YneA mRNA instability is involved in temporary inhibition of cell division during the SOS response of Bacillus megaterium

Microbiology (United Kingdom)

Volumn 159, Issue 8, 2013, Pages 1564-1574

  Buchholz, Meike ^a   Nahrstedt, Hannes ^a   Pillukat, Mike H ^a   Deppe, Veronika ^a   Meinhardt, Friedhelm ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; BACTERIAL PROTEIN; MESSENGER RNA; NUCLEOPROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTIONAL REPRESSOR DINR; UNCLASSIFIED DRUG; YNEA PROTEIN;

ARTICLE; BACILLUS MEGATERIUM; BACILLUS SUBTILIS; BACTERIAL GROWTH; CATALYSIS; CELL DIVISION; CELL FUNCTION; DNA DAMAGE; DNA REPAIR; ENZYME ACTIVITY; GENE OVEREXPRESSION; MUTAGENESIS; OPEN READING FRAME; OPERON; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; RNA STABILITY; TRANSCRIPTION INITIATION;

BACILLUS MEGATERIUM; BACTERIAL PROTEINS; BLOTTING, NORTHERN; CELL DIVISION; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE KNOCKOUT TECHNIQUES; REAL-TIME POLYMERASE CHAIN REACTION; RNA STABILITY; SOS RESPONSE (GENETICS);

EID: 84881252080     PISSN: 13500872     EISSN: 14652080     Source Type: Journal    
DOI: 10.1099/mic.0.064766-0     Document Type: Article

References (51)

1. Au, N., Kuester-Schoeck, E., Mandava, V., Bothwell, L. E., Canny, S. P., Chachu, K., Colavito, S. A., Fuller, S. N., Groban, E. S. & other authors (2005). Genetic composition of the Bacillus subtilis SOS system. J Bacteriol 187, 7655-7666.
2. Barg, H., Malten, M., Jahn, M. & Jahn, D. (2005). Protein and vitamin production in Bacillus megaterium. In Microbial Processes and Products, vol. 18, pp. 205-223. Edited by J. L. Barredo. Totowa, NJ: Humana Press.
3. Bateman, A. & Bycroft, M. (2000). The structure of a LysM domain from E. coli membrane-bound lytic murein transglycosylase D (MltD). J Mol Biol 299, 1113-1119.
4. Bendtsen, J. D., Nielsen, H., von Heijne, G. & Brunak, S. (2004). Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340, 783-795.
5. Berney, M., Weilenmann, H. U. & Egli, T. (2006). Gene expression of Escherichia coli in continuous culture during adaptation to artificial sunlight. Environ Microbiol 8, 1635-1647.
6. Bi, E. & Lutkenhaus, J. (1993). Cell division inhibitors SulA and MinCD prevent formation of the FtsZ ring. J Bacteriol 175, 1118-1125.
7. Borgmeier, C., Bongaerts, J. & Meinhardt, F. (2012). Genetic analysis of the Bacillus licheniformis degSU operon and the impact of regulatory mutations on protease production. J Biotechnol 159, 12-20.
8. Brown, B. J. & Carlton, B. C. (1980). Plasmid-mediated transformation in Bacillus megaterium. J Bacteriol 142, 508-512.
9. Deppe, V. M., Bongaerts, J., O'Connell, T., Maurer, K. H. & Meinhardt, F. (2011a). Enzymatic deglycation of Amadori products in bacteria: mechanisms, occurrence and physiological functions. Appl Microbiol Biotechnol 90, 399-406.
10. Deppe, V. M., Klatte, S., Bongaerts, J., Maurer, K. H., O'Connell, T. & Meinhardt, F. (2011b). Genetic control of Amadori product degradation in Bacillus subtilis via regulation of frlBONMD expression by FrlR. Appl Environ Microbiol 77, 2839-2846.
11. Durand, S., Gilet, L., Bessieres, 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.
12. English, J. D. & Vary, P. S. (1986). Isolation of recombinationdefective and UV-sensitive mutants of Bacillus megaterium. J Bacteriol 165, 155-160.
13. Eppinger, M., Bunk, B., Johns, M. A., Edirisinghe, J. N., Kutumbaka, K. K., Koenig, S. S., Creasy, H. H., Rosovitz, M. J., Riley, D. R. & other authors (2011). Genome sequences of the biotechnologically important Bacillus megaterium strains QM B1551 and DSM319. J Bacteriol 193, 4199-4213.
14. Fernández de Henestrosa, A. R., Ogi, T., Aoyagi, S., Chafin, D., Hayes, J. J., Ohmori, H. & Woodgate, R. (2000). Identification of additional genes belonging to the LexA regulon in Escherichia coli. Mol Microbiol 35, 1560-1572.
15. Friedberg, E. C., Walker, G. C., Siede, W., Wood, R. D., Schultz, R. A. & Ellenberger, T. (1995). The SOS response of prokaryotes to DNA damage. In DNA Repair and Mutagenesis, pp. 463-508. Edited by E. C. Friedberg, G. C. Walker, W. Siede, R. D. Wood, R. A. Schultz & T. Ellenberger. Washington, DC: American Society for Microbiology.
16. Goranov, A. I., Kuester-Schoeck, E., Wang, J. D. & Grossman, A. D. (2006). Characterization of the global transcriptional responses to different types of DNA damage and disruption of replication in Bacillus subtilis. J Bacteriol 188, 5595-5605.
17. Gottesman, S., Halpern, E. & Trisler, P. (1981). Role of sulA and sulB in filamentation by lon mutants of Escherichia coli K-12. J Bacteriol 148, 265-273.
18. Groban, E. S., Johnson, M. B., Banky, P., Burnett, P. G., Calderon, G. L., Dwyer, E. C., Fuller, S. N., Gebre, B., King, L. M. & other authors (2005). Binding of the Bacillus subtilis LexA protein to the SOS operator. Nucleic Acids Res 33, 6287-6295.
19. Haijema, B. J., van Sinderen, D., Winterling, K., Kooistra, J., Venema, G. & Hamoen, L. W. (1996). Regulated expression of the dinR and recA genes during competence development and SOS induction in Bacillus subtilis. Mol Microbiol 22, 75-85.
20. Huisman, O., D'Ari, R. & Gottesman, S. (1984). Cell-division control in Escherichia coli: specific induction of the SOS function SfiA protein is sufficient to block septation. Proc Natl Acad Sci U S A 81, 4490-4494.
21. Kawai, Y. & Ogasawara, N. (2006). Bacillus subtilis EzrA and FtsL synergistically regulate FtsZ ring dynamics during cell division. Microbiology 152, 1129-1141.
22. Kawai, Y., Moriya, S. & Ogasawara, N. (2003). Identification of a protein, YneA, responsible for cell division suppression during the SOS response in Bacillus subtilis. Mol Microbiol 47, 1113-1122.
23. Kawamura, F. & Doi, R. H. (1984). Construction of a Bacillus subtilis double mutant deficient in extracellular alkaline and neutral proteases. J Bacteriol 160, 442-444.
24. Lehnik-Habrink, M., Schaffer, M., Mäder, U., Diethmaier, C., Herzberg, C. & Stü lke, J. (2011). RNA processing in Bacillus subtilis: identification of targets of the essential RNase Y. Mol Microbiol 81, 1459-1473.
25. Little, J. W. (1984). Autodigestion of lexA and phage lambda repressors. Proc Natl Acad Sci U S A 81, 1375-1379.
26. Love, P. E. & Yasbin, R. E. (1984). Genetic characterization of the inducible SOS-like system of Bacillus subtilis. J Bacteriol 160, 910-920.
27. Lovett, C. M., Jr, O'Gara, T. M. & Woodruff, J. N. (1994). Analysis of the SOS inducing signal in Bacillus subtilis using Escherichia coli LexA as a probe. J Bacteriol 176, 4914-4923.
28. Manasherob, R., Miller, C., Kim, K. S. & Cohen, S. N. (2012). Ribonuclease E modulation of the bacterial SOS response. PLoS ONE 7, e38426.
29. McKenzie, G. J., Harris, R. S., Lee, P. L. & Rosenberg, S. M. (2000). The SOS response regulates adaptive mutation. Proc Natl Acad Sci U S A 97, 6646-6651.
30. Meinhardt, F., Stahl, U. & Ebeling, W. (1989). Highly efficient expression of homologous and heterologous genes in Bacillus megaterium. Appl Microbiol Biotechnol 30, 343-350.
31. Meinhardt, F., Bußkamp, M. & Wittchen, K.-D. (1994). Cloning and sequencing of the leu C and npr M genes and a putative spo IV gene from Bacillus megaterium DSM319. Appl Microbiol Biotechnol 41, 344-351.
32. Miller, J. H. (1972). Assay of b-galactosidase. In Experiments in Molecular Genetics, pp. 352-355. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
33. Miller, M. C., Resnick, J. B., Smith, B. T. & Lovett, C. M., Jr (1996). The bacillus subtilis dinR gene codes for the analogue of Escherichia coli LexA. Purification and characterization of the DinR protein. J Biol Chem 271, 33502-33508.
34. Mizusawa, S., Court, D. & Gottesman, S. (1983). Transcription of the sulA gene and repression by LexA. J Mol Biol 171, 337-343.
35. Mo, A. H. & Burkholder, W. F. (2010). YneA, an SOS-induced inhibitor of cell division in Bacillus subtilis, is regulated posttranslationally and requires the transmembrane region for activity. J Bacteriol 192, 3159-3173.
36. Mount, D. W. (1977). A mutant of Escherichia coli showing constitutive expression of the lysogenic induction and error-prone DNA repair pathways. Proc Natl Acad Sci U S A 74, 300-304.
37. Mukherjee, A., Cao, C. & Lutkenhaus, J. (1998). Inhibition of FtsZ polymerization by SulA, an inhibitor of septation in Escherichia coli. Proc Natl Acad Sci U S A 95, 2885-2890.
38. Nahrstedt, H. & Meinhardt, F. (2004). Structural and functional characterization of the Bacillus megaterium uvrBA locus and generation of UV-sensitive mutants. Appl Microbiol Biotechnol 65, 193-199.
39. Nahrstedt, H., Schröder, C. & Meinhardt, F. (2005a). Evidence for two recA genes mediating DNA repair in Bacillus megaterium. Microbiology 151, 775-787.
40. Nahrstedt, H., Waldeck, J., Gröne, M., Eichstädt, R., Feesche, J. & Meinhardt, F. (2005b). Strain development in Bacillus licheniformis: construction of biologically contained mutants deficient in sporulation and DNA repair. J Biotechnol 119, 245-254.
41. Primrose, S. B. & Ehrlich, S. D. (1981). Isolation of plasmid deletion mutants and study of their instability. Plasmid 6, 193-201.
42. Sambrook, J. & Russell, D. (2001). Molecular Cloning: a Laboratory Manual, 3rd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
43. Sanger, F., Nicklen, S. & Coulson, A. R. (1977). DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A 74, 5463-5467.
44. Schmidt, S., Wolf, N., Strey, J., Nahrstedt, H., Meinhardt, F. & Waldeck, J. (2005). Test systems to study transcriptional regulation and promoter activity in Bacillus megaterium. Appl Microbiol Biotechnol 68, 647-655.
45. Schoemaker, J. M., Gayda, R. C. & Markovitz, A. (1984). Regulation of cell division in Escherichia coli: SOS induction and cellular location of the sulA protein, a key to lon-associated filamentation and death. J Bacteriol 158, 551-561.
46. 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.
47. Stahl, U. & Esser, K. (1983). Plasmid heterogeneity in various strains of Bacillus megaterium. Eur J Appl Biotechnol 17, 248-251.
48. Strey, J., Wittchen, K. D. & Meinhardt, F. (1999). Regulation of betagalactosidase expression in Bacillus megaterium DSM319 by a XylS/ AraC-type transcriptional activator. J Bacteriol 181, 3288-3292.
49. Vorob'eva, I. P., Khmel', I. A. & Alfoldi, L. (1980). [Polyethylene glycol induction of Bacillus megaterium protoplast transformation by plasmid DNA]. Dokl Akad Nauk SSSR 251, 977-980 (in Russian).
50. Winterling, K. W., Chafin, D., Hayes, J. J., Sun, J., Levine, A. S., Yasbin, R. E. & Woodgate, R. (1998). The Bacillus subtilis DinR binding site: redefinition of the consensus sequence. J Bacteriol 180, 2201-2211.
51. Woodcock, D. M., Crowther, P. J., Doherty, J., Jefferson, S., DeCruz, E., Noyer-Weidner, M., Smith, S. S., Michael, M. Z. & Graham, M. W. (1989). Quantitative evaluation of Escherichia coli host strains for tolerance to cytosine methylation in plasmid and phage recombinants. Nucleic Acids Res 17, 3469-3478.