Dataset Information

Transcriptional regulation shapes the organization of genes on bacterial chromosomes.

ABSTRACT: Transcription factors (TFs) are the key elements responsible for controlling the expression of genes in bacterial genomes and when visualized on a genomic scale form a dense network of transcriptional interactions among themselves and with other protein coding genes. Although the structure of transcriptional regulatory networks (TRNs) is well understood, it is not clear what constrains govern them. Here, we explore this question using the TRNs of model prokaryotes and provide a link between the transcriptional hierarchy of regulons and their genome organization. We show that, to drive the kinetics and concentration gradients, TFs belonging to big and small regulons, depending on the number of genes they regulate, organize themselves differently on the genome with respect to their targets. We then propose a conceptual model that can explain how the hierarchical structure of TRNs might be ultimately governed by the dynamic biophysical requirements for targeting DNA-binding sites by TFs. Our results suggest that the main parameters defining the position of a TF in the network hierarchy are the number and chromosomal distances of the genes they regulate and their protein concentration gradients. These observations give insights into how the hierarchical structure of transcriptional networks can be encoded on the chromosome to drive the kinetics and concentration gradients of TFs depending on the number of genes they regulate and could be a common theme valid for other prokaryotes, proposing the role of transcriptional regulation in shaping the organization of genes on a chromosome.

SUBMITTER: Janga SC

PROVIDER: S-EPMC2699516 | biostudies-literature | 2009 Jun

REPOSITORIES: biostudies-literature

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Transcriptional regulation shapes the organization of genes on bacterial chromosomes.

Janga Sarath Chandra SC Salgado Heladia H Martínez-Antonio Agustino A

Nucleic acids research 20090416 11

Transcription factors (TFs) are the key elements responsible for controlling the expression of genes in bacterial genomes and when visualized on a genomic scale form a dense network of transcriptional interactions among themselves and with other protein coding genes. Although the structure of transcriptional regulatory networks (TRNs) is well understood, it is not clear what constrains govern them. Here, we explore this question using the TRNs of model prokaryotes and provide a link between the ...[more]

PMID: 19372274

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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

Transcriptional regulation shapes the organization of genes on bacterial chromosomes.

Publications

Transcriptional regulation shapes the organization of genes on bacterial chromosomes.

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