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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

Genome-widely attenuated dark repression and induction by inhibition of ATP synthesis. a Organisation of expression profiles in the light, in the dark without inhibitor, or in the dark treated with DBMIB alone or both DBMIB and rifampicin. Data representation is consistent with that in Fig. 1b. b Total mRNA accumulation levels at each condition. Data representation is consistent with that in Fig. 1c. c Plot of PCA scores. Data representation is consistent with that in Fig. 1d. We obtained the data for panels a to c from independent duplicate experiments DBMIB 2,5-dibromo-3-methyl-6-isopropylbenzoquinone, PCA principal component analysis
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Fig3: Genome-widely attenuated dark repression and induction by inhibition of ATP synthesis. a Organisation of expression profiles in the light, in the dark without inhibitor, or in the dark treated with DBMIB alone or both DBMIB and rifampicin. Data representation is consistent with that in Fig. 1b. b Total mRNA accumulation levels at each condition. Data representation is consistent with that in Fig. 1c. c Plot of PCA scores. Data representation is consistent with that in Fig. 1d. We obtained the data for panels a to c from independent duplicate experiments DBMIB 2,5-dibromo-3-methyl-6-isopropylbenzoquinone, PCA principal component analysis

Mentions: Figure 3a–c shows consistent attenuation of the dark-dependent expression profile of the entire genome. mRNA abundance was reduced to about 50 % upon the dark transition, while in the presence of DBMIB about 80 % of mRNA remained (Fig. 3b). Therefore, DBMIB treatment inhibited about 60 % of dark-dependent mRNA suppression. Figure 3c shows PCA expression profiles, in which PC1 and PC2 account for 69 % and 19 % of the variance of expression data, respectively. As is shown in Fig. 1d, the difference between the illuminated and dark-acclimated samples is represented largely in PC1, and the contribution of PC1 is much higher than the second principal component. The samples incubated in the dark in the presence of DBMIB lay in a position between the illuminated samples and the dark-incubated samples. Scatter plots shown in Additional file 5: Figure S4B show a similar tendency for samples incubated in the dark in the presence of DBMIB, which show a relatively high correlation with the illuminated samples, while the sample incubated in the dark without the inhibitor and the illuminated samples shows a lower correlation (see Additional file 5: Figure S4B). We conducted a Mulcom test on the samples, which led us to a similar conclusion. DBMIB significantly attenuated the dark-dependency of 1,111 among 1,844 dark-regulated genes (see Additional file 6: Figure S5B). Interestingly, therefore, DBMIB inhibited about 60 % of both reduction in the total mRNA amount and dark-regulated genes. The similar effects of the treatment with DBMIB or KCN under dark conditions suggest that the DBMIB-derived de-repression of the dark-induced transcriptional profiles is primarily because of ATP shortage (because of the inhibition of respiration) in the dark. In other words, the dramatic transcriptional shift upon light-to-dark transition seems to require a certain level of ATP, and the maintenance of ATP availability in the dark appears essential for nocturnal transcription profiles.Fig. 3


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

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

Genome-widely attenuated dark repression and induction by inhibition of ATP synthesis. a Organisation of expression profiles in the light, in the dark without inhibitor, or in the dark treated with DBMIB alone or both DBMIB and rifampicin. Data representation is consistent with that in Fig. 1b. b Total mRNA accumulation levels at each condition. Data representation is consistent with that in Fig. 1c. c Plot of PCA scores. Data representation is consistent with that in Fig. 1d. We obtained the data for panels a to c from independent duplicate experiments DBMIB 2,5-dibromo-3-methyl-6-isopropylbenzoquinone, PCA principal component analysis
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4494158&req=5

Fig3: Genome-widely attenuated dark repression and induction by inhibition of ATP synthesis. a Organisation of expression profiles in the light, in the dark without inhibitor, or in the dark treated with DBMIB alone or both DBMIB and rifampicin. Data representation is consistent with that in Fig. 1b. b Total mRNA accumulation levels at each condition. Data representation is consistent with that in Fig. 1c. c Plot of PCA scores. Data representation is consistent with that in Fig. 1d. We obtained the data for panels a to c from independent duplicate experiments DBMIB 2,5-dibromo-3-methyl-6-isopropylbenzoquinone, PCA principal component analysis
Mentions: Figure 3a–c shows consistent attenuation of the dark-dependent expression profile of the entire genome. mRNA abundance was reduced to about 50 % upon the dark transition, while in the presence of DBMIB about 80 % of mRNA remained (Fig. 3b). Therefore, DBMIB treatment inhibited about 60 % of dark-dependent mRNA suppression. Figure 3c shows PCA expression profiles, in which PC1 and PC2 account for 69 % and 19 % of the variance of expression data, respectively. As is shown in Fig. 1d, the difference between the illuminated and dark-acclimated samples is represented largely in PC1, and the contribution of PC1 is much higher than the second principal component. The samples incubated in the dark in the presence of DBMIB lay in a position between the illuminated samples and the dark-incubated samples. Scatter plots shown in Additional file 5: Figure S4B show a similar tendency for samples incubated in the dark in the presence of DBMIB, which show a relatively high correlation with the illuminated samples, while the sample incubated in the dark without the inhibitor and the illuminated samples shows a lower correlation (see Additional file 5: Figure S4B). We conducted a Mulcom test on the samples, which led us to a similar conclusion. DBMIB significantly attenuated the dark-dependency of 1,111 among 1,844 dark-regulated genes (see Additional file 6: Figure S5B). Interestingly, therefore, DBMIB inhibited about 60 % of both reduction in the total mRNA amount and dark-regulated genes. The similar effects of the treatment with DBMIB or KCN under dark conditions suggest that the DBMIB-derived de-repression of the dark-induced transcriptional profiles is primarily because of ATP shortage (because of the inhibition of respiration) in the dark. In other words, the dramatic transcriptional shift upon light-to-dark transition seems to require a certain level of ATP, and the maintenance of ATP availability in the dark appears essential for nocturnal transcription profiles.Fig. 3

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