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Spatial organization shapes the turnover of a bacterial transcriptome
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 mic...
Autores principales: | , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
eLife Sciences Publications, Ltd
2016
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4874777/ https://www.ncbi.nlm.nih.gov/pubmed/27198188 http://dx.doi.org/10.7554/eLife.13065 |
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author | Moffitt, Jeffrey R Pandey, Shristi Boettiger, Alistair N Wang, Siyuan Zhuang, Xiaowei |
author_facet | Moffitt, Jeffrey R Pandey, Shristi Boettiger, Alistair N Wang, Siyuan Zhuang, Xiaowei |
author_sort | Moffitt, Jeffrey R |
collection | PubMed |
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. Time-resolved RNA-sequencing revealed that degradation rates of inner-membrane-protein mRNAs are on average greater that those of the other mRNAs and that this selective destabilization of inner-membrane-protein mRNAs is abolished by dissociating the RNA degradosome from the membrane. Together, these results demonstrate that the bacterial transcriptome is spatially organized and suggest that this organization shapes the post-transcriptional dynamics of mRNAs. DOI: http://dx.doi.org/10.7554/eLife.13065.001 |
format | Online Article Text |
id | pubmed-4874777 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2016 |
publisher | eLife Sciences Publications, Ltd |
record_format | MEDLINE/PubMed |
spelling | pubmed-48747772016-05-23 Spatial organization shapes the turnover of a bacterial transcriptome Moffitt, Jeffrey R Pandey, Shristi Boettiger, Alistair N Wang, Siyuan Zhuang, Xiaowei eLife Biophysics and Structural Biology 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. Time-resolved RNA-sequencing revealed that degradation rates of inner-membrane-protein mRNAs are on average greater that those of the other mRNAs and that this selective destabilization of inner-membrane-protein mRNAs is abolished by dissociating the RNA degradosome from the membrane. Together, these results demonstrate that the bacterial transcriptome is spatially organized and suggest that this organization shapes the post-transcriptional dynamics of mRNAs. DOI: http://dx.doi.org/10.7554/eLife.13065.001 eLife Sciences Publications, Ltd 2016-05-20 /pmc/articles/PMC4874777/ /pubmed/27198188 http://dx.doi.org/10.7554/eLife.13065 Text en © 2016, Moffitt et al http://creativecommons.org/licenses/by/4.0/ This article is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited. |
spellingShingle | Biophysics and Structural Biology Moffitt, Jeffrey R Pandey, Shristi Boettiger, Alistair N Wang, Siyuan Zhuang, Xiaowei Spatial organization shapes the turnover of a bacterial transcriptome |
title | Spatial organization shapes the turnover of a bacterial transcriptome |
title_full | Spatial organization shapes the turnover of a bacterial transcriptome |
title_fullStr | Spatial organization shapes the turnover of a bacterial transcriptome |
title_full_unstemmed | Spatial organization shapes the turnover of a bacterial transcriptome |
title_short | Spatial organization shapes the turnover of a bacterial transcriptome |
title_sort | spatial organization shapes the turnover of a bacterial transcriptome |
topic | Biophysics and Structural Biology |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4874777/ https://www.ncbi.nlm.nih.gov/pubmed/27198188 http://dx.doi.org/10.7554/eLife.13065 |
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