Giving Time Purpose: The <i>Synechococcus elongatus</i> Clock in a Broader Network Context

Shultzaberger, Ryan K.; Boyd, J. Morton; Diamond, Spencer; Greenspan, Ralph J.; Golden, Susan S.

doi:10.1146/annurev-genet-111212-133227

Cited by 32 publications

(32 citation statements)

References 102 publications

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“…Circadian measurements historically have been performed in constant light (LL) conditions to distinguish internal circadian regulation from that which is environmentally driven (16,17). However, diurnal physiology in a natural environment must integrate the two sources of regulation.…”

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confidence: 99%

“…A daily LD cycle presents a strong metabolic driver for the photosynthetic cyanobacteria, but a circadian clock also imposes daily cycles in transcription and redox regulatory systems (17,18). Circadian measurements historically have been performed in constant light (LL) conditions to distinguish internal circadian regulation from that which is environmentally driven (16,17).…”

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confidence: 99%

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Redox crisis underlies conditional light–dark lethality in cyanobacterial mutants that lack the circadian regulator, RpaA

Diamond

Rubin

Shultzaberger

et al. 2017

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

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Cyanobacteria evolved a robust circadian clock, which has a profound influence on fitness and metabolism under daily lightdark (LD) cycles. In the model cyanobacterium Synechococcus elongatus PCC 7942, a functional clock is not required for diurnal growth, but mutants defective for the response regulator that mediates transcriptional rhythms in the wild-type, regulator of phycobilisome association A (RpaA), cannot be cultured under LD conditions. We found that rpaA-null mutants are inviable after several hours in the dark and compared the metabolomes of wild-type and rpaA-null strains to identify the source of lethality. Here, we show that the wild-type metabolome is very stable throughout the night, and this stability is lost in the absence of RpaA. Additionally, an rpaA mutant accumulates excessive reactive oxygen species (ROS) during the day and is unable to clear it during the night. The rpaA-null metabolome indicates that these cells are reductant-starved in the dark, likely because enzymes of the primary nighttime NADPH-producing pathway are direct targets of RpaA. Because NADPH is required for processes that detoxify ROS, conditional LD lethality likely results from inability of the mutant to activate reductant-requiring pathways that detoxify ROS when photosynthesis is not active. We identified second-site mutations and growth conditions that suppress LD lethality in the mutant background that support these conclusions. These results provide a mechanistic explanation as to why rpaA-null mutants die in the dark, further connect the clock to metabolism under diurnal growth, and indicate that RpaA likely has important unidentified functions during the day.C yanobacteria are both key agents of global carbon and nitrogen cycles and promising platforms for renewable chemicals, fuels, and nutraceuticals (1-3). Understanding the control mechanisms that govern the flow of carbon and nitrogen through these organisms is crucial for predicting their behavior in natural environments as well as for improving engineering strategies. Although the basic pathways for carbon and nitrogen metabolism, and their regulation, are well understood in heterotrophic bacteria, cyanobacteria exhibit important deviations in these core metabolic pathways (4-7). Additionally, metabolic control mechanisms in cyanobacteria evolved to be compatible with photoautotrophic metabolism and the dramatic shifts that are imposed on those pathways by predictable daily light-dark (LD) cycles. Examples include enzymatic activity that responds to light-dependent cellular redox changes (8-11); the preference for NADPH, the reductant produced by the photochemical reactions, over NADH by many biosynthetic enzymes (12, 13); and a circadian clock that drives 24-h transcriptional rhythms in most genes (14-16).A daily LD cycle presents a strong metabolic driver for the photosynthetic cyanobacteria, but a circadian clock also imposes daily cycles in transcription and redox regulatory systems (17, 18). Circadian measurements historically have been performed in...

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Redox crisis underlies conditional light–dark lethality in cyanobacterial mutants that lack the circadian regulator, RpaA

Diamond

Rubin

Shultzaberger

et al. 2017

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

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“…The cyanobacterial circadian clock system, an ATP-dependent, posttranslational molecular oscillator, has been thoroughly characterized biochemically, structurally, and functionally (25)(26)(27)(28)(29)(30)(31). Typically, the system consists of three protein components, KaiA, KaiB, and KaiC (Fig.…”

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confidence: 99%

“…KaiB has the thioredoxin fold and interacts with the N-terminal (CI) domain of KaiC, promoting dissociation of KaiA and dephosphorylation of KaiC. The cyanobacterium Prochlorococcus marinus encodes a minimal circadian system that lacks KaiA but nevertheless shows some features of an autonomous oscillator that, however, does not persist long under constant-light conditions, so that the system apparently requires a reset each diel cycle (26,32). However, even when all three components are present, this is not always sufficient to reproduce all of the canonical properties of a circadian clock, as is the case in the purple nonsulfur bacterium Rhodopseudomonas palustris, which only poorly maintains rhythmicity under constant conditions (33).…”

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“…However, even when all three components are present, this is not always sufficient to reproduce all of the canonical properties of a circadian clock, as is the case in the purple nonsulfur bacterium Rhodopseudomonas palustris, which only poorly maintains rhythmicity under constant conditions (33). Multiple input and output components have been shown to interact with the cyanobacterial circadian clock system, forming a complex, interconnected network that includes transcriptional regulators, receiver (REC) domains, and sensory histidine kinases, as well as light-sensitive redox molecules such as quinones (26). Some of the input and output proteins contain KaiAor KaiB-like domains and directly interact with KaiC.…”

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Proposed Role for KaiC-Like ATPases as Major Signal Transduction Hubs in Archaea

Makarova

Galperin

Koonin

2017

mBio

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All organisms must adapt to ever-changing environmental conditions and accordingly have evolved diverse signal transduction systems. In bacteria, the most abundant networks are built around the two-component signal transduction systems that include histidine kinases and receiver domains. In contrast, eukaryotic signal transduction is dominated by serine/threonine/tyrosine protein kinases. Both of these systems are also found in archaea, but they are not as common and diversified as their bacterial and eukaryotic counterparts, suggesting the possibility that archaea have evolved other, still uncharacterized signal transduction networks. Here we propose a role for KaiC family ATPases, known to be key components of the circadian clock in cyanobacteria, in archaeal signal transduction. The KaiC family is notably expanded in most archaeal genomes, and although most of these ATPases remain poorly characterized, members of the KaiC family have been shown to control archaellum assembly and have been found to be a stable component of the gas vesicle system in Halobacteria. Computational analyses described here suggest that KaiC-like ATPases and their homologues with inactivated ATPase domains are involved in many other archaeal signal transduction pathways and comprise major hubs of complex regulatory networks. We predict numerous input and output domains that are linked to KaiC-like proteins, including putative homologues of eukaryotic DEATH domains that could function as adapters in archaeal signaling networks. We further address the relationships of the archaeal family of KaiC homologues to the bona fide KaiC of cyanobacteria and implications for the existence of a KaiCbased circadian clock apparatus in archaea.IMPORTANCE Little is currently known about signal transduction pathways in Archaea. Recent studies indicate that KaiC-like ATPases, known as key components of the circadian clock apparatus in cyanobacteria, are involved in the regulation of archaellum assembly and, likely, type IV pili and the gas vesicle system in Archaea. We performed comprehensive comparative genomic analyses of the KaiC family. A vast protein interaction network was revealed, with KaiC family proteins as hubs for numerous input and output components, many of which are shared with twocomponent signal transduction systems. Putative KaiC-based signal transduction systems are predicted to regulate the activities of membrane-associated complexes and individual proteins, such as signal recognition particle and membrane transporters, and also could be important for oxidative stress response regulation. KaiC-centered signal transduction networks are predicted to play major roles in archaeal physiology, and this work is expected to stimulate their experimental characterization.

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Circadian Programmes in Cyanobacteria

Cohen

2021

Encyclopedia of Life Sciences

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Cyanobacteria are bacteria 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 rhythmic outputs including global rhythms of gene expression, cell division, compaction of the chromosome and metabolism. KaiA, KaiB and KaiC form a multiprotein nanomachine that can reconstitute a circadian oscillator in vitro , and this oscillator appears to function as a posttranslational oscillator (PTO) in vivo . In vivo , an extended clock network allows the core oscillator to synchronize with the environment and relate temporal information to clock‐controlled activities. 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. 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 3D 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. Rhythmic associations of the extended clock network with the KaiABC oscillator help to coordinate rhythmic outputs.

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Giving Time Purpose: The Synechococcus elongatus Clock in a Broader Network Context

Cited by 32 publications

References 102 publications

Redox crisis underlies conditional light–dark lethality in cyanobacterial mutants that lack the circadian regulator, RpaA

Redox crisis underlies conditional light–dark lethality in cyanobacterial mutants that lack the circadian regulator, RpaA

Proposed Role for KaiC-Like ATPases as Major Signal Transduction Hubs in Archaea

Circadian Programmes in Cyanobacteria

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