Synergies Between RNA Degradation and Trans-translation in Streptococcus Pneumoniae: Cross Regulation and Co-transcription of RNase R and SmpB

Overview

Journal BMC Microbiol

Publisher Biomed Central

Specialty Microbiology

Date 2012 Nov 22

PMID 23167513

Citations 12

Authors

Ricardo N Moreira

Susana Domingues

Sandra C Viegas

Monica Amblar

Cecilia M Arraiano

Affiliations

Soon will be listed here.

Abstract

Background: 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 trans-translation process. Transfer-messenger RNA (tmRNA/SsrA RNA) and SmpB are the main effectors of trans-translation, an RNA and protein quality control system that resolves challenges associated with stalled ribosomes on non-stop mRNAs. Trans-translation has also been associated with deficiencies in stress-response mechanisms and pathogenicity.

Results: In this work we study the expression of RNase R in the human pathogen Streptococcus pneumoniae and analyse the interplay of this enzyme with the main components of the trans-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 smpB transcript in the absence of RNase R at 15°C. Transcriptional analysis of the S. pneumoniae rnr gene demonstrated that it is co-transcribed with the flanking genes, secG and smpB. Transcription of these genes is driven from a promoter upstream of secG 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.

Conclusions: This study unravels an additional contribution of RNase R to the trans-translation system by demonstrating that smpB 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, trans-translation and cold-shock response in an important human pathogen.

Citing Articles

Functional activity of E. coli RNase R in the Antarctic Pseudomonas syringae Lz4W.

Hussain A, Ray M J Genet Eng Biotechnol. 2023; 21(1):101.

PMID: 37843651 PMC: 10579198. DOI: 10.1186/s43141-023-00553-2.

How hydrolytic exoribonucleases impact human disease: Two sides of the same story.

Costa S, Saramago M, Matos R, Arraiano C, Viegas S FEBS Open Bio. 2022; 13(6):957-974.

PMID: 35247037 PMC: 10240344. DOI: 10.1002/2211-5463.13392.

RNase R, a New Virulence Determinant of .

Barria C, Mil-Homens D, Pinto S, Fialho A, Arraiano C, Domingues S Microorganisms. 2022; 10(2).

PMID: 35208772 PMC: 8875335. DOI: 10.3390/microorganisms10020317.

Cbl upregulates for hydrogen sulfide production in .

Zhang Y, Liu Z, Tang Y, Ma X, Tang H, Li H PeerJ. 2021; 9:e12058.

PMID: 34589297 PMC: 8435198. DOI: 10.7717/peerj.12058.

A Small Non-Coding RNA Modulates Expression of Pilus-1 Type in .

Acebo P, Herranz C, Espenberger L, Gomez-Sanz A, Terron M, Luque D Microorganisms. 2021; 9(9).

PMID: 34576778 PMC: 8465756. DOI: 10.3390/microorganisms9091883.

References

Cairrao F, Chora A, Zilhao R, Carpousis A, Arraiano C . RNase II levels change according to the growth conditions: characterization of gmr, a new Escherichia coli gene involved in the modulation of RNase II. Mol Microbiol. 2001; 39(6):1550-61. DOI: 10.1046/j.1365-2958.2001.02342.x. View

Silva I, Saramago M, Dressaire C, Domingues S, Viegas S, Arraiano C . Importance and key events of prokaryotic RNA decay: the ultimate fate of an RNA molecule. Wiley Interdiscip Rev RNA. 2011; 2(6):818-36. DOI: 10.1002/wrna.94. View

Campos-Guillen J, Arvizu-Gomez J, Jones G, Olmedo-Alvarez G . Characterization of tRNA(Cys) processing in a conditional Bacillus subtilis CCase mutant reveals the participation of RNase R in its quality control. Microbiology (Reading). 2010; 156(Pt 7):2102-2111. DOI: 10.1099/mic.0.034652-0. View

Liang W, Malhotra A, Deutscher M . Acetylation regulates the stability of a bacterial protein: growth stage-dependent modification of RNase R. Mol Cell. 2011; 44(1):160-6. PMC: 3191462. DOI: 10.1016/j.molcel.2011.06.037. View

Simon D, Chopin A . Construction of a vector plasmid family and its use for molecular cloning in Streptococcus lactis. Biochimie. 1988; 70(4):559-66. DOI: 10.1016/0300-9084(88)90093-4. View

Reese M . Application of a time-delay neural network to promoter annotation in the Drosophila melanogaster genome. Comput Chem. 2002; 26(1):51-6. DOI: 10.1016/s0097-8485(01)00099-7. View

Papanikou E, Karamanou S, Economou A . Bacterial protein secretion through the translocase nanomachine. Nat Rev Microbiol. 2007; 5(11):839-51. DOI: 10.1038/nrmicro1771. View

Liang W, Deutscher M . A novel mechanism for ribonuclease regulation: transfer-messenger RNA (tmRNA) and its associated protein SmpB regulate the stability of RNase R. J Biol Chem. 2010; 285(38):29054-8. PMC: 2937936. DOI: 10.1074/jbc.C110.168641. View

Cairrao F, Cruz A, Mori H, Arraiano C . Cold shock induction of RNase R and its role in the maturation of the quality control mediator SsrA/tmRNA. Mol Microbiol. 2003; 50(4):1349-60. DOI: 10.1046/j.1365-2958.2003.03766.x. View

10.

Acebo P, Martin-Galiano A, Navarro S, Zaballos A, Amblar M . Identification of 88 regulatory small RNAs in the TIGR4 strain of the human pathogen Streptococcus pneumoniae. RNA. 2012; 18(3):530-46. PMC: 3285940. DOI: 10.1261/rna.027359.111. View

11.

Studier F, Moffatt B . Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes. J Mol Biol. 1986; 189(1):113-30. DOI: 10.1016/0022-2836(86)90385-2. View

12.

Hong S, Tran Q, Keiler K . Cell cycle-regulated degradation of tmRNA is controlled by RNase R and SmpB. Mol Microbiol. 2005; 57(2):565-75. PMC: 3776457. DOI: 10.1111/j.1365-2958.2005.04709.x. View

13.

Cheng Z, Zuo Y, Li Z, Rudd K, Deutscher M . The vacB gene required for virulence in Shigella flexneri and Escherichia coli encodes the exoribonuclease RNase R. J Biol Chem. 1998; 273(23):14077-80. DOI: 10.1074/jbc.273.23.14077. View

14.

Overbeek R, Larsen N, Pusch G, DSouza M, Selkov Jr E, Kyrpides N . WIT: integrated system for high-throughput genome sequence analysis and metabolic reconstruction. Nucleic Acids Res. 1999; 28(1):123-5. PMC: 102471. DOI: 10.1093/nar/28.1.123. View

15.

Ge Z, Mehta P, Richards J, Karzai A . Non-stop mRNA decay initiates at the ribosome. Mol Microbiol. 2010; 78(5):1159-70. PMC: 3056498. DOI: 10.1111/j.1365-2958.2010.07396.x. View

16.

Tettelin H, Nelson K, Paulsen I, Eisen J, Read T, Peterson S . Complete genome sequence of a virulent isolate of Streptococcus pneumoniae. Science. 2001; 293(5529):498-506. DOI: 10.1126/science.1061217. View

17.

Reva O, Weinel C, Weinel M, Bohm K, Stjepandic D, Hoheisel J . Functional genomics of stress response in Pseudomonas putida KT2440. J Bacteriol. 2006; 188(11):4079-92. PMC: 1482902. DOI: 10.1128/JB.00101-06. View

18.

Keiler K . Biology of trans-translation. Annu Rev Microbiol. 2008; 62:133-51. DOI: 10.1146/annurev.micro.62.081307.162948. View

19.

Cheng Z, Deutscher M . An important role for RNase R in mRNA decay. Mol Cell. 2005; 17(2):313-8. DOI: 10.1016/j.molcel.2004.11.048. View

20.

Grossman D, van Hoof A . RNase II structure completes group portrait of 3' exoribonucleases. Nat Struct Mol Biol. 2006; 13(9):760-1. DOI: 10.1038/nsmb0906-760. View