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.
Cells make many proteins that are eventually released outside the cell or inserted into the cell’s membrane. As these proteins are still being made, they are captured by a “signal recognition particle” (or SRP); this molecular machine then guides the newly forming protein to the cell’s membrane. SRPs are found in all living organisms on Earth and contain several different proteins and a short RNA molecule. However, a few species belonging to the archaeal domain of life did not seem to contain an identifiable gene for the RNA component of the SRP.
Now Plagens et al. have sought to solve the mystery of the “missing” component of this essential protein-targeting machine. This involved searching through the RNAs that are produced by an archaeon called Thermoproteus tenax, a single-celled microbe which grows in the absence of oxygen and at temperatures of up to 95°C.
Plagens et al. discovered that the “missing” SRP RNA gene had not yet been identified because rearrangements in this archaeon’s genome had swapped the left and right portions of the SRP RNA gene. Further experiments revealed that the correct sequence order is restored in mature SRP RNA molecules by the two ends of the molecule being linked to form a circle. These RNA circles are made by the cellular machinery that normally removes the unneeded sections from other RNA molecules (called transfer RNAs).
Circular RNA is much more stable at high temperatures and does not degrade easily, and Plagens et al. suggest that this particular arrangement is therefore especially advantageous for this species. Future work will now aim to work out which selective pressures favor the evolution of such fragmented RNAs.