Metabolic Compensation and Circadian Resilience in Prokaryotic Cyanobacteria

Abstract

For a biological oscillator to function as a circadian pacemaker that confers a fitness advantage, its timing functions must be stable in response to environmental and metabolic fluctuations. One such stability enhancer, temperature compensation, has long been a defining characteristic of these timekeepers. However, an accurate biological timekeeper must also resist changes in metabolism, and this review suggests that temperature compensation is actually a subset of a larger phenomenon, namely metabolic compensation, which maintains the frequency of circadian oscillators in response to a host of factors that impinge on metabolism and would otherwise destabilize these clocks. The circadian system of prokaryotic cyanobacteria is an illustrative model because it is composed of transcriptional and nontranscriptional oscillators that are coupled to promote resilience. Moreover, the cyanobacterial circadian program regulates gene activity and metabolic pathways, and it can be manipulated to improve the expression of bioproducts that have practical value.

Timing the day: what makes bacterial clocks tick?

“…Interestingly, changes in metabolism that depend on the light and dark cycle, in particular redox status and/or energy levels, can directly the cyanobacterial clockwork 28–31 . Metabolic feedback might even provide mechanisms to compensate for temperature and other changes to enable the clock to maintain accurate timekeeping 32 .…”

“…The dephosphorylation phase proceeds, at least partially, by regenerating ATP from CII-bound ADP and the phosphates that are bound to T432 and S431 (REFS 57,58). This remarkable phosphotransferase activity limits the overall consumption of ATP, which possibly preserves clock function when cellular ATP concentrations fluctuate; the cyanobacterial clock accurately tracks time during extended exposure to the dark, when cells are not able to produce ATP by photosynthesis 28,32,51,52,57 .…”

Diel Infection of Cyanobacteria by Cyanophages

“…The cyanobacterial circadian clock regulates many important cellular processes, including cell cycle, amino acid uptake, nitrogen fixation, photosynthesis, carbohydrate synthesis, and respiration (Golden et al, 1997). The molecular mechanism of cyanobacterial circadian clock has been reviewed extensively (Johnson and Egli, 2014;Cohen and Golden, 2015), and here we introduce its major components for reference. The circadian clock of S. elongatus PCC 7942 is composed of three proteins KaiA, KaiB, and KaiC (Ishiura et al, 1998).…”

“…Sequenced Prochlorococcus strains all encode kaiB and kaiC, but lack kaiA (Holtzendorff et al, 2008;Axmann et al, 2014), suggesting that their biological timing system is different from that of S. elongatus (Holtzendorff et al, 2008;Johnson and Egli, 2014). Indeed, synchronized S. elongatus cells are able to maintain periodic oscillations of cell cycle (Mori et al, 1996) and gene expression under continuous light (Liu et al, 1995), while Prochlorococcus lacks this ability (Holtzendorff et al, 2008).…”

Circadian Clocks: Unexpected Biochemical Cogs

“…The KaiABC in vitro oscillator constitutes a core post-translational oscillator (PTO) of the cyanobacterial circadian system, which couples transcriptional (TTFL) and non-transcriptional (PTO) oscillators to achieve resilience and robustness [6]. The PTO can be reconstituted in vitro by incubating together the three proteins and Mg 2+ -ATP [2].…”