Escherichia coli ribosomal protein S1 unfolds structured mRNAs onto the ribosome for active translation initiation

PLoS Biol. 2013 Dec;11(12):e1001731. doi: 10.1371/journal.pbio.1001731. Epub 2013 Dec 10.


Regulation of translation initiation is well appropriate to adapt cell growth in response to stress and environmental changes. Many bacterial mRNAs adopt structures in their 5' untranslated regions that modulate the accessibility of the 30S ribosomal subunit. Structured mRNAs interact with the 30S in a two-step process where the docking of a folded mRNA precedes an accommodation step. Here, we used a combination of experimental approaches in vitro (kinetic of mRNA unfolding and binding experiments to analyze mRNA-protein or mRNA-ribosome complexes, toeprinting assays to follow the formation of ribosomal initiation complexes) and in vivo (genetic) to monitor the action of ribosomal protein S1 on the initiation of structured and regulated mRNAs. We demonstrate that r-protein S1 endows the 30S with an RNA chaperone activity that is essential for the docking and the unfolding of structured mRNAs, and for the correct positioning of the initiation codon inside the decoding channel. The first three OB-fold domains of S1 retain all its activities (mRNA and 30S binding, RNA melting activity) on the 30S subunit. S1 is not required for all mRNAs and acts differently on mRNAs according to the signals present at their 5' ends. This work shows that S1 confers to the ribosome dynamic properties to initiate translation of a large set of mRNAs with diverse structural features.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Escherichia coli / physiology*
  • Escherichia coli Proteins / physiology*
  • Gene Expression Regulation, Bacterial / physiology
  • Protein Biosynthesis / physiology*
  • RNA Folding / physiology*
  • RNA, Messenger / physiology*
  • Ribosomal Proteins / physiology*
  • Ribosomes / physiology*


  • Escherichia coli Proteins
  • RNA, Messenger
  • Ribosomal Proteins
  • ribosomal protein S1, E coli

Grant support

This work was supported by the Centre National de la Recherche Scientifique (CNRS, MS, PR), Agence Nationale de la Recherche (ANR-07-BLAN-0351-02, PR, MS & BPK), the “Laboratoires d'excellence” (LABEX) NetRNA grant ANR-10-LABX-36 (PR), and the Austrian Science Fund (P21641, RM), the French Infrastructure for Integrated Structural Biology Grant ANR-10-INSB-05-01 (BPK), and Instruct as part of European Strategy Forum on Research Infrastructures (BPK). AK was supported by a Marie Curie fellowship and by RFBR (research project N° 12-04-33272a). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.