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      Choreography of the Transcriptome, Photophysiology, and Cell Cycle of a Minimal Photoautotroph, Prochlorococcus

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          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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          Most cited references127

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          Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing

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            Emergent biogeography of microbial communities in a model ocean.

            A marine ecosystem model seeded with many phytoplankton types, whose physiological traits were randomly assigned from ranges defined by field and laboratory data, generated an emergent community structure and biogeography consistent with observed global phytoplankton distributions. The modeled organisms included types analogous to the marine cyanobacterium Prochlorococcus. Their emergent global distributions and physiological properties simultaneously correspond to observations. This flexible representation of community structure can be used to explore relations between ecosystems, biogeochemical cycles, and climate change.
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              Microbial community gene expression in ocean surface waters.

              Metagenomics is expanding our knowledge of the gene content, functional significance, and genetic variability in natural microbial communities. Still, there exists limited information concerning the regulation and dynamics of genes in the environment. We report here global analysis of expressed genes in a naturally occurring microbial community. We first adapted RNA amplification technologies to produce large amounts of cDNA from small quantities of total microbial community RNA. The fidelity of the RNA amplification procedure was validated with Prochlorococcus cultures and then applied to a microbial assemblage collected in the oligotrophic Pacific Ocean. Microbial community cDNAs were analyzed by pyrosequencing and compared with microbial community genomic DNA sequences determined from the same sample. Pyrosequencing-based estimates of microbial community gene expression compared favorably to independent assessments of individual gene expression using quantitative PCR. Genes associated with key metabolic pathways in open ocean microbial species-including genes involved in photosynthesis, carbon fixation, and nitrogen acquisition-and a number of genes encoding hypothetical proteins were highly represented in the cDNA pool. Genes present in the variable regions of Prochlorococcus genomes were among the most highly expressed, suggesting these encode proteins central to cellular processes in specific genotypes. Although many transcripts detected were highly similar to genes previously detected in ocean metagenomic surveys, a significant fraction ( approximately 50%) were unique. Thus, microbial community transcriptomic analyses revealed not only indigenous gene- and taxon-specific expression patterns but also gene categories undetected in previous DNA-based metagenomic surveys.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2009
                8 April 2009
                : 4
                : 4
                : e5135
                Affiliations
                [1 ]Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge, Massachusetts, United States of America
                [2 ]Department of Microbiology, University of Tennessee, Knoxville, Tennessee, United States of America
                [3 ]Faculty of Biology, Technion-Israel Institute of Technology, Haifa, Israel
                [4 ]Department of Oceanography, University of Hawaii, Honolulu, Hawaii, United States of America
                [5 ]Institute of Theoretical Biology, Humboldt University, Berlin, Germany
                [6 ]Center for Molecular and Structural Biomedicine, University of Algarve, Faro, Portugal
                [7 ]Institute of Biology III, University of Freiburg, Freiburg, Germany
                [8 ]Department of Genetics, Harvard Medical School, Boston, Massachusetts, United States of America
                [9 ]Department of Biology, Massachusetts Institute of Technology, Cambridge, Massachusetts, United States of America
                Universidad Miguel Hernandez, Spain
                Author notes

                Conceived and designed the experiments: ERZ DL ZJ SWC. Performed the experiments: ERZ DL ZJ CS MC NM. Analyzed the data: ERZ DL ZJ MEF CS MC LRT SWC. Contributed reagents/materials/analysis tools: MEF MC MAW TR RS SWC. Wrote the paper: ERZ DL ZJ MEF CS MC LRT SWC.

                Article
                08-PONE-RA-07909
                10.1371/journal.pone.0005135
                2663038
                19352512
                39fdc0fb-2fec-4733-845f-e293b3a8152c
                Zinser et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                History
                : 23 December 2008
                : 19 January 2009
                Page count
                Pages: 18
                Categories
                Research Article
                Computational Biology/Genomics
                Ecology/Marine and Freshwater Ecology
                Genetics and Genomics/Gene Expression
                Microbiology/Microbial Evolution and Genomics
                Microbiology/Microbial Physiology and Metabolism
                Computational Biology/Genomics
                Computational Biology/Systems Biology
                Computational Biology/Transcriptional Regulation
                Ecology/Marine and Freshwater Ecology
                Ecology/Physiological Ecology
                Genetics and Genomics/Microbial Evolution and Genomics
                Microbiology/Microbial Evolution and Genomics
                Microbiology/Microbial Growth and Development
                Microbiology/Microbial Physiology and Metabolism

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                Uncategorized

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