No Promoter Left Behind: Global Circadian Gene Expression in Cyanobacteria

Abstract

Prokaryotic cyanobacteria express robust circadian (daily) rhythms under the control of a clock system that appears to be similar to those of eukaryotes in many ways. On the other hand, the KaiABC-based core cyanobacterial clockwork is clearly different from the transcriptiontranslation feedback loop model of eukaryotic clocks in that the cyanobacterial clock system regulates gene expression patterns globally, and specific clock gene promoters are not essential in mediating the circadian feedback loop. A novel model, the oscilloid model, proposes that the KaiABC oscillator ultimately mediates rhythmic changes in the status of the cyanobacterial chromosome, and these topological changes underlie the global rhythms of transcription. The authors suggest that this model represents one of several possible modes of regulating gene expression by circadian clocks, even those of eukaryotes. Keywords circadian; biological clock; kai; prokaryote; global gene expression; supercoiling Animals, plants, fungi, and cyanobacteria all display daily or circadian rhythms in their biochemistry, physiology, and/or behavior that are controlled by biological clocks (Dunlap et al., 2004). A variety of biological processes in various organisms are controlled by biological clocks such as gene expression, photosynthesis, sleeping/waking, and development, and this regulation is thought to help organisms adapt to the daily changes in light, temperature, and other factors in their environment. Circadian regulation of gene expression (i.e., the levels of specific proteins in cells) can be accomplished by clock control of transcription, mRNA stability, translation, and protein degradation. A particularly fascinating example of translational control by a circadian clock is that in the dinoflagellate alga, Gonyaulax (Rossini et al., 2003). However, we focus our discussion specifically on clock control of cyanobacterial gene expression at the level of transcription.In general, studies of circadian gene expression in eukaryotes have often used microarray analyses to show that a relatively small proportion of genes (~5%-15%) in eukaryotic genomes display rhythms in mRNA abundance. While microarray technology is well advanced, it should be noted that microarrays are not very sensitive to small changes of mRNA abundance, and moreover, they are not a good measure of rhythmic transcriptional activity for mRNAs that are either very unstable or very stable. Therefore, microarray results might not be reflective of transcriptional control in detail.

Circadian rhythms of superhelical status of DNA in cyanobacteria

“…Therefore, the plasmid topology rhythm is conditionally coupled to the core KaiABC circadian oscillator in a light-dependent manner (12). In DD, the core oscillator can continue to ''tick'' but is uncoupled from its ability to modulate changes in plasmid topology and other clock outputs as well, most significantly, the global rhythm of gene expression (24).…”

“…Although microarrays are informative, this technique is not sensitive to small changes in mRNA abundance and is not a quantitative measure of rhythmic transcriptional activity for mRNAs that are either very unstable or very stable. Because of these limitations of microarrays, the degree to which circadian clocks control promoter activity is likely to have been underestimated in eukaryotes (12,13). Because the promoter trap technique measures promoter activity, its application in S. elongatus may explain why pervasive clock control over gene expression has been found in cyanobacteria, but not in eukaryotic circadian systems.…”

Biological Rhythms Workshop IA: Molecular Basis of Rhythms Generation

“…The lowamplitude and bright (LabA) protein is proposed to act in a repression pathway to feed temporal information Output. The cyanobacterial circadian clock regulates global gene expression, such that every promoter tested drives expression of luciferase reporter genes in a 24-hour rhythm (for review, see Johnson 2004;Woelfle and Johnson 2006). This global control is likely the result of the Kai-dependent circadian rhythm in chromosome compaction that alters the availability of promoter regions to transcriptional machinery (Fig.…”

Global transcriptomic analysis ofCyanothece51142 reveals robust diurnal oscillation of central metabolic processes

“…During the past 15 years, numerous studies have shown that cyanobacteria, photosynthetic microbes, are the only prokaryotes known to have a circadian clock (6,7). Although components of the circadian clock have been identified and analyzed in detail in cyanobacteria (8)(9)(10), the interactions between the clock and cellular physiology and metabolism have not been well elucidated.…”