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The initiation of nocturnal dormancy in Synechococcus as an active process.

Takano S, Tomita J, Sonoike K, Iwasaki H - BMC Biol. (2015)

Bottom Line: Because Synechococcus is an obligate photoautotroph, it has been generally assumed that repression of the transcription in the dark (dark repression) would be caused by a nocturnal decrease in photosynthetic activities through the reduced availability of energy (e.g. adenosine triphosphate (ATP)) needed for mRNA synthesis.By contrast, when ATP levels were decreased by the inhibition of both photosynthesis and respiration, the transcriptional repression was attenuated through inhibition of RNA degradation.Even though the level of total mRNA dramatically decreased in the dark, Synechococcus cells were still viable, and they do not need de novo transcription for their survival in the dark for at least 48 hours.

View Article: PubMed Central - PubMed

Affiliation: Department of Electrical Engineering and Biological Science, Waseda University, TWIns, Shinjuku, Tokyo, 162-8480, Japan. sou.tacano@gmail.com.

ABSTRACT

Background: Most organisms, especially photoautotrophs, alter their behaviours in response to day-night alternations adaptively because of their great reliance on light. Upon light-to-dark transition, dramatic and universal decreases in transcription level of the majority of the genes in the genome of the unicellular cyanobacterium, Synechococcus elongatus PCC 7942 are observed. Because Synechococcus is an obligate photoautotroph, it has been generally assumed that repression of the transcription in the dark (dark repression) would be caused by a nocturnal decrease in photosynthetic activities through the reduced availability of energy (e.g. adenosine triphosphate (ATP)) needed for mRNA synthesis.

Results: However, against this general assumption, we obtained evidence that the rapid and dynamic dark repression is an active process. Although the addition of photosynthesis inhibitors to cells exposed to light mimicked transcription profiles in the dark, it did not significantly affect the cellular level of ATP. By contrast, when ATP levels were decreased by the inhibition of both photosynthesis and respiration, the transcriptional repression was attenuated through inhibition of RNA degradation. This observation indicates that Synechococcus actively downregulates genome-wide transcription in the dark. Even though the level of total mRNA dramatically decreased in the dark, Synechococcus cells were still viable, and they do not need de novo transcription for their survival in the dark for at least 48 hours.

Conclusions: Dark repression appears to enable cells to enter into nocturnal dormancy as a feed-forward process, which would be advantageous for their survival under periodic nocturnal conditions.

No MeSH data available.


Related in: MedlinePlus

Synechococcus actively initiates a nocturnal dormancy-like state. a Model of nocturnal dormancy-like state initiation. Initiating nocturnal depression of transcription requires maintenance of ATP content and possibly oxidation of the acceptor side of PS I. PS II, photosystem II; NDH, NAD(P)H dehydrogenase complex; SDH, succinate dehydrogenase; PQ, plastoquinone pool; b/f, cytochrome b6/f complex; PS I, photosystem I; FNR, ferredoxin; Fd, ferredoxin; Ox, cytochrome-c oxidase. bSynechococcus colonies grown in the light after incubation under different conditions: in the light or the dark in the presence or absence of rifampicin (Rif) for the indicated time. Cells survived in the dark even without de novo transcription. c The time course of cell survival under each condition quantified from visible colony numbers from independent triplicate experiments. In each experiment, colony numbers were normalized to the average number of control samples at time 0, corresponding to 12 hours in the light. Bars indicate the standard deviation
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Fig4: Synechococcus actively initiates a nocturnal dormancy-like state. a Model of nocturnal dormancy-like state initiation. Initiating nocturnal depression of transcription requires maintenance of ATP content and possibly oxidation of the acceptor side of PS I. PS II, photosystem II; NDH, NAD(P)H dehydrogenase complex; SDH, succinate dehydrogenase; PQ, plastoquinone pool; b/f, cytochrome b6/f complex; PS I, photosystem I; FNR, ferredoxin; Fd, ferredoxin; Ox, cytochrome-c oxidase. bSynechococcus colonies grown in the light after incubation under different conditions: in the light or the dark in the presence or absence of rifampicin (Rif) for the indicated time. Cells survived in the dark even without de novo transcription. c The time course of cell survival under each condition quantified from visible colony numbers from independent triplicate experiments. In each experiment, colony numbers were normalized to the average number of control samples at time 0, corresponding to 12 hours in the light. Bars indicate the standard deviation

Mentions: Our results have shown that Synechococcus actively stops transcription and enhances mRNA degradation in the dark via respiration, which requires both the inhibition of photosynthetic electron flow and the maintenance of ATP synthesis via respiration. Considering that ATP content is gradually lowered after longer dark acclimation during the night [5], we assume that dark acclimation triggers the genome-wide transcriptional depression, which is most likely advantageous for suppression of ATP-consuming reactions, such as transcription and translation, in anticipation of the subsequent loss of energy availability during the night. This is a typical feed-forward regulation, which would be important for Synechococcus to survive during nocturnal ‘starvation’ time in a relatively inactive fashion, as if they were in a dormant state (Fig. 4a).Fig. 4


The initiation of nocturnal dormancy in Synechococcus as an active process.

Takano S, Tomita J, Sonoike K, Iwasaki H - BMC Biol. (2015)

Synechococcus actively initiates a nocturnal dormancy-like state. a Model of nocturnal dormancy-like state initiation. Initiating nocturnal depression of transcription requires maintenance of ATP content and possibly oxidation of the acceptor side of PS I. PS II, photosystem II; NDH, NAD(P)H dehydrogenase complex; SDH, succinate dehydrogenase; PQ, plastoquinone pool; b/f, cytochrome b6/f complex; PS I, photosystem I; FNR, ferredoxin; Fd, ferredoxin; Ox, cytochrome-c oxidase. bSynechococcus colonies grown in the light after incubation under different conditions: in the light or the dark in the presence or absence of rifampicin (Rif) for the indicated time. Cells survived in the dark even without de novo transcription. c The time course of cell survival under each condition quantified from visible colony numbers from independent triplicate experiments. In each experiment, colony numbers were normalized to the average number of control samples at time 0, corresponding to 12 hours in the light. Bars indicate the standard deviation
© Copyright Policy - open-access
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4494158&req=5

Fig4: Synechococcus actively initiates a nocturnal dormancy-like state. a Model of nocturnal dormancy-like state initiation. Initiating nocturnal depression of transcription requires maintenance of ATP content and possibly oxidation of the acceptor side of PS I. PS II, photosystem II; NDH, NAD(P)H dehydrogenase complex; SDH, succinate dehydrogenase; PQ, plastoquinone pool; b/f, cytochrome b6/f complex; PS I, photosystem I; FNR, ferredoxin; Fd, ferredoxin; Ox, cytochrome-c oxidase. bSynechococcus colonies grown in the light after incubation under different conditions: in the light or the dark in the presence or absence of rifampicin (Rif) for the indicated time. Cells survived in the dark even without de novo transcription. c The time course of cell survival under each condition quantified from visible colony numbers from independent triplicate experiments. In each experiment, colony numbers were normalized to the average number of control samples at time 0, corresponding to 12 hours in the light. Bars indicate the standard deviation
Mentions: Our results have shown that Synechococcus actively stops transcription and enhances mRNA degradation in the dark via respiration, which requires both the inhibition of photosynthetic electron flow and the maintenance of ATP synthesis via respiration. Considering that ATP content is gradually lowered after longer dark acclimation during the night [5], we assume that dark acclimation triggers the genome-wide transcriptional depression, which is most likely advantageous for suppression of ATP-consuming reactions, such as transcription and translation, in anticipation of the subsequent loss of energy availability during the night. This is a typical feed-forward regulation, which would be important for Synechococcus to survive during nocturnal ‘starvation’ time in a relatively inactive fashion, as if they were in a dormant state (Fig. 4a).Fig. 4

Bottom Line: Because Synechococcus is an obligate photoautotroph, it has been generally assumed that repression of the transcription in the dark (dark repression) would be caused by a nocturnal decrease in photosynthetic activities through the reduced availability of energy (e.g. adenosine triphosphate (ATP)) needed for mRNA synthesis.By contrast, when ATP levels were decreased by the inhibition of both photosynthesis and respiration, the transcriptional repression was attenuated through inhibition of RNA degradation.Even though the level of total mRNA dramatically decreased in the dark, Synechococcus cells were still viable, and they do not need de novo transcription for their survival in the dark for at least 48 hours.

View Article: PubMed Central - PubMed

Affiliation: Department of Electrical Engineering and Biological Science, Waseda University, TWIns, Shinjuku, Tokyo, 162-8480, Japan. sou.tacano@gmail.com.

ABSTRACT

Background: Most organisms, especially photoautotrophs, alter their behaviours in response to day-night alternations adaptively because of their great reliance on light. Upon light-to-dark transition, dramatic and universal decreases in transcription level of the majority of the genes in the genome of the unicellular cyanobacterium, Synechococcus elongatus PCC 7942 are observed. Because Synechococcus is an obligate photoautotroph, it has been generally assumed that repression of the transcription in the dark (dark repression) would be caused by a nocturnal decrease in photosynthetic activities through the reduced availability of energy (e.g. adenosine triphosphate (ATP)) needed for mRNA synthesis.

Results: However, against this general assumption, we obtained evidence that the rapid and dynamic dark repression is an active process. Although the addition of photosynthesis inhibitors to cells exposed to light mimicked transcription profiles in the dark, it did not significantly affect the cellular level of ATP. By contrast, when ATP levels were decreased by the inhibition of both photosynthesis and respiration, the transcriptional repression was attenuated through inhibition of RNA degradation. This observation indicates that Synechococcus actively downregulates genome-wide transcription in the dark. Even though the level of total mRNA dramatically decreased in the dark, Synechococcus cells were still viable, and they do not need de novo transcription for their survival in the dark for at least 48 hours.

Conclusions: Dark repression appears to enable cells to enter into nocturnal dormancy as a feed-forward process, which would be advantageous for their survival under periodic nocturnal conditions.

No MeSH data available.


Related in: MedlinePlus