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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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Relative RMA-normalized expression levels of all annotated open reading frames in MED4 over a two-day diel.Relative PAR (photosynthetically available radiation) over the experiment is represented above the expression patterns. Each line represents one of the 1698 unique open reading frames (line colors are arbitrary). Vertical dotted lines denote light/dark transitions.
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pone-0005135-g001: Relative RMA-normalized expression levels of all annotated open reading frames in MED4 over a two-day diel.Relative PAR (photosynthetically available radiation) over the experiment is represented above the expression patterns. Each line represents one of the 1698 unique open reading frames (line colors are arbitrary). Vertical dotted lines denote light/dark transitions.

Mentions: Prochlorococcus strain MED4, a member of the high-light adapted clade of Prochlorococcus that dominates surface waters over much of the mid-latitude oceans [26] was used for this study. It has one of the smallest genomes of all cultured Prochlorococcus strains, synchronizes tightly to a light dark cycle, and can achieve a growth rate of one doubling per day under optimal conditions. The doubling times of the replicate cultures used in this study were 1.1 and 1.0 days, and thus the cells within the population progressed through the cell cycle in synchrony. The important consequence is that our population-level measurements of gene expression and cell physiology approximate what is happening in an individual cell. As a result, the periodicity in the global transcriptome was very well defined and reproducible over both days of sampling in both of the replicate cultures (Figure 1, and see Table S1 for expression data), forming a solid database for all of our analyses.


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)

Relative RMA-normalized expression levels of all annotated open reading frames in MED4 over a two-day diel.Relative PAR (photosynthetically available radiation) over the experiment is represented above the expression patterns. Each line represents one of the 1698 unique open reading frames (line colors are arbitrary). Vertical dotted lines denote light/dark transitions.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0005135-g001: Relative RMA-normalized expression levels of all annotated open reading frames in MED4 over a two-day diel.Relative PAR (photosynthetically available radiation) over the experiment is represented above the expression patterns. Each line represents one of the 1698 unique open reading frames (line colors are arbitrary). Vertical dotted lines denote light/dark transitions.
Mentions: Prochlorococcus strain MED4, a member of the high-light adapted clade of Prochlorococcus that dominates surface waters over much of the mid-latitude oceans [26] was used for this study. It has one of the smallest genomes of all cultured Prochlorococcus strains, synchronizes tightly to a light dark cycle, and can achieve a growth rate of one doubling per day under optimal conditions. The doubling times of the replicate cultures used in this study were 1.1 and 1.0 days, and thus the cells within the population progressed through the cell cycle in synchrony. The important consequence is that our population-level measurements of gene expression and cell physiology approximate what is happening in an individual cell. As a result, the periodicity in the global transcriptome was very well defined and reproducible over both days of sampling in both of the replicate cultures (Figure 1, and see Table S1 for expression data), forming a solid database for all of our analyses.

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