Natural changes in light interact with circadian regulation at promoters to control gene expression in cyanobacteria.

Joseph Robert Piechura,Kapil Amarnath,Erin K O'Shea

doi:10.7554/elife.32032

Joseph Robert Piechura, Kapil Amarnath + Show 1 more

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https://doi.org/10.7554/elife.32032

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Abstract

The circadian clock interacts with other regulatory pathways to tune physiology to predictable daily changes and unexpected environmental fluctuations. However, the complexity of circadian clocks in higher organisms has prevented a clear understanding of how natural environmental conditions affect circadian clocks and their physiological outputs. Here, we dissect the interaction between circadian regulation and responses to fluctuating light in the cyanobacterium Synechococcus elongatus. We demonstrate that natural changes in light intensity substantially affect the expression of hundreds of circadian-clock-controlled genes, many of which are involved in key steps of metabolism. These changes in expression arise from circadian and light-responsive control of RNA polymerase recruitment to promoters by a network of transcription factors including RpaA and RpaB. Using phenomenological modeling constrained by our data, we reveal simple principles that underlie the small number of stereotyped responses of dusk circadian genes to changes in light.

Highlights

Circadian clocks allow organisms from almost all branches of life to alter physiology in anticipation of diurnal changes in the environment
Note that the Low Light condition used here differs from the Constant Light condition in that the cells are exposed to more naturally-relevant 12 hr light-12 h dark days (LD)
We show that natural fluctuations in light intensity significantly affect the dynamics of circadian gene expression (Figures 2 and 3)

Summary

Introduction

Circadian clocks allow organisms from almost all branches of life to alter physiology in anticipation of diurnal changes in the environment. Circadian clocks are autonomous core oscillators that keep time even in the absence of environmental cues (Dunlap et al, 2004). Output pathways interpret timing information from the core oscillator to generate oscillating outputs, such as oscillations in the mRNA levels (expression) of genes and higher order behaviors (Dunlap et al, 2004; Wijnen and Young, 2006). Laboratory studies of the outputs of circadian clocks have been primarily performed under constant conditions to isolate circadian regulation from environmental responses. Organisms with circadian clocks must cope with unexpected fluctuations in the environment. A major challenge in chronobiology is to understand circadian regulation in dynamic environments

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