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

Abstract

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.signaling network | transcription regulation | chronobiology

Circadian Rhythms in Cyanobacteria

“…Taken together, these reports suggest that RpaA and RpaB act cooperatively to regulate expression of circadian targets, perhaps by RpaA displacement of RpaB. Genes included as part of the RpaA regulon, including kaiBC (class 1) and purF (class 2), have also been shown to be negatively regulated by RpaB (87).…”

“…Moreover, overexpression of the RpaB receiver domain resulted in decreased RpaA phosphorylation levels, suggesting not only that RpaA and RpaB are competing for binding to targets but also that RpaB can act as a modulator of RpaA activity via regulation of RpaA phosphorylation status (87). These new findings highlight how cross talk occurs between a circadian (SasA-RpaA) pathway and an environmentally controlled pathway (NblS-RpaB) and how the pathways cooperate to generate rhythms of gene expression.…”

“…While the phosphorylation of RpaA oscillates in a circadian manner, oscillations in RpaB phosphorylation are observed only when cells are grown under diel conditions (12 h of light followed by 12 h of dark) and are not regulated by the clock (87). Moreover, overexpression of the RpaB receiver domain resulted in decreased RpaA phosphorylation levels, suggesting not only that RpaA and RpaB are competing for binding to targets but also that RpaB can act as a modulator of RpaA activity via regulation of RpaA phosphorylation status (87).…”

A Combined Computational and Genetic Approach Uncovers Network Interactions of the Cyanobacterial Circadian Clock

“…Cross talk between the response regulator RpaB (regulator of phycobilisome association B) and RpaA demonstrated integration between the SasA-RpaA and environmentally sensitive NblS (nonbleaching sensor)-RpaB TCS (13). However, cross talk between other TCS and the SasA-RpaA circadian TCS remained unexplored, due in part to the complexity of the network and the likelihood that signal transfer pathways are redundant.…”

Evolution of the circadian clock system in cyanobacteria: a genomic perspective

“…Циркадная система очень важна для обеспечения адаптационной и экологической пластичности цианобактерий, поскольку она контролирует основные физиоло-гические процессы, такие как фотосинтез, фиксация азота и клеточное деление (Johnson, Golden, 1999). Молекулярный механизм циркадных ритмов цианобактерий был тщательно изучен в последние два десятилетия (Hosokawa et al, 2013;Espinosa et al, 2015), однако о том, как этот механизм развивался и превратился в высокоэффективную и надежную циркадную систему, известно пока сравнительно немного.…”