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Spatial and genetic constraints govern transcription-translation coupling and mRNA degradation in bacteria

ABSTRACT: Bacterial gene expression is thought to involve tightly coupled transcription, translation, and mRNA degradation. However, recent work has indicated that this is not always the case, leaving the generality and regulation of this coordination unclear. Here, we use genetic, kinetic, and spatial analyses in Escherichia coli to show that transcription–translation coupling requires high translational activity and that nearly half of the transcriptome exhibits signatures consistent with partial uncoupling. We find that co-transcriptional mRNA degradation is rare due to membrane localization of RNase E, except for transcripts encoding inner membrane proteins. Our results show that translation efficiency determines the level of premature transcription termination, which in turn shapes mRNA degradation patterns and kinetics. Comparative analyses in Bacillus subtilis and Caulobacter crescentus also reveal gene- and species-specific coordination strategies. This challenges the universality of co-transcriptional coupling and defines how spatial and genetic features coordinate bacterial gene expression.

ORGANISM(S): Escherichia coli str. K-12 substr. MG1655

PROVIDER: GSE298132 | GEO | 2026/04/16

REPOSITORIES: GEO

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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.

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Spatial and genetic constraints govern transcription-translation coupling and mRNA degradation in bacteria

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