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MinD-RNase E interplay controls localization of polar mRNAs in E. coli

ABSTRACT: We have recently shown that the polar transcriptome of E. coli is unique compared to the membrane and cytosolic ones. Several factors were suggested to mediate mRNA localization to the membrane, but the mechanism of localizing mRNAs to the poles is not known. We combined a candidate system approach with high-throughput proteomics to identify factors that mediate polar mRNAs localization. We identified MinD as an essential factor in this process, whose binding to RNAs is indirect. We demonstrate that RNase E, previously shown to interact with MinD, is also required for proper localization of polar mRNAs. Using in silico modeling followed by experimental validation, the membrane-binding site in RNase E was found to mediate binding to MinD. Intriguingly, not only does MinD affect RNase E interaction with the membrane, but it also affects its mode of action and dynamics. Polar accumulation of RNase E in ΔminCDE cells resulted in destabilization and depletion of mRNAs from the poles. Finally, we show that mislocalization of polar mRNAs may prevent polar localization of their protein products. Taken together, MinD and RNase E are assigned novel roles, whereas the interplay between them determines the composition of the polar transcriptome, thus affecting the polar proteome.

INSTRUMENT(S): Q Exactive Plus

ORGANISM(S): Escherichia Coli

SUBMITTER: Tamar Geiger

LAB HEAD: Tamar Geiger

PROVIDER: PXD044814 | Pride | 2023-12-17

REPOSITORIES: Pride

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			Action	DRS
	Animal_20161006_GB_collab_priya_6xbs_mini1.raw	Raw
	Animal_20161006_GB_collab_priya_6xbs_mini2.raw	Raw
	Animal_20161006_GB_collab_priya_6xbs_mini3.raw	Raw
	Animal_20161006_GB_collab_priya_bglG_mini1.raw	Raw
	Animal_20161006_GB_collab_priya_bglG_mini2.raw	Raw

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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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MinD-RNase E interplay controls localization of polar mRNAs in E. coli

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