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Choreography of the transcriptome, photophysiology, and cell cycle of a minimal photoautotroph, prochlorococcus.

Zinser ER, Lindell D, Johnson ZI, Futschik ME, Steglich C, Coleman ML, Wright MA, Rector T, Steen R, McNulty N, Thompson LR, Chisholm SW - PLoS ONE (2009)

Bottom Line: Furthermore, the transitions between photosynthesis during the day and catabolic consumption of energy reserves at night- metabolic processes that share some of the same enzymes--appear to be tightly choreographed at the level of RNA expression.In-depth investigation of these patterns identified potential regulatory proteins involved in balancing these opposing pathways.Finally, while this analysis has not helped resolve how a cell with so little regulatory capacity, and a 'deficient' circadian mechanism, aligns its cell cycle and metabolism so tightly to a light-dark cycle, it does provide us with a valuable framework upon which to build when the Prochlorococcus proteome and metabolome become available.

View Article: PubMed Central - PubMed

Affiliation: Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge, Massachusetts, United States of America.

ABSTRACT
The marine cyanobacterium Prochlorococcus MED4 has the smallest genome and cell size of all known photosynthetic organisms. Like all phototrophs at temperate latitudes, it experiences predictable daily variation in available light energy which leads to temporal regulation and partitioning of key cellular processes. To better understand the tempo and choreography of this minimal phototroph, we studied the entire transcriptome of the cell over a simulated daily light-dark cycle, and placed it in the context of diagnostic physiological and cell cycle parameters. All cells in the culture progressed through their cell cycles in synchrony, thus ensuring that our measurements reflected the behavior of individual cells. Ninety percent of the annotated genes were expressed, and 80% had cyclic expression over the diel cycle. For most genes, expression peaked near sunrise or sunset, although more subtle phasing of gene expression was also evident. Periodicities of the transcripts of genes involved in physiological processes such as in cell cycle progression, photosynthesis, and phosphorus metabolism tracked the timing of these activities relative to the light-dark cycle. Furthermore, the transitions between photosynthesis during the day and catabolic consumption of energy reserves at night- metabolic processes that share some of the same enzymes--appear to be tightly choreographed at the level of RNA expression. In-depth investigation of these patterns identified potential regulatory proteins involved in balancing these opposing pathways. Finally, while this analysis has not helped resolve how a cell with so little regulatory capacity, and a 'deficient' circadian mechanism, aligns its cell cycle and metabolism so tightly to a light-dark cycle, it does provide us with a valuable framework upon which to build when the Prochlorococcus proteome and metabolome become available.

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Related in: MedlinePlus

Expression time course of regulatory proteins.(A) Circadian clock genes kaiB and kaiC, and clock output genes rpaA and cpmA; (B) Sigma factor genes PMM0496 (rpoD), PMM0577, PMM1289, PMM1629, and PMM1697; and (C) cbbR, and representative Calvin cycle genes rbcL, csoS3, and fbaA are shown. Error bars represent one standard deviation of the mean for the replicate cultures.
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pone-0005135-g008: Expression time course of regulatory proteins.(A) Circadian clock genes kaiB and kaiC, and clock output genes rpaA and cpmA; (B) Sigma factor genes PMM0496 (rpoD), PMM0577, PMM1289, PMM1629, and PMM1697; and (C) cbbR, and representative Calvin cycle genes rbcL, csoS3, and fbaA are shown. Error bars represent one standard deviation of the mean for the replicate cultures.

Mentions: The kaiB clock gene of MED4 exhibited strong diel periodicity in our experiment, with a maximum at dawn and a minimum at sunset (Figure 8A). kaiC showed low, albeit significant diel periodicity, peaking near the onset of darkness. While the kaiB pattern resembles that reported by Holtzendorff et al. (2008) for Prochlorococcus PCC 9511, the kaiC pattern is just the opposite: they found that kaiC peaked at dawn, in phase with kaiB (albeit with a small secondary peak just after dark, in phase with the peak we observed). This difference is puzzling. At this time, we can only add that we found the same weak periodicity of kaiC— with a small peak after the onset of darkness — in our Pilot Study (see methods) using quantitative reverse transcription PCR (Figure S3), as was observed in our study with the arrays.


Choreography of the transcriptome, photophysiology, and cell cycle of a minimal photoautotroph, prochlorococcus.

Zinser ER, Lindell D, Johnson ZI, Futschik ME, Steglich C, Coleman ML, Wright MA, Rector T, Steen R, McNulty N, Thompson LR, Chisholm SW - PLoS ONE (2009)

Expression time course of regulatory proteins.(A) Circadian clock genes kaiB and kaiC, and clock output genes rpaA and cpmA; (B) Sigma factor genes PMM0496 (rpoD), PMM0577, PMM1289, PMM1629, and PMM1697; and (C) cbbR, and representative Calvin cycle genes rbcL, csoS3, and fbaA are shown. Error bars represent one standard deviation of the mean for the replicate cultures.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2663038&req=5

pone-0005135-g008: Expression time course of regulatory proteins.(A) Circadian clock genes kaiB and kaiC, and clock output genes rpaA and cpmA; (B) Sigma factor genes PMM0496 (rpoD), PMM0577, PMM1289, PMM1629, and PMM1697; and (C) cbbR, and representative Calvin cycle genes rbcL, csoS3, and fbaA are shown. Error bars represent one standard deviation of the mean for the replicate cultures.
Mentions: The kaiB clock gene of MED4 exhibited strong diel periodicity in our experiment, with a maximum at dawn and a minimum at sunset (Figure 8A). kaiC showed low, albeit significant diel periodicity, peaking near the onset of darkness. While the kaiB pattern resembles that reported by Holtzendorff et al. (2008) for Prochlorococcus PCC 9511, the kaiC pattern is just the opposite: they found that kaiC peaked at dawn, in phase with kaiB (albeit with a small secondary peak just after dark, in phase with the peak we observed). This difference is puzzling. At this time, we can only add that we found the same weak periodicity of kaiC— with a small peak after the onset of darkness — in our Pilot Study (see methods) using quantitative reverse transcription PCR (Figure S3), as was observed in our study with the arrays.

Bottom Line: Furthermore, the transitions between photosynthesis during the day and catabolic consumption of energy reserves at night- metabolic processes that share some of the same enzymes--appear to be tightly choreographed at the level of RNA expression.In-depth investigation of these patterns identified potential regulatory proteins involved in balancing these opposing pathways.Finally, while this analysis has not helped resolve how a cell with so little regulatory capacity, and a 'deficient' circadian mechanism, aligns its cell cycle and metabolism so tightly to a light-dark cycle, it does provide us with a valuable framework upon which to build when the Prochlorococcus proteome and metabolome become available.

View Article: PubMed Central - PubMed

Affiliation: Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge, Massachusetts, United States of America.

ABSTRACT
The marine cyanobacterium Prochlorococcus MED4 has the smallest genome and cell size of all known photosynthetic organisms. Like all phototrophs at temperate latitudes, it experiences predictable daily variation in available light energy which leads to temporal regulation and partitioning of key cellular processes. To better understand the tempo and choreography of this minimal phototroph, we studied the entire transcriptome of the cell over a simulated daily light-dark cycle, and placed it in the context of diagnostic physiological and cell cycle parameters. All cells in the culture progressed through their cell cycles in synchrony, thus ensuring that our measurements reflected the behavior of individual cells. Ninety percent of the annotated genes were expressed, and 80% had cyclic expression over the diel cycle. For most genes, expression peaked near sunrise or sunset, although more subtle phasing of gene expression was also evident. Periodicities of the transcripts of genes involved in physiological processes such as in cell cycle progression, photosynthesis, and phosphorus metabolism tracked the timing of these activities relative to the light-dark cycle. Furthermore, the transitions between photosynthesis during the day and catabolic consumption of energy reserves at night- metabolic processes that share some of the same enzymes--appear to be tightly choreographed at the level of RNA expression. In-depth investigation of these patterns identified potential regulatory proteins involved in balancing these opposing pathways. Finally, while this analysis has not helped resolve how a cell with so little regulatory capacity, and a 'deficient' circadian mechanism, aligns its cell cycle and metabolism so tightly to a light-dark cycle, it does provide us with a valuable framework upon which to build when the Prochlorococcus proteome and metabolome become available.

Show MeSH
Related in: MedlinePlus