Cross-talk and regulatory interactions between the essential response regulator RpaB and cyanobacterial circadian clock output

• Published in: Proceedings of the National Academy of Sciences - PNAS 2015-02, Vol.112 (7), p.2198-2203
• Main Authors: Espinosa, Javier, Boyd, Joseph S., Cantos, Raquel, Salinas, Paloma, Golden, Susan S., Contreras, Asuncion
• Format: Article
• Language: English
• Subjects: Bacterial Proteins - physiology; Biological Sciences; Circadian Rhythm; Circadian rhythms; Cyanobacteria; Cyanobacteria - genetics; Cyanobacteria - physiology; Gene expression; Genes, Bacterial; Genotype & phenotype; Phosphorylation; Synechococcus elongatus
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.1424632112

The response regulator RpaB (regulator of phycobilisome associated B), part of an essential two-component system conserved in cyanobacteria that responds to multiple environmental signals, has recently been implicated in the control of cell dimensions and of circadian rhythms of gene expression in the model cyanobacterium Synechococcus elongatus PCC 7942. However, little is known of the molecular mechanisms that underlie RpaB functions. In this study we show that the regulation of phenotypes by RpaB is intimately connected with the activity of RpaA (regulator of phycobilisome associated A), the master regulator of circadian transcription patterns. RpaB affects RpaA activity both through control of gene expression, a function requiring an intact effector domain, and via altering RpaA phosphorylation, a function mediated through the N-terminal receiver domain of RpaB. Thus, both phosphorylation cross-talk and coregulation of target genes play a role in the genetic interactions between the RpaA and RpaB pathways. In addition, RpaB∼P levels appear critical for survival under light:dark cycles, conditions in which RpaB phosphorylation is environmentally driven independent of the circadian clock. We propose that the complex regulatory interactions between the essential and environmentally sensitive NblS-RpaB system and the SasA-RpaA clock output system integrate relevant extra- and intracellular signals to the circadian clock. Significance In cyanobacteria, genome-wide transcriptional oscillations and cell division are under the control of the global response regulator RpaA. Here we show that regulator of phycobilisome-associated B (RpaB), a closely related response regulator that is essential in the model cyanobacterium Synechococcus elongatus PCC 7942, is involved in complex regulatory interactions with the RpaA signaling system. RpaB influences circadian timing and cell dimensions by modulating the RpaA∼P levels and by controlling a subset of the RpaA target genes. Our results suggest that regulatory interactions between RpaA and RpaB are required for transmission of updated time information to the level of gene expression, paving the way to uncover regulatory mechanisms involved in integration of temporal and environmental information.