Synergies between RNA degradation and <it>trans</it>-translation in <it>Streptococcus pneumoniae</it>: cross regulation and co-transcription of RNase R and SmpB

• Main Authors: Moreira Ricardo N, Domingues Susana, Viegas Sandra C, Amblar Mónica, Arraiano Cecília M
• Format: Article
• Language: English
• Published: BMC 2012-11-01
• Series: BMC Microbiology
• Subjects: RNA turnover; Post-transcriptional control; Quality control; Transcriptional unit; Non-stop RNA decay
• Online Access: http://www.biomedcentral.com/1471-2180/12/268

<p>Abstract</p> <p>Background</p> <p>Ribonuclease R (RNase R) is an exoribonuclease that recognizes and degrades a wide range of RNA molecules. It is a stress-induced protein shown to be important for the establishment of virulence in several pathogenic bacteria. RNase R has also been implicated in the <it>trans-</it>translation process. Transfer-messenger RNA (tmRNA/SsrA RNA) and SmpB are the main effectors of <it>trans-</it>translation, an RNA and protein quality control system that resolves challenges associated with stalled ribosomes on non-stop mRNAs. <it>Trans</it>-translation has also been associated with deficiencies in stress-response mechanisms and pathogenicity.</p> <p>Results</p> <p>In this work we study the expression of RNase R in the human pathogen <it>Streptococcus pneumoniae</it> and analyse the interplay of this enzyme with the main components of the <it>trans</it>-translation machinery (SmpB and tmRNA/SsrA). We show that RNase R is induced after a 37°C to 15°C temperature downshift and that its levels are dependent on SmpB. On the other hand, our results revealed a strong accumulation of the <it>smpB</it> transcript in the absence of RNase R at 15°C. Transcriptional analysis of the <it>S. pneumoniae rnr</it> gene demonstrated that it is co-transcribed with the flanking genes, <it>secG</it> and <it>smpB</it>. Transcription of these genes is driven from a promoter upstream of <it>secG</it> and the transcript is processed to yield mature independent mRNAs. This genetic organization seems to be a common feature of Gram positive bacteria, and the biological significance of this gene cluster is further discussed.</p> <p>Conclusions</p> <p>This study unravels an additional contribution of RNase R to the <it>trans</it>-translation system by demonstrating that <it>smpB</it> is regulated by this exoribonuclease. RNase R in turn, is shown to be under the control of SmpB. These proteins are therefore mutually dependent and cross-regulated. The data presented here shed light on the interactions between RNase R, <it>trans</it>-translation and cold-shock response in an important human pathogen.</p>