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

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.

The circadian clock and darkness control natural competence in cyanobacteria

“…1a, 4b), has circadian dusk-peaking expression that increases with darkness ( Fig. 3a, b), and is a target for RpaA and RpaB 24,37 , which are both implicated in the regulation of circadian genes by light availability. SigF2 is paralogous to SigF, which in other cyanobacteria is associated with pili formation and motility 41 .…”

“…Loss of the master regulator RpaA has pleiotropic effects, including extreme sensitivity to darkness 34 ; as a result, this locus is so poorly represented in the control library that its loss of competence is not reflected in the pipeline that compares the transformed and untransformed barcodes, as was also true for elucidation of genes required for growth in light-dark cycles 35 . To delve further, we analyzed available circadian and light/dark transcriptomes for S. elongatus 24,36,37 (Supplementary Data 1). The data clearly indicate that most of the T4PM is circadian controlled and expressed in the morning.…”

“…While the induction of dusk genes, including the competence genes pilA3 and pilW, is under the control of phosphorylated RpaA (Supplementary Data 1) 24 , the mechanism behind increased natural competence in response to darkness is less clear. The expression of hundreds of circadian-regulated genes is affected by changes in light intensity, implicating a network of transcription regulators that is still not well understood 37 . The RB-TnSeq screen revealed the antagonistic importance of two sigma factors in natural competence: sigF2 and rpoD2 (Fig.…”

Growth of Cyanobacteria Is Constrained by the Abundance of Light and Carbon Assimilation Proteins

“…Excess light uptake also poses the additional risk of an over-reduced metabolism (lack of re-generated nicotinamide adenine dinucleotide (phosphate) [NAD(P)+]) that eventually reduces growth (Holland et al, 2015). Furthermore, a fluctuating energy source (sunlight) gives rise to temporal gene regulation, such as expression of enzymes for glycogen synthesis and storage, which may constrain their ability to maximize the growth rate under any given condition (Piechura et al, 2017;Reimers et al, 2017).…”

Global analysis of the RpaB regulon based on the positional distribution of HLR1 sequences and comparative differential RNA-Seq data

“…Therefore, it is established that the regulon controlled by RpaB consists of genes encoding photosynthesis-related proteins as well as at least one sRNA and that this regulation is of crucial importance in light acclimation responses and circadian clock-related processes (18). In contrast, its cognate histidine kinase Hik 33 (synonyms NblS or DspA) functions as multistress sensor responding not only to HL (19) but also to low temperature (20), hyperosmolarity (21), high salinity (22), oxidative stress (23) and nutrient stress (7).…”