Conserved Bacterial RNase YbeY Plays Key Roles in 70S Ribosome Quality Control and 16S rRNA Maturation

Abstract

Quality control of ribosomes is critical for cellular function since protein mistranslation leads to severe physiological consequences. We report the first evidence of a ribosome quality control system in bacteria that operates at the level of 70S to remove defective ribosomes. YbeY, a previously unidentified endoribonuclease, and the exonuclease RNase R act together by a process mediated specifically by the 30S ribosomal subunit, to degrade defective 70S ribosomes but not properly matured 70S ribosomes or individual subunits. Furthermore, there is essentially no fully matured 16S rRNA in a ΔybeY mutant at 45°C, making YbeY the first endoribonuclease to be implicated in the critically important processing of the 16S rRNA 3' terminus. These key roles in ribosome quality control and maturation indicate why YbeY is a member of the minimal bacterial gene set and suggest that it could be a potential target for antibacterial drugs.

Absence of YbeY RNase compromises the growth and enhances the virulence plasmid gene expression of Yersinia enterocolitica O:3

“…In trans complementation did not fully restore the growth rates at 4 and 42 u C. This could be due to inadequate expression of ybeY from the pMMB207 plasmid at these temperatures. Indeed, it was earlier found that the expression of ybeY is upregulated in E. coli at 45 u C (Jacob et al, 2013). Whether this could be valid for 4 u C is not known.…”

“…Similar to E. coli (Jacob et al, 2013), YbeY in Y. enterocolitica plays a role in rRNA maturation as a ybeY mutant causes misprocessing of 16S rRNA leading to its degradation, but does not have a visible effect on the 23S and 5S rRNA (Fig. 3).…”

“…The 16S rRNA in prokaryotes also undergoes a maturation process. In the model proposed by Jacob et al (2013) the original transcript (17S rRNA) is cleaved both from the 59 and 39 ends by different endonucleases (RNase E, RNase G, RNase R and YbeY) with the help of ribosome maturation factors, including K. Leskinen, M. Varjosalo and M. Skurnik Era, KsgA, RbfA and RsgA. In this process YbeY cleaves the original 17S rRNA endonucleolytically generating a 39-phosphate terminus at or near the final maturation site (Jacob et al, 2013).…”

“…Although the structure showed similarity to eukaryotic extracellular proteinases such as collagenase and gelatinase, in vitro studies failed to detect any hydrolase activity (Rasouly et al, 2009). Only recently it was discovered that YbeY is an RNase that plays a critical role in rRNA maturation, as well as in late-stage 70S ribosome quality control (Jacob et al, 2013).…”

“…It was proposed that YbeY acts as a sensor of defective ribosomes by recognizing defects in 30S subunits, which subsequently initiates degradation of complete 70S ribosomes by introducing endonucleolytic cuts in the rRNA. Such damage in rRNA leads to its misprocessing and misfolding and further destruction by other RNases (Jacob et al, 2013). Moreover, YbeY is reported to play a role in transcriptional antitermination of rRNA synthesis, which is also critical for ribosome biogenesis (Grinwald & Ron, 2013).…”