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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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Physiological and genomic analysis of MppG regulation.(A) Growth of WT, ΔMppG and ΔMppG+pIND5-mppG with increasing IPTG concentrations under photosynthetic conditions. (B) Amounts of bacteriochlorophyll produced in WT, ΔMppG and ΔMppG+pIND5-mppG. (C) Expression profiles of genes differentially expressed in response to the loss of MppG (ΔMppG) or over-expression of MppG (ΔMppG+pIND5-mppG) strains. Genes differentially expressed in the ΔMppG only are indicated with an asterisk (*). (D) ChIP-seq binding profile of MppG at the mppG, bchF and appA promoters.
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pgen-1004837-g004: Physiological and genomic analysis of MppG regulation.(A) Growth of WT, ΔMppG and ΔMppG+pIND5-mppG with increasing IPTG concentrations under photosynthetic conditions. (B) Amounts of bacteriochlorophyll produced in WT, ΔMppG and ΔMppG+pIND5-mppG. (C) Expression profiles of genes differentially expressed in response to the loss of MppG (ΔMppG) or over-expression of MppG (ΔMppG+pIND5-mppG) strains. Genes differentially expressed in the ΔMppG only are indicated with an asterisk (*). (D) ChIP-seq binding profile of MppG at the mppG, bchF and appA promoters.

Mentions: To assess the physiological role of MppG, we constructed and analyzed the properties of a mppG deletion mutant (ΔMppG). Furthermore, ΔMppG was complemented with mppG from an IPTG-inducible plasmid (ΔMppG+pIND5-mppG). The WT and ΔMppG strains both exhibited similar growth rates (Fig. 4A), while the complemented strains also grew at similar rates up to 10 µM IPTG, beyond which photosynthetic growth, but not aerobic growth, was severely negatively impacted (Fig. 4A, S5A Figure). This suggested a role for MppG in one or more aspects of photosynthesis.


Global analysis of photosynthesis transcriptional regulatory networks.

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

Physiological and genomic analysis of MppG regulation.(A) Growth of WT, ΔMppG and ΔMppG+pIND5-mppG with increasing IPTG concentrations under photosynthetic conditions. (B) Amounts of bacteriochlorophyll produced in WT, ΔMppG and ΔMppG+pIND5-mppG. (C) Expression profiles of genes differentially expressed in response to the loss of MppG (ΔMppG) or over-expression of MppG (ΔMppG+pIND5-mppG) strains. Genes differentially expressed in the ΔMppG only are indicated with an asterisk (*). (D) ChIP-seq binding profile of MppG at the mppG, bchF and appA promoters.
© Copyright Policy
Related In: Results  -  Collection

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

pgen-1004837-g004: Physiological and genomic analysis of MppG regulation.(A) Growth of WT, ΔMppG and ΔMppG+pIND5-mppG with increasing IPTG concentrations under photosynthetic conditions. (B) Amounts of bacteriochlorophyll produced in WT, ΔMppG and ΔMppG+pIND5-mppG. (C) Expression profiles of genes differentially expressed in response to the loss of MppG (ΔMppG) or over-expression of MppG (ΔMppG+pIND5-mppG) strains. Genes differentially expressed in the ΔMppG only are indicated with an asterisk (*). (D) ChIP-seq binding profile of MppG at the mppG, bchF and appA promoters.
Mentions: To assess the physiological role of MppG, we constructed and analyzed the properties of a mppG deletion mutant (ΔMppG). Furthermore, ΔMppG was complemented with mppG from an IPTG-inducible plasmid (ΔMppG+pIND5-mppG). The WT and ΔMppG strains both exhibited similar growth rates (Fig. 4A), while the complemented strains also grew at similar rates up to 10 µM IPTG, beyond which photosynthetic growth, but not aerobic growth, was severely negatively impacted (Fig. 4A, S5A Figure). This suggested a role for MppG in one or more aspects of photosynthesis.

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