1887
No metrics data to plot.
The attempt to load metrics for this article has failed.
The attempt to plot a graph for these metrics has failed.

RNases and Helicases in Gram-Positive Bacteria

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.
Buy this Microbiology Spectrum Article
Price Non-Member $15.00
  • Authors: Sylvain Durand1, Ciaran Condon2
  • Editors: Gisela Storz3, Kai Papenfort4
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: UMR8261 CNRS, Université Paris Diderot (Sorbonne Paris Cité), Institut de Biologie Physico-Chimique, Paris, France; 2: UMR8261 CNRS, Université Paris Diderot (Sorbonne Paris Cité), Institut de Biologie Physico-Chimique, Paris, France; 3: Division of Molecular and Cellular Biology, Eunice Kennedy Shriver National Institute of Child Health and Human Development, Bethesda, MD; 4: Department of Biology I, Microbiology, LMU Munich, Martinsried, Germany
  • Source: microbiolspec April 2018 vol. 6 no. 2 doi:10.1128/microbiolspec.RWR-0003-2017
  • Received 23 October 2017 Accepted 16 January 2018 Published 13 April 2018
  • Sylvain Durand, durand@ibpc.fr
image of RNases and Helicases in Gram-Positive Bacteria
    Preview this microbiology spectrum article:
    Zoom in
    Zoomout

    RNases and Helicases in Gram-Positive Bacteria, Page 1 of 2

    | /docserver/preview/fulltext/microbiolspec/6/2/RWR-0003-2017-1.gif /docserver/preview/fulltext/microbiolspec/6/2/RWR-0003-2017-2.gif
  • Abstract:

    RNases are key enzymes involved in RNA maturation and degradation. Although they play a crucial role in all domains of life, bacteria, archaea, and eukaryotes have evolved with their own sets of RNases and proteins modulating their activities. In bacteria, these enzymes allow modulation of gene expression to adapt to rapidly changing environments. Today, >20 RNases have been identified in both and , the paradigms of the Gram-negative and Gram-positive bacteria, respectively. However, only a handful of these enzymes are common to these two organisms and some of them are essential to only one. Moreover, although sets of RNases can be very similar in closely related bacteria such as the and , the relative importance of individual enzymes in posttranscriptional regulation in these organisms varies. In this review, we detail the role of the main RNases involved in RNA maturation and degradation in Gram-positive bacteria, with an emphasis on the roles of RNase J1, RNase III, and RNase Y. We also discuss how other proteins such as helicases can modulate the RNA-degradation activities of these enzymes.

  • Citation: Durand S, Condon C. 2018. RNases and Helicases in Gram-Positive Bacteria. Microbiol Spectrum 6(2):RWR-0003-2017. doi:10.1128/microbiolspec.RWR-0003-2017.

References

1. Sala A, Bordes P, Genevaux P. 2014. Multiple toxin-antitoxin systems in Mycobacterium tuberculosis. Toxins (Basel) 6:1002–1020. [PubMed]
2. Lehnik-Habrink M, Newman J, Rothe FM, Solovyova AS, Rodrigues C, Herzberg C, Commichau FM, Lewis RJ, Stülke J. 2011. RNase Y in Bacillus subtilis: a natively disordered protein that is the functional equivalent of RNase E from Escherichia coli. J Bacteriol 193:5431–5441. [PubMed]
3. Gilet L, DiChiara JM, Figaro S, Bechhofer DH, Condon C. 2015. Small stable RNA maturation and turnover in Bacillus subtilis. Mol Microbiol 95:270–282. [PubMed]
4. Durand S, Gilet L, Bessières P, Nicolas P, Condon C. 2012. Three essential ribonucleases—RNase Y, J1, and III—control the abundance of a majority of Bacillus subtilis mRNAs. PLoS Genet 8:e1002520. doi:10.1371/journal.pgen.1002520. [PubMed]
5. Laalami S, Bessières P, Rocca A, Zig L, Nicolas P, Putzer H. 2013. Bacillus subtilis RNase Y activity in vivo analysed by tiling microarrays. PLoS One 8:e54062. doi:10.1371/journal.pone.0054062. [PubMed]
6. Obana N, Nakamura K, Nomura N. 2016. Role of RNase Y in Clostridium perfringens mRNA decay and processing. J Bacteriol 199:e00703-16. doi:10.1128/JB.00703-16. [PubMed]
7. Deloughery A, Dengler V, Chai Y, Losick R. 2011. A multiprotein complex required for biofilm formation by Bacillus subtilis. Mol Microbiol 99:425–437. [PubMed]
8. Figaro S, Durand S, Gilet L, Cayet N, Sachse M, Condon C. 2013. Bacillus subtilis mutants with knockouts of the genes encoding ribonucleases RNase Y and RNase J1 are viable, with major defects in cell morphology, sporulation, and competence. J Bacteriol 195:2340–2348. [PubMed]
9. Chen Z, Itzek A, Malke H, Ferretti JJ, Kreth J. 2013. Multiple roles of RNase Y in Streptococcus pyogenes mRNA processing and degradation. J Bacteriol 195:2585–2594. [PubMed]
10. Marincola G, Schäfer T, Behler J, Bernhardt J, Ohlsen K, Goerke C, Wolz C. 2012. RNase Y of Staphylococcus aureus and its role in the activation of virulence genes. Mol Microbiol 85:817–832. [PubMed]
11. Khemici V, Prados J, Linder P, Redder P. 2015. Decay-initiating endoribonucleolytic cleavage by RNase Y is kept under tight control via sequence preference and sub-cellular localisation. PLoS Genet 11:e1005577. doi:10.1371/journal.pgen. [PubMed]
12. Shahbabian K, Jamalli A, Zig L, Putzer H. 2009. RNase Y, a novel endoribonuclease, initiates riboswitch turnover in Bacillus subtilis. EMBO J 28:3523–3533. [PubMed]
13. Marincola G, Wolz C. 2017. Downstream element determines RNase Y cleavage of the saePQRS operon in Staphylococcus aureus. Nucleic Acids Res 45:5980–5994. [PubMed]
14. Durand S, Braun F, Lioliou E, Romilly C, Helfer AC, Kuhn L, Quittot N, Nicolas P, Romby P, Condon C. 2015. A nitric oxide regulated small RNA controls expression of genes involved in redox homeostasis in Bacillus subtilis. PLoS Genet 11:e1004957. doi:10.1371/journal.pgen.1004957. [PubMed]
15. Deikus G, Babitzke P, Bechhofer DH. 2004. Recycling of a regulatory protein by degradation of the RNA to which it binds. Proc Natl Acad Sci U S A 101:2747–2751. [PubMed]
16. Deikus G, Bechhofer DH. 2009. Bacillus subtilis trp Leader RNA: RNase J1 endonuclease cleavage specificity and PNPase processing. J Biol Chem 284:26394–26401. [PubMed]
17. Deikus G, Bechhofer DH. 2011. 5′ end-independent RNase J1 endonuclease cleavage of Bacillus subtilis model RNA. J Biol Chem 286:34932–34940. [PubMed]
18. Panganiban AT, Whiteley HR. 1983. Purification and properties of a new Bacillus subtilis RNA processing enzyme. Cleavage of phage SP82 mRNA and Bacillus subtilis precursor rRNA. J Biol Chem 258:12487–12493. [PubMed]
19. Oguro A, Kakeshita H, Nakamura K, Yamane K, Wang W, Bechhofer DH. 1998. Bacillus subtilis RNase III cleaves both 5′- and 3′-sites of the small cytoplasmic RNA precursor. J Biol Chem 273:19542–19547. [PubMed]
20. Lioliou E, Sharma CM, Caldelari I, Helfer AC, Fechter P, Vandenesch F, Vogel J, Romby P. 2012. Global regulatory functions of the Staphylococcus aureus endoribonuclease III in gene expression. PLoS Genet 8:e1002782. doi:10.1371/journal.pgen.1002782. [PubMed]
21. Stead MB, Marshburn S, Mohanty BK, Mitra J, Pena Castillo L, Ray D, van Bakel H, Hughes TR, Kushner SR. 2011. Analysis of Escherichia coli RNase E and RNase III activity in vivo using tiling microarrays. Nucleic Acids Res 39:3188–3203. [PubMed]
22. Toledo-Arana A, Dussurget O, Nikitas G, Sesto N, Guet-Revillet H, Balestrino D, Loh E, Gripenland J, Tiensuu T, Vaitkevicius K, Barthelemy M, Vergassola M, Nahori MA, Soubigou G, Régnault B, Coppée JY, Lecuit M, Johansson J, Cossart P. 2009. The Listeria transcriptional landscape from saprophytism to virulence. Nature 459:950–956. [PubMed]
23. Lasa I, Toledo-Arana A, Dobin A, Villanueva M, de los Mozos IR, Vergara-Irigaray M, Segura V, Fagegaltier D, Penadés JR, Valle J, Solano C, Gingeras TR. 2011. Genome-wide antisense transcription drives mRNA processing in bacteria. Proc Natl Acad Sci U S A 108:20172–20177. [PubMed]
24. Novick RP, Ross HF, Projan SJ, Kornblum J, Kreiswirth B, Moghazeh S. 1993. Synthesis of staphylococcal virulence factors is controlled by a regulatory RNA molecule. EMBO J 12:3967–3975. [PubMed]
25. Kaito C, Saito Y, Ikuo M, Omae Y, Mao H, Nagano G, Fujiyuki T, Numata S, Han X, Obata K, Hasegawa S, Yamaguchi H, Inokuchi K, Ito T, Hiramatsu K, Sekimizu K. 2013. Mobile genetic element SCCmec-encoded psm-mec RNA suppresses translation of agrA and attenuates MRSA virulence. PLoS Pathog 9:e1003269. doi:10.1371/journal.ppat.1003269. [PubMed]
26. Deltcheva E, Chylinski K, Sharma CM, Gonzales K, Chao Y, Pirzada ZA, Eckert MR, Vogel J, Charpentier E. 2011. CRISPR RNA maturation by trans-encoded small RNA and host factor RNase III. Nature 471:602–607. [PubMed]
27. Redko Y, Bechhofer DH, Condon C. 2008. Mini-III, an unusual member of the RNase III family of enzymes, catalyses 23S ribosomal RNA maturation in B. subtilis. Mol Microbiol 68:1096–1106. [PubMed]
28. Olmedo G, Guzmán P. 2008. Mini-III, a fourth class of RNase III catalyses maturation of the Bacillus subtilis 23S ribosomal RNA. Mol Microbiol 68:1073–1076. [PubMed]
29. Hotto AM, Castandet B, Gilet L, Higdon A, Condon C, Stern DB. 2015. Arabidopsis chloroplast mini-ribonuclease III participates in rRNA maturation and intron recycling. Plant Cell 27:724–740. [PubMed]
30. Aït-Bara S, Carpousis AJ. 2015. RNA degradosomes in bacteria and chloroplasts: classification, distribution and evolution of RNase E homologs. Mol Microbiol 97:1021–1135. [PubMed]
31. Zeller ME, Csanadi A, Miczak A, Rose T, Bizebard T, Kaberdin VR. 2007. Quaternary structure and biochemical properties of mycobacterial RNase E/G. Biochem J 403:207–215. [PubMed]
32. Taverniti V, Forti F, Ghisotti D, Putzer H. 2011. Mycobacterium smegmatis RNase J is a 5′-3′ exo-/endoribonuclease and both RNase J and RNase E are involved in ribosomal RNA maturation. Mol Microbiol 82:1260–1276. [PubMed]
33. Kovacs L, Csanadi A, Megyeri K, Kaberdin VR, Miczak A. 2005. Mycobacterial RNase E-associated proteins. Microbiol Immunol 49:1003–1007. [PubMed]
34. Pfeiffer V, Papenfort K, Lucchini S, Hinton JC, Vogel J. 2009. Coding sequence targeting by MicC RNA reveals bacterial mRNA silencing downstream of translational initiation. Nat Struct Mol Biol 16:840–846. [PubMed]
35. Bandyra KJ, Said N, Pfeiffer V, Górna MW, Vogel J, Luisi BF. 2012. The seed region of a small RNA drives the controlled destruction of the target mRNA by the endoribonuclease RNase E. Mol Cell 47:943–953. [PubMed]
36. Wen T, Oussenko IA, Pellegrini O, Bechhofer DH, Condon C. 2005. Ribonuclease PH plays a major role in the exonucleolytic maturation of CCA-containing tRNA precursors in Bacillus subtilis. Nucleic Acids Res 33:3636–3643. [PubMed]
37. Oussenko IA, Abe T, Ujiie H, Muto A, Bechhofer DH. 2005. Participation of 3′-to-5′ exoribonucleases in the turnover of Bacillus subtilis mRNA. J Bacteriol 187:2758–2767. [PubMed]
38. Even S, Pellegrini O, Zig L, Labas V, Vinh J, Bréchemmier-Baey D, Putzer H. 2005. Ribonucleases J1 and J2: two novel endoribonucleases in B.subtilis with functional homology to E.coli RNase E. Nucleic Acids Res 33:2141–2152. [PubMed]
39. Dorléans A, Li de la Sierra-Gallay I, Piton J, Zig L, Gilet L, Putzer H, Condon C. 2011. Molecular basis for the recognition and cleavage of RNA by the bifunctional 5′-3′ exo/endoribonuclease RNase J. Structure 19:1252–1261. [PubMed]
40. Newman JA, Hewitt L, Rodrigues C, Solovyova A, Harwood CR, Lewis RJ. 2011. Unusual, dual endo- and exonuclease activity in the degradosome explained by crystal structure analysis of RNase J1. Structure 19:1241–1251. [PubMed]
41. Mathy N, Hébert A, Mervelet P, Bénard L, Dorléans A, Li de la Sierra-Gallay I, Noirot P, Putzer H, Condon C. 2010. Bacillus subtilis ribonucleases J1 and J2 form a complex with altered enzyme behaviour. Mol Microbiol 75:489–498. [PubMed]
42. Commichau FM, Rothe FM, Herzberg C, Wagner E, Hellwig D, Lehnik-Habrink M, Hammer E, Völker U, Stülke J, Volker U, Stulke J. 2009. Novel activities of glycolytic enzymes in Bacillus subtilis: interactions with essential proteins involved in mRNA processing. Mol Cell Proteomics 8:1350–1360. [PubMed]
43. Mathy N, Bénard L, Pellegrini O, Daou R, Wen T, Condon C. 2007. 5′-to-3′ exoribonuclease activity in bacteria: role of RNase J1 in rRNA maturation and 5′ stability of mRNA. Cell 129:681–692. [PubMed]
44. Li de la Sierra-Gallay I, Zig L, Jamalli A, Putzer H, de la Sierra-Gallay IL. 2008. Structural insights into the dual activity of RNase J. Nat Struct Mol Biol 15:206–212. [PubMed]
45. Linder P, Lemeille S, Redder P. 2014. Transcriptome-wide analyses of 5′-ends in RNase J mutants of a Gram-positive pathogen reveal a role in RNA maturation, regulation and degradation. PLoS Genet 10:e1004207. doi:10.1371/journal.pgen.1004207. [PubMed]
46. Hausmann S, Guimarães VA, Garcin D, Baumann N, Linder P, Redder P, Redder P. 2017. Both exo- and endo-nucleolytic activities of RNase J1 from Staphylococcus aureus are manganese dependent and active on triphosphorylated 5′-ends. RNA Biol 14:1431–1443. [PubMed]
47. Bugrysheva JV, Scott JR. 2010. The ribonucleases J1 and J2 are essential for growth and have independent roles in mRNA decay in Streptococcus pyogenes. Mol Microbiol 75:731–743. [PubMed]
48. Chen X, Liu N, Khajotia S, Qi F, Merritt J, Merritt J. 2015. RNases J1 and J2 are critical pleiotropic regulators in Streptococcus mutans. Microbiology 161:797–806. [PubMed]
49. Gao P, Pinkston KL, Bourgogne A, Murray BE, van Hoof A, Harvey BR. 2017. Functional studies of E. faecalis RNase J2 and its role in virulence and fitness. PLoS One 12:e0175212. doi:10.1371/journal.pone.0175212. [PubMed]
50. Luttinger A, Hahn J, Dubnau D. 1996. Polynucleotide phosphorylase is necessary for competence development in Bacillus subtilis. Mol Microbiol 19:343–356. [PubMed]
51. Durand S, Braun F, Helfer AC, Romby P, Condon C. 2017. sRNA-mediated activation of gene expression by inhibition of 5′-3′ exonucleolytic mRNA degradation. eLife 6:e23602. doi:10.7554/eLife.23602. [PubMed]
52. Liu N, Niu G, Xie Z, Chen Z, Itzek A, Kreth J, Gillaspy A, Zeng L, Burne R, Qi F, Merritt J. 2015. The Streptococcus mutans irvA gene encodes a trans-acting riboregulatory mRNA. Mol Cell 57:179–190. [PubMed]
53. Deutscher MP, Reuven NB. 1991. Enzymatic basis for hydrolytic versus phosphorolytic mRNA degradation in Escherichia coli and Bacillus subtilis. Proc Natl Acad Sci U S A 88:3277–3280. [PubMed]
54. Wang ZF, Whitfield ML, Ingledue TC, III, Dominski Z, Marzluff WF. 1996. The protein that binds the 3′ end of histone mRNA: a novel RNA-binding protein required for histone pre-mRNA processing. Genes Dev 10:3028–3040. [PubMed]
55. Liu B, Deikus G, Bree A, Durand S, Kearns DB, Bechhofer DH. 2014. Global analysis of mRNA decay intermediates in Bacillus subtilis wild-type and polynucleotide phosphorylase-deletion strains. Mol Microbiol 94:41–55. [PubMed]
56. Wang W, Bechhofer DH. 1996. Properties of a Bacillus subtilis polynucleotide phosphorylase deletion strain. J Bacteriol 178:2375–2382. [PubMed]
57. Deikus G, Bechhofer DH. 2007. Initiation of decay of Bacillus subtilis trp leader RNA. J Biol Chem 282:20238–20244. [PubMed]
58. De Lay N, Gottesman S. 2011. Role of polynucleotide phosphorylase in sRNA function in Escherichia coli. RNA 17:1172–1189. [PubMed]
59. Bandyra KJ, Sinha D, Syrjanen J, Luisi BF, De Lay NR. 2016. The ribonuclease polynucleotide phosphorylase can interact with small regulatory RNAs in both protective and degradative modes. RNA 22:360–372. [PubMed]
60. Khemici V, Linder P. 2016. RNA helicases in bacteria. Curr Opin Microbiol 30:58–66. [PubMed]
61. Fairman-Williams ME, Guenther UP, Jankowsky E. 2010. SF1 and SF2 helicases: family matters. Curr Opin Struct Biol 20:313–324. [PubMed]
62. Koo JT, Choe J, Moseley SL. 2004. HrpA, a DEAH-box RNA helicase, is involved in mRNA processing of a fimbrial operon in Escherichia coli. Mol Microbiol 52:1813–1826. [PubMed]
63. Salman-Dilgimen A, Hardy PO, Radolf JD, Caimano MJ, Chaconas G. 2013. HrpA, an RNA helicase involved in RNA processing, is required for mouse infectivity and tick transmission of the Lyme disease spirochete. PLoS Pathog 9:e1003841. doi:10.1371/journal.ppat.1003841. [PubMed]
64. Granato LM, Picchi SC, Andrade MO, Takita MA, de Souza AA, Wang N, Machado MA. 2016. The ATP-dependent RNA helicase HrpB plays an important role in motility and biofilm formation in Xanthomonas citri subsp. citri. BMC Microbiol 16:55. doi:10.1186/s12866-016-0655-1. [PubMed]
65. Uson ML, Ordonez H, Shuman S. 2015. Mycobacterium smegmatis HelY is an RNA-activated ATPase/dATPase and 3′-to-5′ helicase that unwinds 3′-tailed RNA duplexes and RNA:DNA hybrids. J Bacteriol 197:3057–3065. [PubMed]
66. Giraud C, Hausmann S, Lemeille S, Prados J, Redder P, Linder P. 2015. The C-terminal region of the RNA helicase CshA is required for the interaction with the degradosome and turnover of bulk RNA in the opportunistic pathogen Staphylococcus aureus. RNA Biol 12:658–674. [PubMed]
67. Pandiani F, Brillard J, Bornard I, Michaud C, Chamot S, Nguyen-the C, Broussolle V. 2010. Differential involvement of the five RNA helicases in adaptation of Bacillus cereus ATCC 14579 to low growth temperatures. Appl Environ Microbiol 76:6692–6697. [PubMed]
68. Lehnik-Habrink M, Rempeters L, Kovács ÁT, Wrede C, Baierlein C, Krebber H, Kuipers OP, Stülke J. 2013. DEAD-box RNA helicases in Bacillus subtilis have multiple functions and act independently from each other. J Bacteriol 195:534–544. [PubMed]
69. Bäreclev C, Vaitkevicius K, Netterling S, Johansson J. 2014. DExD-box RNA-helicases in Listeria monocytogenes are important for growth, ribosomal maturation, rRNA processing and virulence factor expression. RNA Biol 11:1457–1466. [PubMed]
70. Redder P, Hausmann S, Khemici V, Yasrebi H, Linder P. 2015. Bacterial versatility requires DEAD-box RNA helicases. FEMS Microbiol Rev 39:392–412. [PubMed]
71. Lehnik-Habrink M, Pförtner H, Rempeters L, Pietack N, Herzberg C, Stülke J. 2010. The RNA degradosome in Bacillus subtilis: identification of CshA as the major RNA helicase in the multiprotein complex. Mol Microbiol 77:958–971.
72. Roux CM, DeMuth JP, Dunman PM. 2011. Characterization of components of the Staphylococcus aureus mRNA degradosome holoenzyme-like complex. J Bacteriol 193:5520–5526. [PubMed]
73. Oun S, Redder P, Didier JP, François P, Corvaglia AR, Buttazzoni E, Giraud C, Girard M, Schrenzel J, Linder P. 2013. The CshA DEAD-box RNA helicase is important for quorum sensing control in Staphylococcus aureus. RNA Biol 10:157–165. [PubMed]
74. Newman JA, Hewitt L, Rodrigues C, Solovyova AS, Harwood CR, Lewis RJ. 2012. Dissection of the network of interactions that links RNA processing with glycolysis in the Bacillus subtilis degradosome. J Mol Biol 416:121–136. [PubMed]
75. Salvo E, Alabi S, Liu B, Schlessinger A, Bechhofer DH. 2016. Interaction of Bacillus subtilis polynucleotide phosphorylase and RNase Y: structural mapping and effect on mRNA turnover. J Biol Chem 291:6655–6663. [PubMed]
76. Cascante-Estepa N, Gunka K, Stülke J. 2016. Localization of components of the RNA-degrading machine in Bacillus subtilis. Front Microbiol 7:1492. doi:10.3389/fmicb.2016.01492. [PubMed]
77. Jamalli A, Hébert A, Zig L, Putzer H. 2014. Control of expression of the RNases J1 and J2 in Bacillus subtilis. J Bacteriol 196:318–324. [PubMed]
78. DiChiara JM, Liu B, Figaro S, Condon C, Bechhofer DH. 2016. Mapping of internal monophosphate 5′ ends of Bacillus subtilis messenger RNAs and ribosomal RNAs in wild-type and ribonuclease-mutant strains. Nucleic Acids Res 44:3373–3389. [PubMed]
79. Zhang X, Zhu Q, Tian T, Zhao C, Zang J, Xue T, Sun B. 2015. Identification of RNAIII-binding proteins in Staphylococcus aureus using tethered RNAs and streptavidin aptamers based pull-down assay. BMC Microbiol 15:102. doi:10.1186/s12866-015-0435-3. [PubMed]
80. Condon C, Putzer H. 2002. The phylogenetic distribution of bacterial ribonucleases. Nucleic Acids Res 30:5339–5346. [PubMed]
81. Kaberdin VR, Singh D, Lin-Chao S. 2011. Composition and conservation of the mRNA-degrading machinery in bacteria. J Biomed Sci 18:23. doi:10.1186/1423-0127-18-23. [PubMed]
82. Bronesky D, Wu Z, Marzi S, Walter P, Geissmann T, Moreau K, Vandenesch F, Caldelari I, Romby P. 2016. Staphylococcus aureus RNAIII and its regulon link quorum sensing, stress responses, metabolic adaptation, and regulation of virulence gene expression. Annu Rev Microbiol 70:299–316. [PubMed]
83. Obana N, Shirahama Y, Abe K, Nakamura K. 2010. Stabilization of Clostridium perfringens collagenase mRNA by VR-RNA-dependent cleavage in 5′ leader sequence. Mol Microbiol 77:1416–1428. [PubMed]
84. Boisset S, Geissmann T, Huntzinger E, Fechter P, Bendridi N, Possedko M, Chevalier C, Helfer AC, Benito Y, Jacquier A, Gaspin C, Vandenesch F, Romby P. 2007. Staphylococcus aureus RNAIII coordinately represses the synthesis of virulence factors and the transcription regulator Rot by an antisense mechanism. Genes Dev 21:1353–1366. [PubMed]
85. Bandyra KJ, Luisi BF. 2018. RNase E and the high fidelity orchestration of RNA metabolism. Microbiol Spectrum 6(2):RWR-0008-2017.
Loading

Article metrics loading...

/content/journal/microbiolspec/10.1128/microbiolspec.RWR-0003-2017
2018-04-13
2018-07-18

Abstract:

RNases are key enzymes involved in RNA maturation and degradation. Although they play a crucial role in all domains of life, bacteria, archaea, and eukaryotes have evolved with their own sets of RNases and proteins modulating their activities. In bacteria, these enzymes allow modulation of gene expression to adapt to rapidly changing environments. Today, >20 RNases have been identified in both and , the paradigms of the Gram-negative and Gram-positive bacteria, respectively. However, only a handful of these enzymes are common to these two organisms and some of them are essential to only one. Moreover, although sets of RNases can be very similar in closely related bacteria such as the and , the relative importance of individual enzymes in posttranscriptional regulation in these organisms varies. In this review, we detail the role of the main RNases involved in RNA maturation and degradation in Gram-positive bacteria, with an emphasis on the roles of RNase J1, RNase III, and RNase Y. We also discuss how other proteins such as helicases can modulate the RNA-degradation activities of these enzymes.

Highlighted Text: Show | Hide
Loading full text...

Full text loading...

Figures

Image of FIGURE 1
FIGURE 1

A schematic view of the pathways involved in RNA degradation in Gram-positive bacteria. (A) Primary mRNA transcripts in bacteria are protected at their 5′ end by a triphosphate group. Initiation of mRNA degradation can involve an endoribonuclease cut (RNase Y or RNase III), which is the limiting step. This step generates a downstream product with a 5′ monophosphate extremity, which can be attacked by the 5′-to-3′ exoribonuclease RNase J (in blue). The 3′ end of the upstream cleavage product is degraded by 3′-to-5′ exoribonucleases (in green), principally PNPase in . (B) In the alternative degradation pathway, the 5′ triphosphate of the mRNA can be converted to a 5′ monophosphate by an RNA pyrophosphohydrolase (e.g., RppH [yellow square]). After removal of the triphosphate, the mRNA can be degraded by the 5′-to-3′ exoribonuclease RNase J or by RNase Y in cases where initial cleavage by RNase Y is sensitive to the 5′ status of the mRNA.

Source: microbiolspec April 2018 vol. 6 no. 2 doi:10.1128/microbiolspec.RWR-0003-2017
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 2
FIGURE 2

Comparison of the domain structure of RNases described in this review. All structures are based on RNases found in except RNase E (structure from ). Abbreviations: H, RNase H domain; CCD, coiled-coil domain; TMD, transmembrane domain; β-Lact., β-lactamase domain. RNA binding domains: S1, S1 domain; KH, KH domain; AR2, AR2 domain; RBD, RNA binding domain; dsRBD, double-stranded RNA binding omain.

Source: microbiolspec April 2018 vol. 6 no. 2 doi:10.1128/microbiolspec.RWR-0003-2017
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 3
FIGURE 3

(A) Role of RNase Y in the regulation of expression by the -encoded sRNA VR-RNA. VR-RNA binds the 5′ UTR of the mRNA, encoding a collagenase, and triggers cleavage of the mRNA by RNase Y. This cleavage in turn stabilizes the mRNA by creating a stem-loop structure at the 5′ end of the mRNA. The binding of the sRNA also stimulates translation by releasing the SD sequence ( 83 ). (B) The RoxS sRNA binds to the SD sequence of mRNA, inhibiting its translation. The reduction of the ribosome trafficking on the mRNA uncovers RNase Y cleavage sites. The sRNA is in blue, the mRNA target is colored in black, the SD sequence is in gray, ribosomes are in blue, and RNase Y is represented by red scissors.

Source: microbiolspec April 2018 vol. 6 no. 2 doi:10.1128/microbiolspec.RWR-0003-2017
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 4
FIGURE 4

Regulation of the expression of the operon. When tryptophan is not limiting, the TRAP protein binds to the 5′ UTR of the operon and facilitates transcriptional termination at the terminator. The aborted transcript is probably cleaved by either RNase Y or J1 followed by the attack of the new 3′ end by PNPase. This degradation allows release of the TRAP protein for further regulation (left). When tryptophan is limiting, TRAP complex does not bind to the operon and an antiterminator structure can be formed to allow transcription of the mRNA (right). The mRNA is colored in black, the SD sequence is in gray, Ter is for terminator and anti-Ter for antiterminator, TRAP proteins are colored in green, PNPase is represented by a light green Pacman symbol, and RNase Y/J1 by red scissors.

Source: microbiolspec April 2018 vol. 6 no. 2 doi:10.1128/microbiolspec.RWR-0003-2017
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 5
FIGURE 5

Role of RNase III in the regulation of gene expression by antisense and -encoded sRNA. (A) type I TA system TxpA/RatA. The 3′ end of the RatA sRNA forms a large duplex with the mRNA, which is then cleaved by RNase III. (B) The excludon in . One of the transcripts of the operon starts with the Lmo0677 open reading frame on the opposite strand. The long 5′ UTR of the operon (Anti0677) is antisense to the operon. The duplex RNA is probably cleaved by RNase III, although this has not been shown directly. (C) RNAIII represses translation of the mRNA by sequestering the SD sequence ( 84 ). The sRNA is in blue, the mRNA target is colored in black, the SD sequence is in gray, and RNase III represented by red scissors.

Source: microbiolspec April 2018 vol. 6 no. 2 doi:10.1128/microbiolspec.RWR-0003-2017
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 6
FIGURE 6

Role of RNase J in the regulation of gene expression by antisense and -encoded sRNA. (A) RoxS sRNA forms base-pairing interactions with the first 7 nucleotides of the mRNA to create a stable RNA helix at the 5′ end of the mRNA and protect it from degradation by RNase J1 (left) ( 50 ). RoxS binding also stimulates translation by rendering the SD sequence more accessible. This increase of translation protects the mRNA from degradation by RNase Y (left). In contrast, when RoxS does not bind to , the 5′ end of this mRNA is free and can be attacked by RNase J1. The SD sequence of mRNA also stays embedded in a stem-loop structure that reduces its translation efficiency and promotes degradation by RNase Y (right). Exoribonucleolytic activity of RNase J1 is represented by a light blue Pacman symbol. The sRNA is in blue, the mRNA target is colored in black, the SD sequence is in gray, and ribosomes are in blue. (B) The 5′ UTR of the mRNA base-pairs with the coding sequence of the mRNA to block endoribonucleolytic cleavage by RNase J2 ( 52 ). The inhibition of the endoribonucleolytic activity of RNase J2 is represented by red scissors.

Source: microbiolspec April 2018 vol. 6 no. 2 doi:10.1128/microbiolspec.RWR-0003-2017
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 7
FIGURE 7

Schematic representation of the DLN. RNase Y is anchored at the membrane and can transiently interact with metabolic enzymes (enolase and phosphofructokinase) and the 3′-to-5′ exoribonuclease PNPase. Domains of interaction between RNase Y and each partner are not characterized. Transient interactions are represented by two-headed arrows. RNase Y domains are indicated (TMD, transmembrane domain; CCD, coiled-coil domain; KH, KH domain; HD, HD domain with the catalytic site represented by red scissors).

Source: microbiolspec April 2018 vol. 6 no. 2 doi:10.1128/microbiolspec.RWR-0003-2017
Permissions and Reprints Request Permissions
Download as Powerpoint

Tables

Generic image for table
TABLE 1

RNases and their functions

Source: microbiolspec April 2018 vol. 6 no. 2 doi:10.1128/microbiolspec.RWR-0003-2017

Supplemental Material

No supplementary material available for this content.

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error