Circadian rhythms of superhelical status of DNA in cyanobacteria

Woelfle, Mark A.; Xu, Yao; Qin, Ximing; Johnson, Carl Hirschie

doi:10.1073/pnas.0706069104

Cited by 96 publications

(122 citation statements)

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“…Since we know that circadian oscillations in gene expression and supercoiling are dependent on KaiC (3,6,13,14), the primary hypothesis is that KaiC either directly or indirectly controls supercoiling. KaiC sequence analysis suggests that it belongs in the RecA/DnaB superfamily (21) and KaiC has been shown to have DNA-binding activity in vitro (22), allowing for the possibility that KaiC may be able to directly change the superhelicity of DNA (14). An alternative model is that KaiC controls the ratio of negative versus positive supercoiling generating activity (14).…”

Section: Discussionmentioning

confidence: 99%

“…KaiC sequence analysis suggests that it belongs in the RecA/DnaB superfamily (21) and KaiC has been shown to have DNA-binding activity in vitro (22), allowing for the possibility that KaiC may be able to directly change the superhelicity of DNA (14). An alternative model is that KaiC controls the ratio of negative versus positive supercoiling generating activity (14). (26).…”

Section: Discussionmentioning

confidence: 99%

“…1B) sampled from the same time-course as the expression analysis (Fig. S6) (14). A comparison of the topological analysis with the microarray data suggests that each topological state corresponds to a unique state of gene expression ( Fig.…”

Section: Correlation Between Topological State and Gene Expressionmentioning

confidence: 98%

“…Plasmid isolation and CAGE technique were performed similarly to (14). Endogenous S. elongatus plasmid (pANS) was isolated using QIAprep miniprep kit (Qiagen).…”

Section: Isolation Of Plasmid Dna and Chloroquine Agarose Gel Electromentioning

confidence: 99%

“…In this model, circadian rhythms in the topology of the S. elongatus chromosome are thought to impart circadian gene expression patterns by modulating the affinity of the transcription machinery for promoters during the circadian cycle. After this model was proposed, two studies demonstrated circadian oscillations in the compaction and superhelical status of the S. elongatus chromosome and an endogenous plasmid, respectively (13,14). Although circadian oscillations in the topology of the chromosome are evident, it is unclear whether these oscillations cause circadian changes in gene expression.…”

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confidence: 99%

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Oscillations in supercoiling drive circadian gene expression in cyanobacteria

Vijayan

Zuzow

O’Shea

2009

Proc. Natl. Acad. Sci. U.S.A.

170

239

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The cyanobacterium Synechococcus elongatus PCC 7942 exhibits oscillations in mRNA transcript abundance with 24-h periodicity under continuous light conditions. The mechanism underlying these oscillations remains elusive-neither cis nor trans-factors controlling circadian gene expression phase have been identified. Here, we show that the topological status of the chromosome is highly correlated with circadian gene expression state. We also demonstrate that DNA sequence characteristics of genes that appear monotonically activated and monotonically repressed by chromosomal relaxation during the circadian cycle are similar to those of supercoiling-responsive genes in Escherichia coli. Furthermore, perturbation of superhelical status within the physiological range elicits global changes in gene expression similar to those that occur during the normal circadian cycle.circadian clock ͉ gene expression ͉ supercoiling ͉ cyanobacteria C ircadian rhythms in gene expression have been identified in many organisms. In general, 5-15% of an organism's transcriptome oscillates with 24-h periodicity in the absence of external cues such as light to dark or dark to light transitions (1). These transcriptional rhythms are controlled by an endogenous biological clock and allow organisms to schedule processes at appropriate times during the day and night cycle. The cyanobacterium Synechococcus elongatus PCC 7942 (hereafter, S. elongatus) is particularly striking because the majority of its gene expression is under circadian control in continuous light conditions. A ''promoter trap'' analysis using a bacterial luciferase reporter integrated at approximately 30,000 random loci showed circadian oscillations in bioluminescence at all 800 locations where bioluminescence signal was detected (2). A recent measurement of mRNA levels by microarray analysis demonstrated that at least 30% of transcript levels oscillated in circadian fashion (3). The discrepancy between promoter trap and microarray analysis is not surprising and is at least partially attributable to a combination of: (i) the limited time-resolution of microarrays and; (ii) the time-averaging of transcript levels observed in the bioluminescence output of promoter trap studies due to finite luciferase protein lifetime. The actual percentage of circadian transcripts in S. elongatus is likely between 30 and 100%; here we observe that 64% of transcripts oscillate with circadian periodicity (Fig. 1A).In S. elongatus, circadian oscillations in transcriptional activity require three genes, kaiA, kaiB, and kaiC, whose products comprise the core circadian oscillator. The proteins encoded by the kai genes interact with one another to generate circadian rhythms in KaiC phosphorylation at serine and threonine residues (4). Amazingly, an in vitro mixture of the Kai proteins and ATP reproduces in vivo oscillations in the phosphorylation state of KaiC (5). Inactivation of any kai gene abolishes circadian oscillations in both transcription and phosphorylation, and when kaiC is mutated such that p...

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Correlation Between Topological State and Gene Expressionmentioning

confidence: 98%

“…Plasmid isolation and CAGE technique were performed similarly to (14). Endogenous S. elongatus plasmid (pANS) was isolated using QIAprep miniprep kit (Qiagen).…”

Section: Isolation Of Plasmid Dna and Chloroquine Agarose Gel Electromentioning

confidence: 99%

mentioning

confidence: 99%

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Oscillations in supercoiling drive circadian gene expression in cyanobacteria

Vijayan

Zuzow

O’Shea

2009

Proc. Natl. Acad. Sci. U.S.A.

170

239

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Circadian Programmes in Cyanobacteria

Johnson

2011

Encyclopedia of Life Sciences

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Cyanobacteria are prokaryotes that express circadian (daily) rhythms. In rhythmic environments, the fitness of cyanobacteria is improved when this clock is operational and when its circadian period is similar to the period of the environmental cycle. In cyanobacteria, three key proteins (KaiA, KaiB and KaiC) form a core molecular clockwork that orchestrates global gene expression by modulating chromosomal topology. The three‐dimensional structures of these proteins have been determined. KaiA, KaiB and KaiC form a multiprotein nanomachine that can reconstitute a circadian oscillator in vitro , and this oscillator appears to function as a post‐translational oscillator (PTO) in vivo . Because this PTO regulates rhythmic transcription and translation, the entire circadian system comprises both the PTO and a transcriptional/translational feedback loop. Models of the complete in vivo system have important implications for our understanding of circadian clocks in higher organisms, including mammals. Key Concepts: Prokaryotic cyanobacteria have a circadian timekeeping system that enhances fitness. These cells exhibit pervasive circadian regulation of gene expression, possibly mediated by cyclic changes of chromosomal topology. A circadian rhythm of the phosphorylation of the central clock protein KaiC can be reconstituted in vitro with three proteins derived from cyanobacteria (KaiA, KaiB and KaiC) and ATP. KaiA, KaiB and KaiC are the only circadian clock proteins for which the 3‐D structure of full‐length proteins is known. Structural, biochemical and biophysical methods have been used to study the mechanism by which KaiC is rhythmically phosphorylated and dephosphorylated. Mathematical modelling that has been applied to the in vitro and in vivo systems indicate the existence of a core biochemical post‐translational oscillator (PTO) that controls a larger transcription/translation feedback loop (TTFL).

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