Secondary Structure across the Bacterial Transcriptome Reveals Versatile Roles in mRNA Regulation and Function

PLoS Genet. 2015 Oct 23;11(10):e1005613. doi: 10.1371/journal.pgen.1005613. eCollection 2015 Oct.

Abstract

Messenger RNA acts as an informational molecule between DNA and translating ribosomes. Emerging evidence places mRNA in central cellular processes beyond its major function as informational entity. Although individual examples show that specific structural features of mRNA regulate translation and transcript stability, their role and function throughout the bacterial transcriptome remains unknown. Combining three sequencing approaches to provide a high resolution view of global mRNA secondary structure, translation efficiency and mRNA abundance, we unraveled structural features in E. coli mRNA with implications in translation and mRNA degradation. A poorly structured site upstream of the coding sequence serves as an additional unspecific binding site of the ribosomes and the degree of its secondary structure propensity negatively correlates with gene expression. Secondary structures within coding sequences are highly dynamic and influence translation only within a very small subset of positions. A secondary structure upstream of the stop codon is enriched in genes terminated by UAA codon with likely implications in translation termination. The global analysis further substantiates a common recognition signature of RNase E to initiate endonucleolytic cleavage. This work determines for the first time the E. coli RNA structurome, highlighting the contribution of mRNA secondary structure as a direct effector of a variety of processes, including translation and mRNA degradation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Binding Sites
  • Escherichia coli / genetics
  • Nucleic Acid Conformation*
  • Nucleotide Motifs / genetics
  • Protein Biosynthesis / genetics*
  • Protein Structure, Secondary
  • RNA Stability / genetics*
  • RNA, Messenger / chemistry
  • RNA, Messenger / genetics*
  • Ribonucleases / genetics
  • Ribosomes / genetics
  • Sequence Analysis, RNA
  • Transcriptome / genetics*

Substances

  • RNA, Messenger
  • Ribonucleases

Grants and funding

This work was supported by the Deutsche Forschungsgemeinschaft (FOR 1805) and European Union (grant NICHE ITN) to ZI. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.