Switching of metabolic programs in response to light availability is an essential function of the cyanobacterial circadian output pathway

Puszynska, Anna M.; O’Shea, Erin K.

doi:10.7554/elife.23210

Cited by 44 publications

(55 citation statements)

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“…Studies that report conditional LDC effects have been limited to a small number of genes. For instance, mutants defective for the circadian clock output pathway genes, rpaA and sasA (15,16,18,19), and mutants unable to mobilize carbon through the OPPP and glycogen breakdown (16,20,21), or unable to synthesize the alarmone nucleotide ppGpp (22,23), have conditional defects specific to growth in LDC. To identify the genetic contributors to fitness under LDC and acquire a more comprehensive picture of the regulatory network, we used an unbiased population-based screen that tracks the fitness contributions of individual S. elongatus genes to reproduction in diel cycles.…”

Section: Significancementioning

confidence: 99%

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Genome-wide fitness assessment during diurnal growth reveals an expanded role of the cyanobacterial circadian clock protein KaiA

Welkie

Rubin

Chang

et al. 2018

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

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The recurrent pattern of light and darkness generated by Earth's axial rotation has profoundly influenced the evolution of organisms, selecting for both biological mechanisms that respond acutely to environmental changes and circadian clocks that program physiology in anticipation of daily variations. The necessity to integrate environmental responsiveness and circadian programming is exemplified in photosynthetic organisms such as cyanobacteria, which depend on light-driven photochemical processes. The cyanobacterium PCC 7942 is an excellent model system for dissecting these entwined mechanisms. Its core circadian oscillator, consisting of three proteins, KaiA, KaiB, and KaiC, transmits time-of-day signals to clock-output proteins, which reciprocally regulate global transcription. Research performed under constant light facilitates analysis of intrinsic cycles separately from direct environmental responses but does not provide insight into how these regulatory systems are integrated during light-dark cycles. Thus, we sought to identify genes that are specifically necessary in a day-night environment. We screened a dense bar-coded transposon library in both continuous light and daily cycling conditions and compared the fitness consequences of loss of each nonessential gene in the genome. Although the clock itself is not essential for viability in light-dark cycles, the most detrimental mutations revealed by the screen were those that disrupt KaiA. The screen broadened our understanding of light-dark survival in photosynthetic organisms, identified unforeseen clock-protein interaction dynamics, and reinforced the role of the clock as a negative regulator of a nighttime metabolic program that is essential for to survive in the dark.

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Section: Significancementioning

confidence: 99%

“…Among the targets of the RpaA regulon are the genes that facilitate catabolism of glycogen and generation of NADPH via the oxidative pentose phosphate pathway (OPPP) (14). These enzymatic reactions are essential for the cyanobacterium to survive the night when photosynthetic generation of reductant is disabled (15,16).…”

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confidence: 99%

Genome-wide fitness assessment during diurnal growth reveals an expanded role of the cyanobacterial circadian clock protein KaiA

Welkie

Rubin

Chang

et al. 2018

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

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“…The clock primarily regulates the expression of dusk genes [10], which include the genes required to utilize glycogen as an energy source in the absence of sunlight, such as glycogen phosphorylase and cytochrome c oxidase. As such, the circadian clock serves a critical function in switching S. elongatus from a daytime state of photosynthesis to a nighttime state of carbon metabolism through glycogen breakdown [9,[11][12][13]. In Constant Light conditions, the dusk and dawn genes show oscillatory expression with a 24 hr period, resulting in broad peaks of maximal expression ( Figure 1A, solid green line and dashed red line) [7,8].…”

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confidence: 99%

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

Piechura

Amarnath

O’Shea

2017

Preprint

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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 in metabolism. These changes in expression arise from control of RNA polymerase recruitment to promoters by circadian and light-responsive regulation of 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.Circadian clocks allow organisms from almost all branches of life to alter physiology in anticipation of diurnal changes in the environment. Circadian clocks keep time using autonomous core oscillators which control output pathways to direct periodic changes in the mRNA levels (expression) of genes, ultimately leading to oscillations in higher order behaviors [1]. Laboratory studies of the outputs of circadian clocks have been primarily performed under constant conditions to isolate circadian regulation from environmental responses. In nature, however, organisms with circadian clocks must also cope with unexpected fluctuations in the environment. Thus a major challenge in chronobiology is to understand circadian clocks and their outputs in dynamic environments.Previous studies suggest that circadian clock output pathways interact with environmental responses to tailor physiological outputs to both the time of day and the current state of the environment. For example, sleep/wake cycles in Drosophila melanogaster and photosynthesis in Arabidopsis thaliana are controlled by both the circadian clock and environmental variables like day length or light [2,3]. Further, circadian clocks can modulate environmental responses based on the time-of-day in a process called circadian gating [4,5]. However, the complexity of higher organisms has prevented a detailed understanding of the interaction between circadian timing information and environmental responses. In contrast, the circadian clock in the cyanobacterium Synechococcus elongatus PCC7942, an obligate photoautotroph, has a simple architecture which controls gene expression oscillations ( Figure 1A) to influence metabolism and growth. S. elongatus must carefully monitor its environment, as the sunlight required for photosynthesis fluctuates on the * These authors contributed equally to this work.† Correspondence: osheae@hhmi.org minute, day, and seasonal timescales (Figure 1B,[6]). While it is well understood how the ...

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“…Photosynthetic organisms experience drastic changes in their carbon metabolism during diurnal growth. Recent research has highlighted the contribution of glycogen metabolism and the OPP pathway to the fitness of cyanobacteria during diurnal growth (Diamond et al, 2017; Puszynska and O’Shea, 2017; Welkie et al, 2018). However, knowledge on metabolic engagement during the initiation of photosynthesis is not well understood.…”

Section: Discussionmentioning

confidence: 99%

“…When photosynthesis reactions start upon light, intermediates in the Calvin-Benson cycle might be limited after dark respiration, leading to stalled carbon fixation reactions. Dynamic metabolic regulation to ensure smooth transition from dark respiration to photosynthesis reactions is thus essential for the fitness of cyanobacteria during diurnal growth(Puszynska and O’Shea, 2017; Welkie et al, 2018). In this study, we discovered the active participation of glycogen metabolism during the dark-to-light transition period in cyanobacteria.…”

Section: Introductionmentioning

confidence: 99%

Glycogen metabolism jump-starts photosynthesis through the oxidative pentose phosphate pathway (OPPP) in cyanobacteria

Shinde

Singapuri

Zhang

et al. 2019

Preprint

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1Cyanobacteria experience drastic changes in their carbon metabolism under daily light-2 dark cycles. In the light, the Calvin-Benson cycle fixes CO 2 and divert excess carbon into 3 glycogen storage. At night, glycogen is degraded to support cellular respiration. Dark-light 4 transition represents a universal environmental stress for cyanobacteria and other photosynthetic 5 lifeforms. Recent studies in the field revealed the essential genetic background necessary for the 6 fitness of cyanobacteria during diurnal growth. However, the metabolic engagement behind the 7 dark-light transition is not well understood. In this study, we discovered that glycogen 8 metabolism can jump-start photosynthesis in the cyanobacterium Synechococcus elongatus PCC 9 7942 when photosynthesis reactions start upon light. Compared to the wild type, the glycogen 10 mutant (∆glgC) showed much lower photosystem II efficiency and slower photosystem I-11 mediated cyclic electron flow rate when photosynthesis starts. Proteomics analyses indicated that 12 glycogen is degraded through the oxidative pentose phosphate pathway (OPPP) during dark-light 13 transition. We confirmed that the OPPP is essential for the initiation of photosynthesis, and 14 further showed that glycogen degradation through the OPPP is likely to contribute to the 15 activation of key Calvin-Benson cycle enzymes by modulating NADPH levels during the 16 transition period. This ingenious strategy helps jump-start photosynthesis in cyanobacteria 17 following dark respiration, and stabilize the Calvin-Benson cycle under fluctuating 18 environmental conditions. It has evolutionary advantages for the survival of photosynthetic 19 organisms using the Calvin-Benson cycle for carbon fixation. 20

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Switching of metabolic programs in response to light availability is an essential function of the cyanobacterial circadian output pathway

Cited by 44 publications

References 42 publications

Genome-wide fitness assessment during diurnal growth reveals an expanded role of the cyanobacterial circadian clock protein KaiA

Genome-wide fitness assessment during diurnal growth reveals an expanded role of the cyanobacterial circadian clock protein KaiA

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

Glycogen metabolism jump-starts photosynthesis through the oxidative pentose phosphate pathway (OPPP) in cyanobacteria

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