses of PrrA, FnrL and PpsR, illustrate the depth, complexity and robustness of the photosynthetic TRN. They also highlight significant combinatorial regulation of target genes, cross-talk between regulators and redundancy in the use of TFs within this network (Fig. 5), features that are likely to be broadly seen in the TRN of other biological systems.


Global analysis of photosynthesis transcriptional regulatory networks.

Imam S, Noguera DR, Donohue TJ - PLoS Genet. (2014)

Photosynthetic gene regulatory network.An overview of the R. sphaeroides photosynthetic gene regulatory network, showing known transcriptional regulators and their photosynthesis-related direct target genes. Grey nodes and edges indicate inactive genes and interactions. The top panel (Aerobic) depicts the regulatory control mechanism of photosynthesis genes under aerobic respiratory conditions in the dark. Under this condition the anti-repressor protein AppA, which has been proposed to be sensitive to oxygen and light, is inactivated. This allows its cognate repressor, PpsR, to downregulate the expression of several photosynthesis related genes including the gene encoding the transcription factor PrrA. This results in the inhibition of photosynthesis by preventing the production of photopigments. Molecular oxygen also inhibits the activity of the transcription factors FnrL and potentially MppG (the uncertain nature of effect is indicated by a dashed edge). Under anoxygenic photosynthetic conditions (bottom panel), AppA becomes active and directly interacts with PpsR(depicted by the white circle above ppsR) inhibiting its activity. In addition, the activators of photosynthesis, PrrA, FnrL and CrpK, become active under these conditions and induce the expression of photosynthetic genes. Under these conditions, the photopigment gene repressors MppG and the sRNA PcrZ are also active, negatively modulating photopigment gene expression. The expression of appA and the activity of its gene product is dependent on regulatory inputs from PrrA, MppG, PcrZ and oxygen. Biotapestry was used for network visualization [91].
© Copyright Policy
Related In: Results  -  Collection

License
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getmorefigures.php?uid=PMC4263372&req=5

pgen-1004837-g005: Photosynthetic gene regulatory network.An overview of the R. sphaeroides photosynthetic gene regulatory network, showing known transcriptional regulators and their photosynthesis-related direct target genes. Grey nodes and edges indicate inactive genes and interactions. The top panel (Aerobic) depicts the regulatory control mechanism of photosynthesis genes under aerobic respiratory conditions in the dark. Under this condition the anti-repressor protein AppA, which has been proposed to be sensitive to oxygen and light, is inactivated. This allows its cognate repressor, PpsR, to downregulate the expression of several photosynthesis related genes including the gene encoding the transcription factor PrrA. This results in the inhibition of photosynthesis by preventing the production of photopigments. Molecular oxygen also inhibits the activity of the transcription factors FnrL and potentially MppG (the uncertain nature of effect is indicated by a dashed edge). Under anoxygenic photosynthetic conditions (bottom panel), AppA becomes active and directly interacts with PpsR(depicted by the white circle above ppsR) inhibiting its activity. In addition, the activators of photosynthesis, PrrA, FnrL and CrpK, become active under these conditions and induce the expression of photosynthetic genes. Under these conditions, the photopigment gene repressors MppG and the sRNA PcrZ are also active, negatively modulating photopigment gene expression. The expression of appA and the activity of its gene product is dependent on regulatory inputs from PrrA, MppG, PcrZ and oxygen. Biotapestry was used for network visualization [91].
Mentions: Our analyses have provided new information on the TRN controlling bacterial photosynthesis in R. sphaeroides. We confirmed the predicted involvement of two previously uncharacterized TFs, CrpK and MppG, in the regulation of photosynthesis related genes. We also extended the regulons of PrrA and FnrL, which had previously been implicated in regulation of the photosynthetic lifestyle of R. sphaeroides. Our analyses, combined with previous analyses of PrrA, FnrL and PpsR, illustrate the depth, complexity and robustness of the photosynthetic TRN. They also highlight significant combinatorial regulation of target genes, cross-talk between regulators and redundancy in the use of TFs within this network (Fig. 5), features that are likely to be broadly seen in the TRN of other biological systems.

Bottom Line: PrrA regulates ∼34 operons encoding mainly photosynthesis and electron transport functions, while CrpK, a previously uncharacterized Crp-family protein, regulates genes involved in photosynthesis and maintenance of iron homeostasis.Furthermore, CrpK and FnrL share similar DNA binding determinants, possibly explaining our observation of the ability of CrpK to partially compensate for the growth defects of a ΔFnrL mutant.We show that the Rrf2 family protein, MppG, plays an important role in photopigment biosynthesis, as part of an incoherent feed-forward loop with PrrA.

View Article: PubMed Central - PubMed

Affiliation: Program in Cellular and Molecular Biology, University of Wisconsin - Madison, Madison, Wisconsin, United States of America; Department of Bacteriology, University of Wisconsin - Madison, Wisconsin Energy Institute, Madison, Wisconsin, United States of America; DOE Great Lakes Bioenergy Research Center, University of Wisconsin - Madison, Madison, Wisconsin, United States of America.

ABSTRACT
Photosynthesis is a crucial biological process that depends on the interplay of many components. This work analyzed the gene targets for 4 transcription factors: FnrL, PrrA, CrpK and MppG (RSP_2888), which are known or predicted to control photosynthesis in Rhodobacter sphaeroides. Chromatin immunoprecipitation followed by high-throughput sequencing (ChIP-seq) identified 52 operons under direct control of FnrL, illustrating its regulatory role in photosynthesis, iron homeostasis, nitrogen metabolism and regulation of sRNA synthesis. Using global gene expression analysis combined with ChIP-seq, we mapped the regulons of PrrA, CrpK and MppG. PrrA regulates ∼34 operons encoding mainly photosynthesis and electron transport functions, while CrpK, a previously uncharacterized Crp-family protein, regulates genes involved in photosynthesis and maintenance of iron homeostasis. Furthermore, CrpK and FnrL share similar DNA binding determinants, possibly explaining our observation of the ability of CrpK to partially compensate for the growth defects of a ΔFnrL mutant. We show that the Rrf2 family protein, MppG, plays an important role in photopigment biosynthesis, as part of an incoherent feed-forward loop with PrrA. Our results reveal a previously unrealized, high degree of combinatorial regulation of photosynthetic genes and significant cross-talk between their transcriptional regulators, while illustrating previously unidentified links between photosynthesis and the maintenance of iron homeostasis.

Show MeSH
Related in: MedlinePlus