Maturation of atypical ribosomal RNA precursors in Helicobacter pylori

Nucleic Acids Res. 2019 Jun 20;47(11):5906-5921. doi: 10.1093/nar/gkz258.

Abstract

In most bacteria, ribosomal RNA is transcribed as a single polycistronic precursor that is first processed by RNase III. This double-stranded specific RNase cleaves two large stems flanking the 23S and 16S rRNA mature sequences, liberating three 16S, 23S and 5S rRNA precursors, which are further processed by other ribonucleases. Here, we investigate the rRNA maturation pathway of the human gastric pathogen Helicobacter pylori. This bacterium has an unusual arrangement of its rRNA genes, the 16S rRNA gene being separated from a 23S-5S rRNA cluster. We show that RNase III also initiates processing in this organism, by cleaving two typical stem structures encompassing 16S and 23S rRNAs and an atypical stem-loop located upstream of the 5S rRNA. Deletion of RNase III leads to the accumulation of a large 23S-5S precursor that is found in polysomes, suggesting that it can function in translation. Finally, we characterize a cis-encoded antisense RNA overlapping the leader of the 23S-5S rRNA precursor. We present evidence that this antisense RNA interacts with this precursor, forming an intermolecular complex that is cleaved by RNase III. This pairing induces additional specific cleavages of the rRNA precursor coupled with a rapid degradation of the antisense RNA.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Escherichia coli / metabolism
  • Helicobacter pylori / genetics*
  • Humans
  • Nucleic Acid Conformation
  • Oligonucleotides / genetics
  • Polyribosomes / metabolism
  • RNA Precursors / metabolism*
  • RNA, Antisense
  • RNA, Bacterial / metabolism
  • RNA, Ribosomal / metabolism
  • RNA, Ribosomal, 16S / genetics*
  • RNA, Ribosomal, 23S / metabolism*
  • RNA, Ribosomal, 5S / metabolism*
  • Ribonuclease III / metabolism*
  • Stomach Diseases / microbiology

Substances

  • Oligonucleotides
  • RNA Precursors
  • RNA, Antisense
  • RNA, Bacterial
  • RNA, Ribosomal
  • RNA, Ribosomal, 16S
  • RNA, Ribosomal, 23S
  • RNA, Ribosomal, 5S
  • Ribonuclease III