Daily Rhythms in the Cyanobacterium Synechococcus elongatus Probed by High-resolution Mass Spectrometry–based Proteomics Reveals a Small Defined Set of Cyclic Proteins

Guerreiro, Ana C. L.; Benevento, Marco; Lehmann, Robert; Breukelen, Bas van; Post, Harm; Giansanti, Piero; Altelaar, Maarten; Axmann, Ilka M.; Heck, Albert J. R.

doi:10.1074/mcp.m113.035840

Cited by 75 publications

(79 citation statements)

References 52 publications

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“…Finally, we performed untargeted metabolic profiling of WTcells and ΔkaiC mutants to investigate how oscillator activity affects global metabolite abundance at the transition from darkness into light. We present a hypothesis for clock regulation of diurnal metabolism that combines our data with previous reports on S. elongatus transcript and protein rhythms (17,21,23) and that highlights the importance of circadian output for proper metabolite partitioning under LD growth regimes.…”

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confidence: 56%

“…A few studies have investigated the transcriptome, proteome, and physiological dynamics of particular species of cyanobacteria over a 24-h period under LD growth (6,22,23). In general, systems for oxygenic photosynthesis are activated during the day, and systems for respiratory metabolism are activated at night.…”

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confidence: 99%

“…The available studies investigate these effects only over a lightto-dark transition, so currently there is an incomplete understanding of the circadian influence on cellular events over a full 24-h LD cycle. Finally, although there is a proteomics dataset for S. elongatus that covers a full 24-h LD period, that study tracked only WT cells and does not decouple clock and environmental influences (23).…”

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confidence: 99%

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The circadian oscillator in Synechococcus elongatus controls metabolite partitioning during diurnal growth

Diamond

Jun

Rubin

et al. 2015

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

122

158

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Synechococcus elongatus PCC 7942 is a genetically tractable model cyanobacterium that has been engineered to produce industrially relevant biomolecules and is the best-studied model for a prokaryotic circadian clock. However, the organism is commonly grown in continuous light in the laboratory, and data on metabolic processes under diurnal conditions are lacking. Moreover, the influence of the circadian clock on diurnal metabolism has been investigated only briefly. Here, we demonstrate that the circadian oscillator influences rhythms of metabolism during diurnal growth, even though lightdark cycles can drive metabolic rhythms independently. Moreover, the phenotype associated with loss of the core oscillator protein, KaiC, is distinct from that caused by absence of the circadian output transcriptional regulator, RpaA (regulator of phycobilisome-associated A). Although RpaA activity is important for carbon degradation at night, KaiC is dispensable for those processes. Untargeted metabolomics analysis and glycogen kinetics suggest that functional KaiC is important for metabolite partitioning in the morning. Additionally, output from the oscillator functions to inhibit RpaA activity in the morning, and kaiC-null strains expressing a mutant KaiC phosphomimetic, KaiC-pST, in which the oscillator is locked in the most active output state, phenocopies a ΔrpaA strain. Inhibition of RpaA by the oscillator in the morning suppresses metabolic processes that normally are active at night, and kaiC-null strains show indications of oxidative pentose phosphate pathway activation as well as increased abundance of primary metabolites. Inhibitory clock output may serve to allow secondary metabolite biosynthesis in the morning, and some metabolites resulting from these processes may feed back to reinforce clock timing.C yanobacteria comprise a promising engineering platform for the production of fuels and industrial chemicals. These organisms already have been engineered to produce ethanol, isobutyraldehyde, alkanes, and hydrogen (1-4). However, the efficient industrial-scale application of these photosynthetic organisms will require their growth and maintenance in the outdoors where they will be subjected to light-dark (LD) cycles (5). Phototrophic cyanobacteria present a completely different engineering challenge relative to heterotrophic bacteria such as Escherichia coli: their cellular activities respond strongly to the presence and absence of light because their metabolism is centered on photosynthesis (6, 7). Diverse cyanobacteria also possess a true circadian clock that synchronizes with external LD cycles and has been demonstrated to drive both gene expression and metabolic rhythms (8-10). It is important to understand how signals from the external environment and the internal circadian clock are integrated to modulate metabolic processes in environmentally relevant LD cycles to optimize the engineering of these organisms. In this work we attempt to separate the influences of environment and circadian control using the cyan...

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confidence: 56%

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confidence: 99%

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confidence: 99%

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The circadian oscillator in Synechococcus elongatus controls metabolite partitioning during diurnal growth

Diamond

Jun

Rubin

et al. 2015

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

122

158

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“…For example, a major unknown factor is the relative amount of noncatalytic proteins, reported to be up to 55% of total protein for slow-growing cells (31). We hypothesize that, for fast-growing cells, this percentage is considerably lower.…”

Section: Discussionmentioning

confidence: 95%

“…measurements over a full diurnal cycle have been conducted yet, several studies have investigated the transcriptome, proteome, and physiology of S. elongatus PCC 7942 and other cyanobacteria over a full 24-h diurnal cycle (9,31,33,34). Published transcriptome studies of cyanobacteria typically show global rhythms in gene expression, including a significant reduction of the transcriptional output during the dark period (33,35,36).…”

Section: Resultsmentioning

confidence: 99%

Cellular trade-offs and optimal resource allocation during cyanobacterial diurnal growth

Reimers

Knoop

Bockmayr

et al. 2017

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

100

130

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Cyanobacteria are an integral part of Earth's biogeochemical cycles and a promising resource for the synthesis of renewable bioproducts from atmospheric CO 2 . Growth and metabolism of cyanobacteria are inherently tied to the diurnal rhythm of light availability. As yet, however, insight into the stoichiometric and energetic constraints of cyanobacterial diurnal growth is limited. Here, we develop a computational framework to investigate the optimal allocation of cellular resources during diurnal phototrophic growth using a genome-scale metabolic reconstruction of the cyanobacterium Synechococcus elongatus PCC 7942. We formulate phototrophic growth as an autocatalytic process and solve the resulting time-dependent resource allocation problem using constraint-based analysis. Based on a narrow and well-defined set of parameters, our approach results in an ab initio prediction of growth properties over a full diurnal cycle. The computational model allows us to study the optimality of metabolite partitioning during diurnal growth. The cyclic pattern of glycogen accumulation, an emergent property of the model, has timing characteristics that are in qualitative agreement with experimental findings. The approach presented here provides insight into the time-dependent resource allocation problem of phototrophic diurnal growth and may serve as a general framework to assess the optimality of metabolic strategies that evolved in phototrophic organisms under diurnal conditions. constraint-based analysis | whole-cell models | bioenergetics | metabolism | circadian clock C yanobacterial photoautotrophic growth requires a highly coordinated distribution of cellular resources to different intracellular processes, including the de novo synthesis of proteins, ribosomes, lipids, and other cellular components. For unicellular organisms, the optimal allocation of limiting resources is a key determinant of evolutionary fitness. Owing to the importance of cellular resource allocation for understanding evolutionary trade-offs in bacterial metabolism, the cellular "protein economy" and its implications for bacterial growth laws have been studied extensively, albeit almost exclusively for heterotrophic organisms under stationary environmental conditions (1-7). For photoautotrophic organisms, including cyanobacteria, growthdependent resource allocation is further subject to diurnal lightdark (LD) cycles that partition cellular metabolism into distinct phases. Recent experimental results have demonstrated the relevance of time-specific synthesis for cellular survival and growth (8-10). Nonetheless, the implications and consequences of a diurnal environment for the cellular resource allocation problem are insufficiently understood, and computational approaches hitherto developed for heterotrophic growth are not straightforwardly applicable to diurnal phototrophic growth (11).Here, we propose a computational framework to quantitatively assess the optimality of diurnal resource allocation for phototrophic growth. We are primarily interested i...

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The Kai-Protein Clock—Keeping Track of Cyanobacteria’s Daily Life

Snijder

Axmann

2019

Subcellular Biochemistry

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Daily Rhythms in the Cyanobacterium Synechococcus elongatus Probed by High-resolution Mass Spectrometry–based Proteomics Reveals a Small Defined Set of Cyclic Proteins

Cited by 75 publications

References 52 publications

The circadian oscillator in Synechococcus elongatus controls metabolite partitioning during diurnal growth

The circadian oscillator in Synechococcus elongatus controls metabolite partitioning during diurnal growth

Cellular trade-offs and optimal resource allocation during cyanobacterial diurnal growth

The Kai-Protein Clock—Keeping Track of Cyanobacteria’s Daily Life

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