RNA stability is regulated by both RNA polyadenylation and ATP levels, linking RNA and energy metabolisms in Escherichia coli
2025
Roux, Charlotte | Ramos-Hue, Marvin | Audonnet, Marjorie | Duviau, Marie-Pierre | Nouaille, Sébastien | Carpousis, Agamemnon, J. | Laguerre, Sandrine | Hajnsdorf, Eliane | Cocaign‐bousquet, Muriel | Girbal, Laurence | Toulouse Biotechnology Institute (TBI) ; Institut National des Sciences Appliquées - Toulouse (INSA Toulouse) ; Institut National des Sciences Appliquées (INSA)-Université de Toulouse (UT)-Institut National des Sciences Appliquées (INSA)-Université de Toulouse (UT)-Centre National de la Recherche Scientifique (CNRS)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE) | Institut de biologie physico-chimique (IBPC (FR_550)) ; Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS) | ANR-18-CE43-0010,RIB-ECO,Ingénierie du cycle de vie des ARN pour une approche économique de l'énergétique microbienne: application à la bioconversion des sources de carbone dérivées de la biomasse(2018) | ANR-23-CE44-0022,RECOM,La compétition des ARNs pour la RNase E, un mécanisme régulant leur dégradation et le métabolisme de l'énergie et du carbone dans la cellule(2023)
International audience
Afficher plus [+] Moins [-]anglais. The post-transcriptional process of RNA polyadenylation sits at the crossroads of energy metabolism and RNA metabolism. RNA polyadenylation is catalyzed by poly(A) polymerases which use ATP as a substrate to add adenine to the 3’-end of RNAs, which can alter their stability. In E. coli, RNA polyadenylation mediated by the major poly(A) polymerase was previously shown to facilitate degradation of individual RNAs. In this study, we performed the first genome-wide study of RNA stability in the absence of PAP I. Inactivation of the pcnB gene coding for PAP I led to the stabilization of more than a thousand of E. coli RNAs in the form of full-length functional molecules or non-functional fragments. The absence of PAP I altered the energy metabolism, with an almost 20% reduction in ATP levels. To better understand how RNA and energy metabolisms are interconnected, we investigated the role of ATP levels in regulating RNA stability. When we lowered intracellular ATP levels below 0.5mM, many RNAs were stabilized demonstrating the causal link between ATP levels and RNA stability for the first time in E. coli. Above this concentration, changes in ATP levels had no impact on RNA stability. We also demonstrated that some RNAs were stabilized when PAP I was inactivated by low ATP availability. These results clearly demonstrate that PAP I mediates an energy-dependent RNA stabilization which may contribute to cell energy homeostasis under energy-limited conditions.
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