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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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Cellular processes regulated by photosynthesis global regulators.Overview of the different cellular processes coordinated by the TFs regulating photosynthesis in R. sphaeroides.
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pgen-1004837-g006: Cellular processes regulated by photosynthesis global regulators.Overview of the different cellular processes coordinated by the TFs regulating photosynthesis in R. sphaeroides.

Mentions: Bacteria and other cells use a myriad of TRNs to respond to different types of stimuli, with these TRNs varying in depth and complexity [46], [47]. While the regulation of some cellular processes can be largely controlled by a TRN involving just one TF (for instance, LexA regulation of DNA repair in some bacteria [48]), other cellular processes involve the coordinated activities of multiple globally and locally acting TFs (e.g., the regulation of amino acid metabolism by ArgR, Lrp and TrpR in E. coli[49]). Generally, cellular processes which result in significant physiological or morphological changes (such as sporulation in Bacillus [50]–[53]) or are central to cell survival (such as central metabolism [54] or chemotaxis [55]) require highly interconnected TRNs involving multiple TFs and sensory components. The TRN network controlling photosynthesis in R. sphaeroides is multi-faceted, involving the activities of at least 5 TFs (including 4 global regulators) and one sRNA (Figs. 5, 6).


Global analysis of photosynthesis transcriptional regulatory networks.

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

Cellular processes regulated by photosynthesis global regulators.Overview of the different cellular processes coordinated by the TFs regulating photosynthesis in R. sphaeroides.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4263372&req=5

pgen-1004837-g006: Cellular processes regulated by photosynthesis global regulators.Overview of the different cellular processes coordinated by the TFs regulating photosynthesis in R. sphaeroides.
Mentions: Bacteria and other cells use a myriad of TRNs to respond to different types of stimuli, with these TRNs varying in depth and complexity [46], [47]. While the regulation of some cellular processes can be largely controlled by a TRN involving just one TF (for instance, LexA regulation of DNA repair in some bacteria [48]), other cellular processes involve the coordinated activities of multiple globally and locally acting TFs (e.g., the regulation of amino acid metabolism by ArgR, Lrp and TrpR in E. coli[49]). Generally, cellular processes which result in significant physiological or morphological changes (such as sporulation in Bacillus [50]–[53]) or are central to cell survival (such as central metabolism [54] or chemotaxis [55]) require highly interconnected TRNs involving multiple TFs and sensory components. The TRN network controlling photosynthesis in R. sphaeroides is multi-faceted, involving the activities of at least 5 TFs (including 4 global regulators) and one sRNA (Figs. 5, 6).

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