Global analysis of photosynthesis transcriptional regulatory networks

• Published in: PLoS genetics 2014-12, Vol.10 (12), p.e1004837-e1004837
• Main Authors: Imam, Saheed, Noguera, Daniel R, Donohue, Timothy J
• Format: Article
• Language: English
• Subjects: Alternative energy sources; Bacterial Proteins - genetics; Bacterial Proteins - metabolism; BASIC BIOLOGICAL SCIENCES; binding analysis; Binding sites; Biology and life sciences; Chromatin Immunoprecipitation; DNA-Binding Proteins; Electron Transport; Gene expression; Gene Expression Regulation, Bacterial; gene regulation; Gene Regulatory Networks; Genetic aspects; Genetic research; Genetic transcription; Genomics; Homeostasis; Lifestyles; Metabolism; Microbiological research; Operon; operons; Organisms; Photosynthesis; Photosynthesis - genetics; Proteins; Proteobacteria; regulator genes; Regulon; regulons; Respiration; Rhodobacter sphaeroides - genetics; Rhodobacter sphaeroides - growth & development; RNA, Messenger - genetics; RNA, Messenger - metabolism; Trans-Activators - genetics; Trans-Activators - metabolism; Transcription factors; transcriptional control
• ISSN: 1553-7404; 1553-7390; 1553-7404
• DOI: 10.1371/journal.pgen.1004837

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.