RNA processing in Bacillus subtilis: Identification of targets of the essential RNase Y

Molecular Microbiology

Volumn 81, Issue 6, 2011, Pages 1459-1473

  Lehnik Habrink, Martin ^a   Schaffer, Marc ^b   Mäder, Ulrike ^b   Diethmaier, Christine ^a   Herzberg, Christina ^a   Stülke, Jörg ^a  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

^b UNIVERSITY OF GREIFSWALD   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; RIBONUCLEASE; RIBONUCLEASE Y; TRANSCRIPTOME; UNCLASSIFIED DRUG;

ARTICLE; BACILLUS SUBTILIS; BIOFILM; CONTROLLED STUDY; GENE OVEREXPRESSION; NONHUMAN; OPERON; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN STABILITY; PROTEIN TARGETING; RNA METABOLISM; RNA PROCESSING; RNA TRANSCRIPTION;

BACILLUS SUBTILIS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; RIBONUCLEASES; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA STABILITY; SUBSTRATE SPECIFICITY;

BACILLUS SUBTILIS; POSIBACTERIA;

EID: 80052698341     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2011.07777.x     Document Type: Article

References (64)

1. Abramoff, M.D., Magelhaes, P.J., and Ram, S.J. (2004) Image processing with ImageJ. Biophotonics Int 11: 36-42.
2. Ait-Bara, S., and Carpousis, A.J. (2010) Characterization of the 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 mRNA stability) protein and ribonuclease E are encoded by the same structural gene of Escherichia coli. Proc Natl Acad Sci USA 88: 1-5.
4. Belasco, J.G. (2010) All things must pass: contrasts and commonalities in eukaryotic and bacterial mRNA decay. Nat Rev Mol Cell Biol 11: 467-478.
5. Bessarab, D.A., Kaberdin, V.R., Wei, C.L., Liou, G.G., and Lin-Chao, S. (1998) RNA components of Escherichia coli RNA degradosome: evidence for rRNA decay. Proc Natl Acad Sci USA 95: 3157-3161.
6. Branda, S.S., González-Pastor, J.E., Ben-Yehuda, S., Losick, R., and Kolter, R. (2001) Fruiting body formation by Bacillus subtilis. Proc Natl Acad Sci USA 98: 11621-11626.
7. Britton, R.A., Wen, T., Schaefer, L., Pellegrini, O., Uicker, W.C., Mathy, N., etal. (2007) Maturation of the 5' end of Bacillus subtilis 16S rRNA by the essential ribonuclease YkqC/RNase J1. Mol Microbiol 63: 127-138.
8. Butcher, B.G., Lin, Y.P., and Helmann, J.D. (2007) The yydFGHIJ operon of Bacillus subtilis encodes a peptide that induces the LiaRS two-component system. J Bacteriol 189: 8616-8625.
9. Carpousis, A.J. (2007) The RNA degradosome of Escherichia coli: an mRNA-degrading machine assembled on RNase E. Annu Rev Microbiol 61: 71-87.
10. Chai, Y., Norman, T., Kolter, R., and Losick, R. (2010) An epigenetic switch governing daughter cell separation in Bacillus subtilis. Genes Dev 24: 754-765.
11. Charbonnier, Y., Gettler, B., François, P., Bento, M., Renzoni, A., Vaudaux, P., etal. (2005) A generic approach for the design of whole-genome oligoarrays, validated for genomotyping, deletion mapping and gene expression analysis on Staphylococcus aureus. BMC Genomics 6: 95.
12. Chu, F., Kearns, D.B., Branda, S.S., Kolter, R., and Losick, R. (2006) Targets of the master regulator of biofilm formation in Bacillus subtilis. Mol Microbiol 59: 1216-1228.
13. Commichau, F.M., Herzberg, C., Tripal, P., Valerius, O., and Stülke, J. (2007) A regulatory protein-protein interaction governs glutamate biosynthesis in Bacillus subtilis: the glutamate dehydrogenase RocG moonlights in controlling the transcription factor GltC. Mol Microbiol 65: 642-654.
14. Commichau, F.M., Rothe, F.M., Herzberg, C., Wagner, E., Hellwig, D., Lehnik-Habrink, M., etal. (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., and Bechhofer, D. (2011) Regulated RNA stability in the Gram-positives. Curr Opin Microbiol 14: 148-154.
16. 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.
17. Condon, C., Putzer, H., Luo, D., and Grunberg-Manago, M. (1997) Processing of the Bacillus subtilis thrS leader mRNA is RNase E-dependent in Escherichia coli. J Mol Biol 268: 235-242.
18. Deikus, G., Babitzke, P., and Bechhofer, D. (2004) Recycling of a regulatory protein by degradation of the RNA to which it binds. Proc Natl Acad Sci USA 101: 2747-2751.
19. Deikus, G., Condon, C., and Bechhofer, D. (2008) Role of Bacillus subtilis RNase J1 endonuclease and 5'-exonuclease activities in trp leader RNA turnover. J Biol Chem 283: 17158-17167.
20. Diwa, A., Bricker, A.L., Jain, C., and Belasco, J.G. (2000) An evolutionarily conserved RNA stem-look functions as a sensor that directs feedback regulation of RNase E gene expression. Genes Dev 14: 1249-1260.
21. 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.
22. Gollnick, P., Babitzke, P., Antson, A., and Yanofsky, C. (2005) Complexity in regulation of tryptophan biosynthesis in Bacillus subtilis. Annu Rev Genet 39: 47-68.
23. González-Pastor, J.E., Hobbs, E.C., and Losick, R. (2003) Cannibalism by sporulating bacteria. Science 301: 510-513.
24. 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.
25. 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.
26. Homuth, G., Mogk, A., and Schumann, W. (1999) Post-transcriptional regulation of the Bacillus subtilis dnaK operon. Mol Microbiol 32: 1183-1197.
27. Hunt, A., Rawlings, J.P., Thomaides, H.B., and Errington, J. (2006) Functional analysis of 11 putative essential genes in Bacillus subtilis. Microbiology 152: 2895-2907.
28. Irnov, I., Sharma, C.M., Vogel, J., and Winkler, W.C. (2010) Identification of regulatory RNAs in Bacillus subtilis. Nucleic Acids Res 38: 6637-6651.
29. Kearns, D.B., Chu, F., Branda, S.S., Kolter, R., and Losick, R. (2005) A master regulator for biofilm formation by Bacillus subtilis. Mol Microbiol 55: 739-749.
30. Khemici, V., Poljak, L., Luisi, B.F., and Carpousis, A.J. (2008) The RNase E of Escherichia coli is a membrane binding protein. Mol Microbiol 70: 799-813.
31. Kolodkin-Gal, I., Romero, D., Cao, S., Clardy, J., Kolter, R., and Losick, R. (2010) d-amino acids trigger biofilm disassembly. Science 328: 627-629.
32. Kunst, F., and Rapoport, G. (1995) Salt stress is an environmental signal affecting degradative enzyme synthesis in Bacillus subtilis. J Bacteriol 177: 2403-2407.
33. Kushner, S.R. (2002) mRNA decay in Escherichia coli comes of age. J Bacteriol 184: 4658-4665.
34. Lammers, C.R., Flórez, L.A., Schmeisky, A.G., Roppel, S.F., Mäder, U., Hamoen, L., and Stülke, J. (2010) Connecting parts with processes: SubtiWiki and SubtiPathways integrate gene and pathway annotation for Bacillus subtilis. Microbiology 156: 849-859.
35. Lazarevic, V., Düsterhöft, A., Soldo, B., Hilbert, H., Mauël, C., and Karamata, D. (1999) Nucleotide sequence of the Bacillus subtilis temperate bacteriophage SPbetaC2. Microbiology 145: 1055-1067.
36. Le Brun, N.E., Bengtsson, J., and Hederstedt, L. (2000) Genes required for cytochrome c synthesis in Bacillus subtilis. Mol Microbiol 36: 638-650.
37. Lee, K., Bernstein, J.A., and Cohen, S.N. (2002) RNase G complementation of rne null mutation identifies functional interrelationships with RNase E in Escherichia coli. Mol Microbiol 43: 1445-1456.
38. 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.
39. 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.
40. 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.
41. 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.
42. 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.
43. Martin-Verstraete, I., Débarbouillé, M., Klier, A., and Rapoport, G. (1994) Interaction of wild-type truncated LevR of Bacillus subtilis with the upstream activating sequence of the levanase operon. J Mol Biol 241: 178-192.
44. 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.
45. Mathy, N., Hébert, A., Mervelet, P., Bénard, L., Dorléans, A., Sierra-Gallay, I.L., etal. (2010) Bacillus subtilis ribonucleases J1 and J2 form a complex with altered enzyme behaviour. Mol Microbiol 75: 489-498.
46. 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.
47. Oussenko, I.A., Abe, T., Ujie, H., Muto, A., and Bechhofer, D.H. (2005) Participation of 3'-to-5' exoribonucleases in the turnover of Bacillus subtilis mRNA. J Bacteriol 187: 2758-2767.
48. Paik, S.H., Chakicherla, A., and Hansen, J.N. (1998) Identification and characterization of the structural and transporter genes for, and the chemical and biological properties of, sublancin 168, a novel lantibiotic produced by Bacillus subtilis 168. J Biol Chem 273: 23134-23142.
49. Rietkötter, E., Hoyer, D., and Mascher, T. (2008) Bacitracin sensing in Bacillus subtilis. Mol Microbiol 68: 768-785.
50. Romero, D., Aguilar, C., Losick, R., and Kolter, R. (2010) Amyloid fibers provide structural integrity to Bacillus subtilis biofilms. Proc Natl Acad Sci USA 107: 2230-2234.
51. Romero, D., Vlamakis, C., Losick, H., and Kolter, R. (2011) An accessory protein required for anchoring and assembly of amyloid fibers in B. subtilis biofilms. Mol Microbiol 80: 1155-1168.
52. de Saizieu, A., Vankan, P., Vockler, C., and van Loon, A.P. (1997) The trp RNA-binding attenuation protein (TRAP) regulates the steady-state levels of transcripts of the Bacillus subtilis folate operon. Microbiology 143: 979-989.
53. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
54. Schilling, O., Frick, O., Herzberg, C., Ehrenreich, A., Heinzle, E., Wittmann, C., and Stülke, J. (2007) Transcriptional and metabolic responses of Bacillus subtilis to the availability of organic acids: transcription regulation is important but not sufficient to account for metabolic adaptation. Appl Environ Microbiol 73: 499-507.
55. Serizawa, M., Kodama, K., Yamamoto, H., Kobayashi, K., Ogasawara, N., and Sekiguchi, J. (2005) Functional analysis of the YvrGHb two-component system of Bacillus subtilis: identification of the regulated genes by DNA microarray and Northern blot analyses. Biosci Biotechnol Biochem 69: 2155-2169.
56. 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.
57. Stead, M.B., Marshburn, S., Mohanty, B.K., Mitra, J., Pena Castillo, L., Ray, D., etal. (2011) Analysis of Escherichia coli RNase E and RNase III activity in vivo using tiling microarrays. Nucleic Acids Res 39: 3188-3203.
58. Stöver, A.G., and Driks, A. (1999) Regulation of synthesis of the Bacillus subtilis transition-phase, spore-associated antibacterial protein TasA. J Bacteriol 181: 5476-5481.
59. Tanaka, K., Kobayashi, K., and Ogasawara, N. (2003) The Bacillus subtilis YufLM two-component system regulates the expression of the malate transporters MaeN (YufR) and YflS, and is essential for utilization of malate in minimal medium. Microbiology 149: 2317-2329.
60. Vanzo, N.F., Li, Y.S., Py, B., Blum, E., Higgins, C.F., Raynal, L.C., etal. (1998) Ribonuclease E organizes the protein interactions in the Escherichia coli RNA degradosome. Genes Dev 12: 2770-2781.
61. Wacker, I., Ludwig, H., Reif, I., Blencke, H.M., Detsch, C., and Stülke, J. (2003) The regulatory link between carbon and nitrogen metabolism in Bacillus subtilis: regulation of the gltAB operon by the catabolite control protein CcpA. Microbiology 149: 3001-3009.
62. Weinrauch, Y., Msadek, T., Kunst, F., and Dubnau, D. (1991) Sequence and properties of comQ, a new competence regulatory gene of Bacillus subtilis. J Bacteriol 173: 5685-5693.
63. Yao, S., and Bechhofer, D.H. (2010) Initiation of decay of Bacillus subtilis rpsO mRNA by endoribonuclease RNase Y. J Bacteriol 192: 3279-3286.
64. Zweers, J.C., Wiegert, T., and van Dijl, J.M. (2009) Stress-responsive systems set specific limits to the overproduction of membrane proteins in Bacillus subtilis. Appl Environ Microbiol 75: 7356-7364.