Choreography of the transcriptome, photophysiology, and cell cycle of a minimal photoautotroph, prochlorococcus
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 cel...
| Main Authors: | , , , , , , , , , , , |
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| Format: | Article |
| Language: | en_US |
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Public Library of Science
2010
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| Online Access: | http://hdl.handle.net/1721.1/52447 |
| _version_ | 1826189619541049344 |
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| author | Zinser, Erik R. Lindell, Debbie Johnson, Zackary I. Futschik, Matthias Steglich, Claudia Wright, Matthew A. Rector, Trent Steen, Robert McNulty, Nathan Thompson, Luke Richard Chisholm, Sallie (Penny) Coleman, Maureen L |
| author2 | Massachusetts Institute of Technology. Department of Biology |
| author_facet | Massachusetts Institute of Technology. Department of Biology Zinser, Erik R. Lindell, Debbie Johnson, Zackary I. Futschik, Matthias Steglich, Claudia Wright, Matthew A. Rector, Trent Steen, Robert McNulty, Nathan Thompson, Luke Richard Chisholm, Sallie (Penny) Coleman, Maureen L |
| author_sort | Zinser, Erik R. |
| collection | MIT |
| description | 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. |
| first_indexed | 2024-09-23T08:18:29Z |
| format | Article |
| id | mit-1721.1/52446 |
| institution | Massachusetts Institute of Technology |
| language | en_US |
| last_indexed | 2024-09-23T08:18:29Z |
| publishDate | 2010 |
| publisher | Public Library of Science |
| record_format | dspace |
| spelling | mit-1721.1/524462022-09-30T08:54:51Z Choreography of the transcriptome, photophysiology, and cell cycle of a minimal photoautotroph, prochlorococcus Zinser, Erik R. Lindell, Debbie Johnson, Zackary I. Futschik, Matthias Steglich, Claudia Wright, Matthew A. Rector, Trent Steen, Robert McNulty, Nathan Thompson, Luke Richard Chisholm, Sallie (Penny) Coleman, Maureen L Massachusetts Institute of Technology. Department of Biology Massachusetts Institute of Technology. Department of Civil and Environmental Engineering Chisholm, Sallie (Penny) Zinser, Erik R. Lindell, Debbie Johnson, Zackary I. Steglich, Claudia Coleman, Maureen L. McNulty, Nathan Thompson, Luke Richard Chisholm, Sallie (Penny) 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. 2010-03-09T21:02:32Z 2010-03-09T21:02:32Z 2009-04 2008-12 Article http://purl.org/eprint/type/JournalArticle 1932-6203 http://hdl.handle.net/1721.1/52447 Zinser ER, Lindell D, Johnson ZI, Futschik ME, Steglich C, et al. (2009) Choreography of the Transcriptome, Photophysiology, and Cell Cycle of a Minimal Photoautotroph, Prochlorococcus. PLoS ONE 4(4): e5135. doi:10.1371/journal.pone.0005135 19352512 en_US http://dx.doi.org/10.1371/journal.pone.0005135 PLoS ONE Creative Commons Attribution http://creativecommons.org/licenses/by/2.5/ application/pdf Public Library of Science PLoS |
| spellingShingle | Zinser, Erik R. Lindell, Debbie Johnson, Zackary I. Futschik, Matthias Steglich, Claudia Wright, Matthew A. Rector, Trent Steen, Robert McNulty, Nathan Thompson, Luke Richard Chisholm, Sallie (Penny) Coleman, Maureen L Choreography of the transcriptome, photophysiology, and cell cycle of a minimal photoautotroph, prochlorococcus |
| title | Choreography of the transcriptome, photophysiology, and cell cycle of a minimal photoautotroph, prochlorococcus |
| title_full | Choreography of the transcriptome, photophysiology, and cell cycle of a minimal photoautotroph, prochlorococcus |
| title_fullStr | Choreography of the transcriptome, photophysiology, and cell cycle of a minimal photoautotroph, prochlorococcus |
| title_full_unstemmed | Choreography of the transcriptome, photophysiology, and cell cycle of a minimal photoautotroph, prochlorococcus |
| title_short | Choreography of the transcriptome, photophysiology, and cell cycle of a minimal photoautotroph, prochlorococcus |
| title_sort | choreography of the transcriptome photophysiology and cell cycle of a minimal photoautotroph prochlorococcus |
| url | http://hdl.handle.net/1721.1/52447 |
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