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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...

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Autores principales: Moffitt, Jeffrey R, Pandey, Shristi, Boettiger, Alistair N, Wang, Siyuan, Zhuang, Xiaowei
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2016
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
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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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