The initiation of nocturnal dormancy in Synechococcus as an active process

The cyanobacterium Synechococcus elongatus relies upon photosynthesis to drive metabolism and growth. During darkness, Synechococcus stops growing, derives energy from its glycogen stores, and greatly decreases rates of macromolecular synthesis via unknown mechanisms. Here, we show that the stringent response, a stress response pathway whose genes are conserved across bacteria and plant plastids, contributes to this dark adaptation. Levels of the stringent response alarmone guanosine 3′-diphosphate 5′-diphosphate (ppGpp) rise after a shift from light to dark, indicating that darkness triggers the same response in cyanobacteria as starvation in heterotrophic bacteria. High levels of ppGpp are sufficient to stop growth and dramatically alter many aspects of cellular physiology, including levels of photosynthetic pigments and polyphosphate, DNA content, and the rate of translation. Cells unable to synthesize ppGpp display pronounced growth defects after exposure to darkness. The stringent response regulates expression of a number of genes in Synechococcus, including ribosomal hibernation promoting factor (hpf), which causes ribosomes to dimerize in the dark and may contribute to decreased translation. Although the metabolism of Synechococcus differentiates it from other model bacterial systems, the logic of the stringent response remains remarkably conserved, while at the same time having adapted to the unique stresses of the photosynthetic lifestyle.

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“…4A), as has been seen previously (9,10), and that some of these gene expression changes are (p)ppGpp-dependent (SI Appendix, Fig. S5).…”

Section: High (P)ppgpp Levels Stop Growth and Dramatically Alter Synesupporting

confidence: 80%

“…Proteins produced in the dark differ from those produced in the light (8), and recent studies have identified genes that are differentially expressed between light and dark (9,10). How the cell coordinates these transcriptional and translational changes remains largely unknown.…”

mentioning

confidence: 99%

The stringent response regulates adaptation to darkness in the cyanobacterium Synechococcus elongatus

Hood

Higgins

Flamholz

et al. 2016

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

106

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“…To decrease the ATP/ADP ratio under conditions in which we do not normally observe foci, that is, in illuminated cultures, we used DCCD, a specific inhibitor of the F o F 1 -ATP synthase (Fig. 6B) (Takano et al, 2015). Foci were first detected 30 min after DCCD treatment, following a fast and sharp decrease in the ATP/ADP ratio, and continued to increase during the following 4 h of the experiment, when ca.…”

Section: Pii-pipx Foci Depend On a Low Atp/adp Ratio: Biochemical Andmentioning

confidence: 99%

“…Sequestering of PipX by PII at low ATP/ADP ratios would interfere with energetically expensive biological processes, decreasing transcriptional activity in the dark (Hosokawa et al, 2011;Takano et al, 2015). In addition to down regulation of NtcA target genes co-regulated by PipX (Espinosa et al, 2007;Valladares et al, 2011;Espinosa et al, 2014;Giner-Lamia et al, 2017), it would also affect the predicted signalling pathway responsible for the toxic functions of PipX in the absence of PII ( Fig.…”

Section: Environmental Importance Of Pii-pipx Complexes and Possible mentioning

confidence: 99%

Energy drives the dynamic localization of cyanobacterial nitrogen regulators during diurnal cycles

Espinosa

Labella

Cantos

et al. 2018

Environmental Microbiology

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Cyanobacteria, phototrophic organisms performing oxygenic photosynthesis, must adapt their metabolic processes to the challenges imposed by the succession of days and nights. Two conserved cyanobacterial proteins, PII and PipX, function as hubs of the nitrogen interaction network, forming complexes with a variety of diverse targets. While PII proteins are found in all three domains of life as integrators of signals of the nitrogen and carbon balance, PipX proteins are unique to cyanobacteria, where they provide a mechanistic link between PII signalling and the control of gene expression by the global nitrogen regulator NtcA. Here we demonstrate that PII and PipX display distinct localization patterns during diurnal cycles, co-localizing into the same foci at the periphery and poles of the cells during dark periods, a circadian-independent process requiring a low ATP/ADP ratio. Genetic, cellular biology and biochemical approaches used here provide new insights into the nitrogen regulatory network, calling attention to the roles of PII as energy sensors and its interactions with PipX in the context of essential signalling pathways. This study expands the contribution of the nitrogen regulators PII and PipX to integrate and transduce key environmental signals that allow cyanobacteria to thrive in our planet.

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“…Some photosynthetic organisms that rely exclusively on light for growth are known to halt DNA synthesis and enter a dormant state (20), or even die (21), in the absence of light. Since control of gene expression in the dark and consumption of energy metabolites are both under active control of the circadian clock in cyanobacteria (9,10,22), we hypothesized that unanticipated nightfall at clock times when energy reserves are low and metabolic rates are high could have deleterious effects. To test this hypothesis, we exposed a uniformly distributed ( Fig.…”

Section: A Subset Of Cells With Misaligned Clocks Do Not Survive the mentioning

confidence: 99%

Costs of Clock-Environment Misalignment in Individual Cyanobacterial Cells

Lambert¹,

Rust²,

Chew³

2016

Preprint

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Circadian rhythms are endogenously generated daily oscillations in physiology that are found in all kingdoms of life. Experimental studies have shown that the fitness of Synechococcus elongatus, a photosynthetic microorganism, is severely affected in non-24-h environments. However, it has been difficult to study the effects of clock-environment mismatch on cellular physiology because such measurements require a precise determination of both clock state and growth rate in the same cell. Here, we designed a microscopy platform that allows us to expose cyanobacterial cells to pulses of light and dark while quantitatively measuring their growth, division rate, and circadian clock state over many days. Our measurements reveal that decreased fitness can result from a catastrophic growth arrest caused by unexpected darkness in a small subset of cells with incorrect clock times corresponding to the subjective morning. We find that the clock generates rhythms in the instantaneous growth rate of the cell, and that the time of darkness vulnerability coincides with the time of most rapid growth. Thus, the clock mediates a fundamental trade-off between growth and starvation tolerance in cycling environments. By measuring the response of the circadian rhythm to dark pulses of varying lengths, we constrain a mathematical model of a population's fitness under arbitrary light/dark schedules. This model predicts that the circadian clock is only advantageous in highly regular cycling environments with frequencies sufficiently close to the natural frequency of the clock.

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The initiation of nocturnal dormancy in Synechococcus as an active process

Cited by 20 publications

References 26 publications

The stringent response regulates adaptation to darkness in the cyanobacterium Synechococcus elongatus

The stringent response regulates adaptation to darkness in the cyanobacterium Synechococcus elongatus

Energy drives the dynamic localization of cyanobacterial nitrogen regulators during diurnal cycles

Costs of Clock-Environment Misalignment in Individual Cyanobacterial Cells

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