Dataset Information

Spatial organization of bacterial transcription and translation.

ABSTRACT: In bacteria such as Escherichia coli, DNA is compacted into a nucleoid near the cell center, whereas ribosomes-molecular complexes that translate mRNAs into proteins-are mainly localized to the poles. We study the impact of this spatial organization using a minimal reaction-diffusion model for the cellular transcriptional-translational machinery. Although genome-wide mRNA-nucleoid segregation still lacks experimental validation, our model predicts that [Formula: see text] of mRNAs are segregated to the poles. In addition, our analysis reveals a "circulation" of ribosomes driven by the flux of mRNAs, from synthesis in the nucleoid to degradation at the poles. We show that our results are robust with respect to multiple, biologically relevant factors, such as mRNA degradation by RNase enzymes, different phases of the cell division cycle and growth rates, and the existence of nonspecific, transient interactions between ribosomes and mRNAs. Finally, we confirm that the observed nucleoid size stems from a balance between the forces that the chromosome and mRNAs exert on each other. This suggests a potential global feedback circuit in which gene expression feeds back on itself via nucleoid compaction.

SUBMITTER: Castellana M

PROVIDER: S-EPMC4995950 | biostudies-literature | 2016 Aug

REPOSITORIES: biostudies-literature

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Publications

Spatial organization of bacterial transcription and translation.

Castellana Michele M Hsin-Jung Li Sophia S Wingreen Ned S NS

Proceedings of the National Academy of Sciences of the United States of America 20160802 33

In bacteria such as Escherichia coli, DNA is compacted into a nucleoid near the cell center, whereas ribosomes-molecular complexes that translate mRNAs into proteins-are mainly localized to the poles. We study the impact of this spatial organization using a minimal reaction-diffusion model for the cellular transcriptional-translational machinery. Although genome-wide mRNA-nucleoid segregation still lacks experimental validation, our model predicts that [Formula: see text] of mRNAs are segregated ...[more]

PMID: 27486246

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Project description:Spatial organization of the transcriptome has emerged as a powerful means for regulating the post-transcriptional fate of RNA in eukaryotes; however, whether prokaryotes use RNA spatial organization as a mechanism for post-transcriptional regulation remains unclear. Here we used super-resolution microscopy to image the E. coli transcriptome and observed a genome-wide spatial organization of RNA: mRNAs encoding inner-membrane proteins are enriched at the membrane, whereas mRNAs encoding outer-membrane, cytoplasmic and periplasmic proteins are distributed throughout the cytoplasm. Membrane enrichment is caused by co-translational insertion of signal peptides recognized by the signal-recognition particle. Our time-resolved RNA-sequencing and live-cell super-resolution imaging experiments revealed a physiological consequence of this spatial organization and the underlying mechanism: membrane localization enhances degradation rates of inner-membrane-protein mRNAs by placing them in proximity to membrane-bound RNA degradation enzymes. Together, these results demonstrate that the bacterial transcriptome is spatially organized and that this organization shapes the posttranscriptional Spatial organization of the transcriptome has emerged as a powerful means for regulating the post-transcriptional fate of RNA in eukaryotes; however, whether prokaryotes use RNA spatial organization as a mechanism for post-transcriptional regulation remains unclear. Here we used super-resolution microscopy to image the E. coli transcriptome and observed a genome-wide spatial organization of RNA: mRNAs encoding inner-membrane proteins are enriched at the membrane, whereas mRNAs encoding outer-membrane, cytoplasmic and periplasmic proteins are distributed throughout the cytoplasm. Membrane enrichment is caused by co-translational insertion of signal peptides recognized by the signal-recognition particle. Our time-resolved RNA-sequencing and live-cell super-resolution imaging experiments revealed a physiological consequence of this spatial organization and the underlying mechanism: membrane localization enhances degradation rates of inner-membrane-protein mRNAs by placing them in proximity to membrane-bound RNA degradation enzymes. Together, these results demonstrate that the bacterial transcriptome is spatially organized and that this organization shapes the post-transcriptional dynamics of mRNAs.

Dataset Information

Spatial organization of bacterial transcription and translation.

Publications

Spatial organization of bacterial transcription and translation.

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