RNase III CLASH in MRSA uncovers sRNA regulatory networks coupling metabolism to toxin expression

Stuart W. McKellar, Ivayla Ivanova, Pedro Arede, Rachel L. Zapf, Noémie Mercier, Liang-Cui Chu, Daniel G. Mediati, Amy C. Pickering, Paul Briaud, Robert G. Foster, Grzegorz Kudla, J. Ross Fitzgerald, Isabelle Caldelari, Ronan K. Carroll, Jai J. Tree and Sander Granneman ()
Additional contact information
Stuart W. McKellar: University of Edinburgh
Ivayla Ivanova: University of Edinburgh
Pedro Arede: University of Edinburgh
Rachel L. Zapf: Ohio University
Noémie Mercier: Université de Strasbourg, CNRS, Architecture et Réactivité de l’ARN, UPR9002
Liang-Cui Chu: University of Edinburgh
Daniel G. Mediati: University of New South Wales
Amy C. Pickering: The Roslin Institute and Edinburgh Infectious Diseases, University of Edinburgh, Easter Bush Campus
Paul Briaud: Ohio University
Robert G. Foster: MRC Human Genetics Unit, University of Edinburgh
Grzegorz Kudla: MRC Human Genetics Unit, University of Edinburgh
J. Ross Fitzgerald: The Roslin Institute and Edinburgh Infectious Diseases, University of Edinburgh, Easter Bush Campus
Isabelle Caldelari: Université de Strasbourg, CNRS, Architecture et Réactivité de l’ARN, UPR9002
Ronan K. Carroll: Ohio University
Jai J. Tree: University of New South Wales
Sander Granneman: University of Edinburgh

Nature Communications, 2022, vol. 13, issue 1, 1-20

Abstract: Abstract Methicillin-resistant Staphylococcus aureus (MRSA) is a bacterial pathogen responsible for significant human morbidity and mortality. Post-transcriptional regulation by small RNAs (sRNAs) has emerged as an important mechanism for controlling virulence. However, the functionality of the majority of sRNAs during infection is unknown. To address this, we performed UV cross-linking, ligation, and sequencing of hybrids (CLASH) in MRSA to identify sRNA-RNA interactions under conditions that mimic the host environment. Using a double-stranded endoribonuclease III as bait, we uncovered hundreds of novel sRNA-RNA pairs. Strikingly, our results suggest that the production of small membrane-permeabilizing toxins is under extensive sRNA-mediated regulation and that their expression is intimately connected to metabolism. Additionally, we also uncover an sRNA sponging interaction between RsaE and RsaI. Taken together, we present a comprehensive analysis of sRNA-target interactions in MRSA and provide details on how these contribute to the control of virulence in response to changes in metabolism.

Date: 2022
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DOI: 10.1038/s41467-022-31173-y

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