Global RNA interactome of Salmonella discovers a 5′ UTR sponge for the MicF small RNA that connects membrane permeability to transport capacity

Gianluca Matera, Yael Altuvia, Milan Gerovac, Youssef El Mouali, Hanah Margalit, Jörg Vogel*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

24 Scopus citations

Abstract

The envelope of Gram-negative bacteria is a vital barrier that must balance protection and nutrient uptake. Small RNAs are crucial regulators of the envelope composition and function. Here, using RIL-seq to capture the Hfq-mediated RNA-RNA interactome in Salmonella enterica, we discover envelope-related riboregulators, including OppX. We show that OppX acts as an RNA sponge of MicF sRNA, a prototypical porin repressor. OppX originates from the 5′ UTR of oppABCDF, encoding the major inner-membrane oligopeptide transporter, and sequesters MicF's seed region to derepress the synthesis of the porin OmpF. Intriguingly, OppX operates as a true sponge, storing MicF in an inactive complex without affecting its levels or stability. Conservation of the opp-OppX-MicF-ompF axis in related bacteria suggests that it serves an important mechanism, adjusting envelope porosity to specific transport capacity. These data also highlight the resource value of this Salmonella RNA interactome, which will aid in unraveling RNA-centric regulation in enteric pathogens.

Original languageAmerican English
Pages (from-to)629-644.e4
JournalMolecular Cell
Volume82
Issue number3
DOIs
StatePublished - 3 Feb 2022

Bibliographical note

Funding Information:
We thank Anke Sparmann for editing the manuscript and Jens Hör, Falk Ponath, and other members of the Vogel lab for ideas, comments, and fruitful discussions. We further thank Kotaro Chihara for technical help in performing the SEC experiment. We also thank Amir Bar, Niv Reiss, Yair Raz, Yair E. Gatt, and Shira Fisher for their help with computational analysis and the adaptation of the code. This work was supported by funds from Deutsche Forschungsgemeinschaft to J.V. (DFG grant Vo875-19/1). Research in the Margalit laboratory was supported by grants from the Israel Science Foundation (# 876/17 ) and European Research Council (ERC) under the European Union's Horizon 2020 research and innovation programme, Grant # 833598 .

Funding Information:
We thank Anke Sparmann for editing the manuscript and Jens H?r, Falk Ponath, and other members of the Vogel lab for ideas, comments, and fruitful discussions. We further thank Kotaro Chihara for technical help in performing the SEC experiment. We also thank Amir Bar, Niv Reiss, Yair Raz, Yair E. Gatt, and Shira Fisher for their help with computational analysis and the adaptation of the code. This work was supported by funds from Deutsche Forschungsgemeinschaft to J.V. (DFG grant Vo875-19/1). Research in the Margalit laboratory was supported by grants from the Israel Science Foundation (#876/17) and European Research Council (ERC) under the European Union's Horizon 2020 research and innovation programme, Grant #833598. G.M. and J.V. designed the experiments. G.M. and Y.E.M. conducted the experiments. Y.A. M.G. and H.M. designed and performed computational analyses. G.M. H.M. and J.V. wrote the paper, which all authors commented on. J.V. is a member of Molecular Cell's advisory board.

Publisher Copyright:
© 2021 The Author(s)

Keywords

  • 5' Untranslated Regions
  • Biological Transport
  • Cell Membrane/genetics
  • Escherichia coli Proteins/genetics
  • Gene Expression Regulation, Bacterial
  • Host Factor 1 Protein/genetics
  • Host-Pathogen Interactions
  • Permeability
  • Porins/genetics
  • RNA, Bacterial/genetics
  • RNA-Seq
  • Salmonella enterica/genetics

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