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Modulation of Polyadenylation InducesStrong Metabolic Rearrangementsin Escherichia coli
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International audience. Background: Bacteria must adapt to changing environments using complex regulatory networks. Post-transcriptional regulations, particularly RNA degradation allow rapid metabolic adjustments by regulating protein synthesis. In E. coli, poly(A) polymerase I (PAP I) promotes RNA degradation by polyadenylating RNA 3’-ends [1]. Interestingly, recent studies on individual metabolic pathways and RNAs have identified cross-regulations between RNA degradation and metabolism [2], raising the possibility of a more general regulatory network linking the two processes. In this work, we aimed to assess the genome-wide role of RNA polyadenylation in regulating of RNA stability and E. coli metabolism.Methods: We performed genome-wide analyses of RNA half-lives along with metabolome quantifications during exponential growth in three E. coli strains: the wild type strain, a strain deficient in PAP I activity and a strain overexpressing PAP I. Results: Upon inactivation and overexpression of PAP I, we observed strong rearrangements of the central carbon metabolism. More particularly, PAP I targets the metabolisms of acetate, UDP-sugars and nucleotides, and the pentose phosphate pathway. In the absence of RNA polyadenylation, we observed a global RNA stabilization with 1403 transcripts significantly stabilized and only 4 destabilized. This is the first report of a genome-wide destabilizing effect of RNA polyadenylation in E. coli. Stabilized RNAs were involved in essential cellular functions such as DNA replication and repair, translation, RNA degradation, envelope biogenesis, central carbon metabolism and stress responses. Conclusion: These results provide the first evidence of global metabolic regulation by PAP I in E. coli. This finding coupled with the general RNA stabilization observed in the absence of PAP I, led us to conclude that E. coli cells can use the polyadenylation-mediated RNA degradation pathway to regulate their metabolic activity. Altogether, this study highlights a clear interaction between the RNA degradation process and metabolism in E. coli.[1] E. Hajnsdorf et V. R. Kaberdin, « RNA polyadenylation and its consequences in prokaryotes », Philos. Trans. R. Soc. Lond., B, Biol. Sci., vol. 373, no 1762, 05 2018, doi: 10.1098/rstb.2018.0166. [2] C. Roux et al., « The essential role of mRNA degradation in understanding and engineering E. coli metabolism », Biotechnol Adv, Jan-Feb 2022;54:107805.doi: 10.1016/j.biotechadv.2021.107805.
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