RNA degradation in Bacillus subtilis: An interplay of essential endo- and exoribonucleasesmmi

Molecular Microbiology

Volumn 84, Issue 6, 2012, Pages 1005-1017

  Lehnik Habrink, Martin ^a   Lewis, Richard J ^b   Mäder, Ulrike ^c   Stülke, Jörg ^a  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

^b NEWCASTLE UNIVERSITY   (United Kingdom)

^c UNIVERSITY OF GREIFSWALD   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

6 PHOSPHOFRUCTOKINASE; BACTERIAL RNA; DEAD BOX PROTEIN; ENOLASE; EXORIBONUCLEASE; GLYCOSYLTRANSFERASE; MESSENGER RNA; POLYRIBONUCLEOTIDE NUCLEOTIDYLTRANSFERASE; PROTEIN CSHA; RIBONUCLEASE; RIBONUCLEASE E; RIBONUCLEASE J1; RIBONUCLEASE J2; RIBONUCLEASE Y; RNA HELICASE; RNA PYROPHOSPHORYLASE; UNCLASSIFIED DRUG;

BACILLUS SUBTILIS; BACTERIAL VIRULENCE; ENZYME ACTIVITY; ENZYME SPECIFICITY; ESCHERICHIA COLI; GENE EXPRESSION REGULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN PROTEIN INTERACTION; PROTEIN RNA BINDING; PROTEIN TARGETING; REVIEW; RNA DEGRADATION; RNA METABOLISM; RNA PROCESSING; RNA STABILITY; STRUCTURE ACTIVITY RELATION; TRANSCRIPTION REGULATION;

BACILLUS SUBTILIS; ENDORIBONUCLEASES; EXORIBONUCLEASES; MODELS, BIOLOGICAL; MODELS, MOLECULAR; RNA; RNA STABILITY;

BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; POSIBACTERIA;

EID: 84865165883     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2012.08072.x     Document Type: Review

References (80)

1. Agaisse, H., and Lereclus, D. (1996) STAB-SD: a Shine-Dalgarno sequence in the 5' untranslated region is a determinant of mRNA stability. Mol Microbiol 20: 633-643.
2. Ait-Bara, S., and Carpousis, A.J. (2010) Characterization ofthe RNA degradosome of Pseudoalteromonas haloplanktis: conservation of the RNase E-RhlB interaction in the gammaproteobacteria. J Bacteriol 192: 5413-5432.
3. Babitzke, P., and Kushner, S.R. (1991) The Ams (altered mRNAstability) protein and ribonuclease E are encoded by the same structural gene of Escherichia coli. Proc Natl Acad Sci USA 88: 1-5.
4. Bechhofer, D.H. (2009) Messenger RNA decay and maturation in Bacillus subtilis. Prog Mol Biol Transl Sci 85: 231-273.
5. Bernstein, J.A., Lin, P.H., Cohen, S.N., and Lin-Chao, S. (2004) Global analysis of Escherichia coli RNA degradosome function using DNA microarrays. Proc Natl Acad Sci USA 101: 2758-2763.
6. Bouvier, M., and Carpousis, A.J. (2011) A tale of two mRNA degradation pathways mediated by RNase E. Mol Microbiol 82: 1305-1310.
7. Bruscella, P., Shahbabian, K., Laalami, S., and Putzer, H. (2011) RNase Y is responsible for uncoupling the expression of translation factor IF3 from that of the ribosomal proteins L35 and L20 in Bacillus subtilis. Mol Microbiol 81: 1526-1541.
8. Bugrysheva, J.V., and Scott, J.R. (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.
9. Callaghan, A.J., Aurikko, J.P., Ilag, L.L., Grossmann, J.G., Chandran, V., Kühnel, K., et al. (2004) Studies of the RNA degradosome-organizing domain of the Escherichia coli ribonuclease RNase E. J Mol Biol 340: 965-979.
10. Carpousis, A.J. (2007) The RNA degradosome of Escherichia coli: an mRNA-degrading machine assembled on RNase E. Annu Rev Microbiol 61: 71-87.
11. Carpousis, A.J., Luisi, B.F., and McDowall, K.J. (2009) Endonucleolytic initiation of mRNA decay in Escherichia coli. Prog Mol Biol Transl Sci 85: 91-135.
12. Chen, Z., Itzek, A., Malke, H., Ferretti, J.J., and Kreth, J. (2012) Dynamics of speB mRNA transcripts in Streptococcus pyogenes. J Bacteriol 194: 1417-1426.
13. Collins, J.A., Irnov, I., Baker, S., and Winkler, W.C. (2007) Mechanism of mRNAdestabilization by the glmS ribozyme. Genes Dev 21: 3356-3368.
14. Commichau, F.M., Rothe, F.M., Herzberg, C., Wagner, E., Hellwig, D., Lehnik-Habrink, M., et al. (2009) Novel activities of glycolytic enzymes in Bacillus subtilis: interactions with essential proteins involved in mRNA processing. Mol Cell Proteomics 8: 1350-1360.
15. Condon, C. (2003) RNA processing and degradation in Bacillus subtilis. Microbiol Mol Biol Rev 67: 157-174.
16. Condon, C. (2010) What is the role of RNase J in RNA turnover? RNA Biol 7: 316-321.
17. Condon, C., and Bechhofer, D. (2011) Regulated RNAstability in the Gram-positives. Curr Opin Microbiol 14: 148-154.
18. Condon, C., and Putzer, H. (2002) The phylogenetic distribution of bacterial ribonucleases. Nucleic Acids Res 30: 5339-5346.
19. Condon, C., Putzer, H., and Grunberg-Manago, M. (1996) Processing of the leader mRNA plays a major role in the induction of thrS expression following threonine starvation in Bacillus subtilis. Proc Natl Acad Sci USA 93: 6992-6997.
20. Daou-Chabo, R., Mathy, N., Benard, L., and Condon, C. (2009) Ribosomes initiating translation of the hbs mRNA protect it from 5'-to-3' exoribonucleolytic degradation by RNase J1. Mol Microbiol 71: 1538-1550.
21. Deana, A., Celesnik, H., and Belasco, J.G. (2008) The bacterial enzyme RppH triggers messenger RNA degradation by 5' pyrophosphate removal. Nature 451: 355-358.
22. Deikus, G., and Bechhofer, D.H. (2007) Initiation of decay of Bacillus subtilis trp leader RNA. J Biol Chem 282: 20238-20244.
23. Deikus, G., and Bechhofer, D.H. (2009) Bacillus subtilis trp leader RNA: RNase J1 endonuclease cleavage specificity and PNPase processing. J Biol Chem 284: 26394-26401.
24. Deikus, G., and Bechhofer, D.H. (2011) 5' End-independent RNase J1 endonuclease cleavage of Bacillus subtilis model RNA. J Biol Chem 286: 34932-34940.
25. Deikus, G., Babitzke, P., and Bechhofer, D.H. (2004) Recycling of a regulatory protein by degradation of the RNA to which it binds. Proc Natl Acad Sci USA 101: 2747-2751.
26. Deikus, G., Condon, C., and Bechhofer, D.H. (2008) Role of Bacillus subtilis RNase J1 endonuclease and 5'-exonuclease activities in trp leader RNA turnover. J Biol Chem 283: 17158-17167.
27. Diethmaier, C., Pietack, N., Gunka, K., Wrede, C., Lehnik-Habrink, M., Herzberg, C., et al. (2011) A novel factor controlling bistability in Bacillus subtilis: the YmdB protein affects flagellin expression and biofilm formation. J Bacteriol 193: 5997-6007.
28. Dorléans, A., Li de la Sierra-Gallay, I., Piton, J., Zig, I., Gilet, L., Putzer, H., and 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.
29. Durand, S., Gilet, L., Bessières, P., Nicolas, P., and 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.
30. Erce, M.A., Low, J.K., and Wilkins, M.R. (2010) Analysis of the RNA degradosome complex in Vibrio angustum S14. FEBS J 277: 5161-5173.
31. Even, S., Pellegrini, O., Zig, L., Labas, V., Vinh, J., Brechemmier-Baey, D., and 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.
32. Evguenieva-Hackenberg, E., Roppelt, V., Lassek, C., and Klug, G. (2011) Subcellular localization of RNA degrading proteins and protein complexes in prokaryotes. RNA Biol 8: 49-54.
33. Fang, M., Zeisberg, W.M., Condon, C., Ogryzko, V., Danchin, A., and Mechold, U. (2009) Degradation of nanoRNA is performed by multiple redundant RNases in Bacillus subtilis. Nucleic Acids Res 37: 5114-5125.
34. Ghosh, S., and Deutscher, M.P. (1999) Oligoribonuclease is an essential component of the mRNA decay pathway. Proc Natl Acad Sci USA 96: 4372-4377.
35. Hambraeus, G., von Wachenfeldt, C., and Hederstedt, L. (2003) Genome-wide survey of mRNA half-lives in Bacillus subtilis identifies extremely stable mRNAs. Mol Genet Genomics 269: 706-714.
36. Hardwick, S.W., Chan, V.S.Y., Broadhurst, R.W., and Luisi, B. (2011) An RNA degradosome assembly in Caulobacter crescentus. Nucleic Acids Res 39: 1449-1459.
37. Herskovitz, M.A., and Bechhofer, D.H. (2000) Endoribonuclease RNase III is essential in Bacillus subtilis. Mol Microbiol 38: 1027-1033.
38. Homuth, G., Mogk, A., and Schumann, W. (1999) Posttranscriptional regulation of the Bacillus subtilis dnaK operon. Mol Microbiol 32: 1183-1197.
39. Hsieh, J., and Fierke, C.A. (2009) Conformational change in the Bacillus subtilis RNase P holoenzyme-pre-tRNA complex enhances substrate affinity and limits cleavage rate. RNA 15: 1565-1577.
40. Jahn, N., Preis, H., Wiedemann, C., and Brantl, S. (2012) BsrG/SR4 from Bacillus subtilis -the first heat-shocksensitive type I toxin-antitoxin system. Mol Microbiol 83: 579-598.
41. Kaito, C., Kurokawa, K., Matsumoto, Y., Terao, Y., Kawabata, S., Hamada, S., and Sekimizu, K. (2005) Silkworm pathogenic bacteria infection model for identification of novel virulence genes. Mol Microbiol 56: 934-944.
42. Kang, S.O., Caparon, M.G., and Cho, K.H. (2010) Virulence gene regulation by CvfA, a putative RNase: the CvfAenolase complex in Streptococcus pyogenes links nutritional stress, growth-phase control, and virulence gene expression. Infect Immun 78: 2754-2767.
43. Klein, D.J., and Ferré-D'Amaré, A.R. (2006) Structural basis of glmS ribozyme activation by glucosamine-6-phosphate. Science 313: 1752-17566.
44. Kushner, S.R. (2002) mRNA decay in Escherichia coli comes of age. J Bacteriol 184: 4658-4665.
45. Laalami, S., and Putzer, H. (2011) mRNA degradation and maturation in prokaryotes: the global players. BioMol Concepts 2: 491-506.
46. Lehnik-Habrink, M., Pförtner, H., Rempeters, L., Pietack, N., Herzberg, C., and Stülke, J. (2010) The RNA degradosome in Bacillus subtilis: identification of CshA as the major RNA helicase in the multi-protein complex. Mol Microbiol 77: 958-971.
47. Lehnik-Habrink, M., Schaffer, M., Mäder, U., Diethmaier, C., Herzberg, C., and Stülke, J. (2011a) RNA processing in Bacillus subtilis: identification of targets of the essential RNase Y. Mol Microbiol 81: 1459-1473.
48. Lehnik-Habrink, M., Newman, M., Rothe, F.M., Solovyova, A.S., Rodrigues, C., Herzberg, C., et al. (2011b) 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.
49. Li de la Sierra-Gallay, I., Zig, L., Jamalli, A., and Putzer, H. (2008) Structural insights into the dual role of RNase J. Nat Struct Mol Biol 15: 206-212.
50. Linder, P., and Jankowsky, E. (2011) From unwinding to clamping -the DEAD box RNA helicase family. Nat Rev Mol Cell Biol 12: 505-516.
51. Liou, G.G., Jane,W.N., Cohen, S.N., Lin, N.S., and Lin-Chao, S. (2001) RNA degradosomes exist in vivo in Escherichia coli as multicomponent complexes associated with the cytoplasmic membrane via the N-terminal region of ribonuclease E. Proc Natl Acad Sci USA 98: 63-68.
52. Ludwig, H., Homuth, G., Schmalisch, M., Dyka, F.M., Hecker, M., and Stülke, J. (2001) Transcription of glycolytic genes and operons in Bacillus subtilis: evidence for the presence of multiple levels of control of the gapA operon. Mol Microbiol 41: 409-422.
53. Luttinger, A., Hahn, J., and Dubnau, D. (1996) Polynucleotide phosphorylase is necessary for competence development in Bacillus subtilis. Mol Microbiol 19: 343-356.
54. McDowall, K.J., Kaberdin, V.R., Wu, S.W., Cohen, S.N., and Lin-Chao, S. (1995) Site-specific RNase E cleavage of oligonucleotides and inhibition by stem-loops. Nature 374: 287-290.
55. Mackie, G.A. (1998) RNase E is a 5'-end-dependent endonuclease. Nature 395: 720-723.
56. Mäder, U., Hennig, S., Hecker, M., and Homuth, G. (2004) Transcriptional organization and posttranscriptional regulation of the Bacillus subtilis branched-chain amino acid biosynthesis genes. J Bacteriol 186: 2240-2252.
57. Mäder, U., Zig, L., Kretschmer, J., Homuth, G., and Putzer, H. (2008) mRNA processing by RNases J1 and J2 affects Bacillus subtilis gene expression on a global scale. Mol Microbiol 70: 183-196.
58. Mäder, U., Schmeisky, A.G., Flórez, L.A., and Stülke, J. (2012) SubtiWiki -a comprehensive community resource for the model organism Bacillus subtilis. Nucleic Acids Res 40: D1278-D1287.
59. Marcaida, M.J., DePristo, M.A., Chandran, V., Carpousis, A.J., and Luisi, B.F. (2006) The RNA degradosome: life in the fast lane of adaptive molecular evolution. Trends Biochem Sci 31: 359-365.
60. Mathy, N., Bénard, L., Pellegrini, O., Daou, R., Wen, T., and 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.
61. Mathy, N., Hébert, A., Mervelet, P., Bénard, L., Dorléans, A., de la Sierra-Gallay, I.L., et al. (2010) Bacillus subtilis ribonucleases J1 and J2 form a complex with altered enzyme behaviour. Mol Microbiol 75: 489-498.
62. Meinken, C., Blencke, H.M., Ludwig, H., and Stülke, J. (2003) Expression of the glycolytic gapA operon in Bacillus subtilis: differential syntheses of proteins encoded by the operon. Microbiology 149: 751-761.
63. Nagata, M., Kaito, C., and Sekimizu, K. (2008) Phosphodiesterase activity of CvfA is required for virulence in Staphyococcus aureus. J Biol Chem 283: 2176-2184.
64. Nevo-Dinur, K., Nussbaum-Schochat, A., Ben-Yehuda, S., and Amster-Choder, O. (2011) Translation-independent localization of mRNA in E. coli. Science 331: 1081-1084.
65. Newman, J., Hewitt, L., Rodrigues, C., Solovyova, A.S., Harwood, C.R., and Lewis, R.J. (2011) Unusual, dual endoand exonuclease activity in the degradosome explained by crystal structure analysis of RNase J1. Structure 19: 1241-1251.
66. Newman, J., Hewitt, L., Rodrigues, C., Solovyova, A.S., Harwood, C.R., and Lewis, R.J. (2012) Dissection of the network of interactions that links RNA processing with glycoloysis in the Bacillus subtilis degradosome. J Mol Biol 416: 121-136.
67. Pellegrini, O., Nezzar, J., Marchfelder, A., Putzer, H., and Condon, C. (2003) Endonucleolytic processing of CCAless tRNA precursors by RNase Z in Bacillus subtilis. EMBO J 22: 4534-4543.
68. Prud'homme-Généreux, A., Beran, R.K., Iost, I., Ramey, C.S., Mackie, G.A., and Simons, R.W. (2004) Physical and functional interactions among RNase E, polynucleotide phosphorylase and the cold-shock protein, CsdA: evidence for a 'cold shock degradosome'. Mol Microbiol 54: 1409-1421.
69. Richards, J., Liu, Q., Pellegrini, O., Celesnik, H., Yao, S., Bechhofer, D.H., et al. (2011) An RNA pyrophosphohydrolase triggers 5'-exonucleolytic degradation of mRNA in Bacillus subtilis. Mol Cell 43: 940-949.
70. Roux, C.M., DeMuth, J.P., and Dunman, P.M. (2011) Characterization of components of the Staphylococcus aureus RNA degradosome holoenzyme-like complex. J Bacteriol 193: 5520-5526.
71. Segev, E., Smith, Y., and Ben-Yehuda, S. (2012) RNA dynamics in aging bacterial spores. Cell 148: 139-149.
72. Shahbabian, K., Jamalli, A., Zig, L., and Putzer, H. (2009) RNase Y, a novel endoribonuclease, initiates riboswitch turnover in Bacillus subtilis. EMBO J 28: 3523-3533.
73. Sharp, J.S., and Bechhofer, D.H. (2005) Effect of 5'-proximal elements on decay of a model RNA in Bacillus subtilis. Mol Microbiol 57: 484-495.
74. Stead, M.B., Marshburn, S., Mohanty, B.K., Mitra, J., Pena Castillo, L., Ray, D., et al. (2011) Analysis of Escherichia coli RNase E and RNase III activity in vivo using tiling microarrays. Nucleic Acids Res 39: 3188-3203.
75. Vanzo, N.F., Li, Y.S., Py, B., Blum, E., Higgins, C.F., Raynal, L.C., et al. (1998) Ribonuclease E organizes the protein interactions in the Escherichia coli RNA degradosome. Genes Dev 12: 2770-2781.
76. Wang, W., and Bechhofer, D.B. (1996) Properties of a Bacillus subtilis polynucleotide phosphorylase deletion strain. J Bacteriol 178: 2375-2382.
77. Yao, S., and Bechhofer, D.H. (2010) Initiation of decay of Bacillus subtilis rpsO mRNA by endoribonuclease RNase Y. J Bacteriol 192: 3279-3286.
78. Yao, S., Blaustein, J.B., and Bechhofer, D.H. (2007) Processing of Bacillus subtilis small cytoplasmic RNA: evidence for an additional endonuclease cleavage site. Nucleic Acids Res 35: 4464-4473.
79. Yao, S., Blaustein, J.B., and Bechhofer, D.H. (2008) Erythromycin-induced ribosome stalling and RNase J1-mediated mRNA processing in Bacillus subtilis. Mol Microbiol 69: 1439-1449.
80. Yao, S., Richards, J., Belasco, J.G., and Bechhofer, D.H. (2011) Decay of model mRNA in Bacillus subtilis by a combination of RNase J1 5' exonuclease and RNase Y endoribonuclease activities. J Bacteriol 193: 6384-6386.