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RNA localization in prokaryotes: Where, when, how, and why

Advanced Review

Mikel Irastortza‐Olaziregi, Orna Amster‐Choder

Published Online: Aug 27 2020

DOI: 10.1002/wrna.1615

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Abstract Only recently has it been recognized that the transcriptome of bacteria and archaea can be spatiotemporally regulated. All types of prokaryotic transcripts—rRNAs, tRNAs, mRNAs, and regulatory RNAs—may acquire specific localization and these patterns can be temporally regulated. In some cases bacterial RNAs reside in the vicinity of the transcription site, but in many others, transcripts show distinct localizations to the cytoplasm, the inner membrane, or the pole of rod‐shaped species. This localization, which often overlaps with that of the encoded proteins, can be achieved either in a translation‐dependent or translation‐independent fashion. The latter implies that RNAs carry sequence‐level features that determine their final localization with the aid of RNA‐targeting factors. Localization of transcripts regulates their posttranscriptional fate by affecting their degradation and processing, translation efficiency, sRNA‐mediated regulation, and/or propensity to undergo RNA modifications. By facilitating complex assembly and liquid–liquid phase separation, RNA localization is not only a consequence but also a driver of subcellular spatiotemporal complexity. We foresee that in the coming years the study of RNA localization in prokaryotes will produce important novel insights regarding the fundamental understanding of membrane‐less subcellular organization and lead to practical outputs with biotechnological and therapeutic implications. This article is categorized under: RNA Export and Localization > RNA Localization Regulatory RNAs/RNAi/Riboswitches > Regulatory RNAs RNA Interactions with Proteins and Other Molecules > Protein‐RNA Interactions: Functional Implications

Translation‐independent mRNA localization. Depicted are episodes of mRNA localization that are independent of translation, which may tentatively lead to localized translation. When transcription occurs, an RNA shielding factor (red ball) binds the nascent RNA, preventing its translation and decay. Once transcription terminates, the ribosome‐free transcripts navigate to their final destination, either in the cytoplasm or near the membrane, to be translated in these domains

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Translation‐dependent mRNA localization. Translation of cytoplasmic mRNAs may start cotranscriptionally, and once transcription terminates, the newly synthesized transcripts remain in the cytoplasm and undergoe repeated cycles of translation. Translation of membranelocalizing transcripts may initiate by transertion events that anchor the transcribing–translating–translocating complex to the cell membrane. Once transcription terminates, the transcript remains in the membrane by means of cotranslational translocation of membrane proteins

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Different localization patterns of mRNAs in bacteria. mRNAs were observed to localize homogeneously (a); segregated from the nucleoid (b); in the poles (c); in a helix‐like path that overlaps the grooves of the nucleoid that accupies a helical elipsoid shape (d); near the inner membrane (e); in discrete sites in the cytoplasm (f); near the transcription site from plasmids in Escherichia coli cells (g); and in the vicinity of the transcription site from the chromosome in Caulobacter crescentus cells (h)

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Different arrangements of the nucleoid and ribosomes in different bacterial species. In species with low nucleoid‐to‐cytoplasm (NC) ratio, for example, Escherichia coli, ribosomes accumulate in nucleoid‐devoid regions, mainly in the cell poles, but also near the membrane. In organisms with a high NC ratio, such as Caulobacter crescentus, ribosomes and the nucleoid mix homogeneously

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RNA localization can affect its propensity to undergo RNA modifications. Cytoplasmic RNAs are preferentially decapped by RppH (red pacmans), thus creating an enriched population of 5′‐monophosphorylated transcripts in the cytoplasm. This population is degraded by RNase E (green pacmans) via the 5′‐end dependent degradation pathway. On the other hand, transcripts localizing to the membrane are less likely to be decapped and, therefore, the “direct entry” pathway is the main pathway for their degradation

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The poles are hubs for sRNA‐mediated regulation. Upon stress, sRNAs (green wavy lines) and Hfq (pink rings) accumulate in the cell poles. Consequently, transcripts localizing to these regions will be more prone to undergo sRNA‐mediated regulation

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mRNA localization affects translational efficiency. Transcripts localizing to nucleoid‐devoid regions, such as the cell poles, are bound by multiple ribosomes creating higher polysomic stoichiometries. Consequently, the translational output per transcript increases. On the other hand, the translational efficiency of transcripts localizing to regions allowing lower polysomic stoichiometries will be lower

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Localization of RNases overlaps with regions of high ribonucleolytic activity. In C. crescentus, RNase E (green pacmans) forms liquid–liquid phase separation (LLPS) droplets that overlap with rRNA transcription hubs and create centers of intensive rRNA processing. In Eschrichia coli, membrane‐bound RNase E creates regions of high ribonucleolytic activity that decrease the average stability of membrane mRNAs in comparison to those localized in the cytosol

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