Circularization restores signal recognition particle RNA functionality in Thermoproteus

Elife. 2015 Oct 24:4:e11623. doi: 10.7554/eLife.11623.

Abstract

Signal recognition particles (SRPs) are universal ribonucleoprotein complexes found in all three domains of life that direct the cellular traffic and secretion of proteins. These complexes consist of SRP proteins and a single, highly structured SRP RNA. Canonical SRP RNA genes have not been identified for some Thermoproteus species even though they contain SRP19 and SRP54 proteins. Here, we show that genome rearrangement events in Thermoproteus tenax created a permuted SRP RNA gene. The 5'- and 3'-termini of this SRP RNA are located close to a functionally important loop present in all known SRP RNAs. RNA-Seq analyses revealed that these termini are ligated together to generate circular SRP RNA molecules that can bind to SRP19 and SRP54. The circularization site is processed by the tRNA splicing endonuclease. This moonlighting activity of the tRNA splicing machinery permits the permutation of the SRP RNA and creates highly stable and functional circular RNA molecules.

Keywords: RNA processing; Thermoproteus tenax; archaea; biochemistry; evolutionary biology; genomics; signal recognition particle; splicing.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • RNA / genetics
  • RNA / metabolism*
  • RNA, Circular
  • RNA, Transfer / genetics
  • RNA, Transfer / metabolism
  • Signal Recognition Particle / genetics
  • Signal Recognition Particle / metabolism*
  • Thermoproteus / genetics*
  • Thermoproteus / metabolism*

Substances

  • RNA, Circular
  • Signal Recognition Particle
  • RNA
  • RNA, Transfer

Grants and funding

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.