1887

Abstract

The SOS response, a mechanism enabling bacteria to cope with DNA damage, is strictly regulated by the two major players, RecA and LexA ( homologue DinR). Genetic stress provokes formation of ssDNA-RecA nucleoprotein filaments, the coprotease activity of which mediates the autocatalytic cleavage of the transcriptional repressor DinR and ensures the expression of a set of (damage-inducible) genes, which encode proteins that enhance repair capacity, accelerate mutagenesis rate and cause inhibition of cell division (ICD). In , the transcriptional activation of the operon is part of the SOS response, with YneA being responsible for the ICD. Pointing to its cellular function in , overexpression of homologous YneA led to filamentous growth, while ICD was temporary during the SOS response. Genetic knockouts of the individual open reading frames of the operon increased the mutagenic sensitivity, proving – for the first time in a species – that each of the three genes is in fact instrumental in coping with genetic stress. Northern- and quantitative real-time PCR analyses revealed – in contrast to other genes (exemplified for ) – transient mRNA-presence of the operon irrespective of persisting SOS-inducing conditions. Promoter test assays and Northern analyses suggest that the decline of the ICD is at least partly due to mRNA instability.

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2013-08-01
2020-08-08
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References

  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 Bacteriol187:7655–7666 [CrossRef][PubMed]
    [Google Scholar]
  2. Barg H., Malten M., Jahn M., Jahn D..( 2005;). Protein and vitamin production in Bacillus megaterium. Microbial Processes and Productsvol. 18205–223 Barredo J. L.. Totowa, NJ: Humana Press; [CrossRef]
    [Google Scholar]
  3. Bateman A., Bycroft M..( 2000;). The structure of a LysM domain from E. coli membrane-bound lytic murein transglycosylase D (MltD). J Mol Biol299:1113–1119 [CrossRef][PubMed]
    [Google Scholar]
  4. Bendtsen J. D., Nielsen H., von Heijne G., Brunak S..( 2004;). Improved prediction of signal peptides: SignalP 3.0. J Mol Biol340:783–795 [CrossRef][PubMed]
    [Google Scholar]
  5. Berney M., Weilenmann H. U., Egli T..( 2006;). Gene expression of Escherichia coli in continuous culture during adaptation to artificial sunlight. Environ Microbiol8:1635–1647 [CrossRef][PubMed]
    [Google Scholar]
  6. Bi E., Lutkenhaus J..( 1993;). Cell division inhibitors SulA and MinCD prevent formation of the FtsZ ring. J Bacteriol175:1118–1125[PubMed]
    [Google Scholar]
  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 Biotechnol159:12–20 [CrossRef][PubMed]
    [Google Scholar]
  8. Brown B. J., Carlton B. C..( 1980;). Plasmid-mediated transformation in Bacillus megaterium. J Bacteriol142:508–512[PubMed]
    [Google Scholar]
  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 Biotechnol90:399–406 [CrossRef][PubMed]
    [Google Scholar]
  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 Microbiol77:2839–2846 [CrossRef][PubMed]
    [Google Scholar]
  11. 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 Genet8:e1002520 [CrossRef][PubMed]
    [Google Scholar]
  12. English J. D., Vary P. S..( 1986;). Isolation of recombination-defective and UV-sensitive mutants of Bacillus megaterium. J Bacteriol165:155–160[PubMed]
    [Google Scholar]
  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 Bacteriol193:4199–4213 [CrossRef][PubMed]
    [Google Scholar]
  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 Microbiol35:1560–1572 [CrossRef][PubMed]
    [Google Scholar]
  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. DNA Repair and Mutagenesis463–508 Friedberg E. C., Walker G. C., Siede W. , Wood R. D., Schultz R. A., Ellenberger T. . Washington, DC: American Society for Microbiology;
    [Google Scholar]
  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 Bacteriol188:5595–5605 [CrossRef][PubMed]
    [Google Scholar]
  17. Gottesman S., Halpern E., Trisler P..( 1981;). Role of sulA and sulB in filamentation by lon mutants of Escherichia coli K-12. J Bacteriol148:265–273[PubMed]
    [Google Scholar]
  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 Res33:6287–6295 [CrossRef][PubMed]
    [Google Scholar]
  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 Microbiol22:75–85 [CrossRef][PubMed]
    [Google Scholar]
  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 A81:4490–4494 [CrossRef][PubMed]
    [Google Scholar]
  21. Kawai Y., Ogasawara N..( 2006;). Bacillus subtilis EzrA and FtsL synergistically regulate FtsZ ring dynamics during cell division. Microbiology152:1129–1141 [CrossRef][PubMed]
    [Google Scholar]
  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 Microbiol47:1113–1122 [CrossRef][PubMed]
    [Google Scholar]
  23. Kawamura F., Doi R. H..( 1984;). Construction of a Bacillus subtilis double mutant deficient in extracellular alkaline and neutral proteases. J Bacteriol160:442–444[PubMed]
    [Google Scholar]
  24. Lehnik-Habrink M., Schaffer M., Mäder U., Diethmaier C., Herzberg C., Stülke J..( 2011;). RNA processing in Bacillus subtilis: identification of targets of the essential RNase Y. Mol Microbiol81:1459–1473 [CrossRef][PubMed]
    [Google Scholar]
  25. Little J. W..( 1984;). Autodigestion of lexA and phage lambda repressors. Proc Natl Acad Sci U S A81:1375–1379 [CrossRef][PubMed]
    [Google Scholar]
  26. Love P. E., Yasbin R. E..( 1984;). Genetic characterization of the inducible SOS-like system of Bacillus subtilis. J Bacteriol160:910–920[PubMed]
    [Google Scholar]
  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 Bacteriol176:4914–4923[PubMed]
    [Google Scholar]
  28. Manasherob R., Miller C., Kim K. S., Cohen S. N..( 2012;). Ribonuclease E modulation of the bacterial SOS response. PLoS ONE7:e38426 [CrossRef][PubMed]
    [Google Scholar]
  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 A97:6646–6651 [CrossRef][PubMed]
    [Google Scholar]
  30. Meinhardt F., Stahl U., Ebeling W..( 1989;). Highly efficient expression of homologous and heterologous genes in Bacillus megaterium. Appl Microbiol Biotechnol30:343–350 [CrossRef]
    [Google Scholar]
  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 Biotechnol41:344–351 [CrossRef][PubMed]
    [Google Scholar]
  32. Miller J. H..( 1972;). Assay of β-galactosidase. Experiments in Molecular Genetics352–355 Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press;
    [Google Scholar]
  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 Chem271:33502–33508 [CrossRef][PubMed]
    [Google Scholar]
  34. Mizusawa S., Court D., Gottesman S..( 1983;). Transcription of the sulA gene and repression by LexA. J Mol Biol171:337–343 [CrossRef][PubMed]
    [Google Scholar]
  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 Bacteriol192:3159–3173 [CrossRef][PubMed]
    [Google Scholar]
  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 A74:300–304 [CrossRef][PubMed]
    [Google Scholar]
  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 A95:2885–2890 [CrossRef][PubMed]
    [Google Scholar]
  38. Nahrstedt H., Meinhardt F..( 2004;). Structural and functional characterization of the Bacillus megaterium uvrBA locus and generation of UV-sensitive mutants. Appl Microbiol Biotechnol65:193–199 [CrossRef][PubMed]
    [Google Scholar]
  39. Nahrstedt H., Schröder C., Meinhardt F..( 2005a;). Evidence for two recA genes mediating DNA repair in Bacillus megaterium. Microbiology151:775–787 [CrossRef][PubMed]
    [Google Scholar]
  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 Biotechnol119:245–254 [CrossRef][PubMed]
    [Google Scholar]
  41. Primrose S. B., Ehrlich S. D..( 1981;). Isolation of plasmid deletion mutants and study of their instability. Plasmid6:193–201 [CrossRef][PubMed]
    [Google Scholar]
  42. Sambrook J., Russell D..( 2001;). Molecular Cloning: a Laboratory Manual Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  43. Sanger F., Nicklen S., Coulson A. R..( 1977;). DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A74:5463–5467 [CrossRef][PubMed]
    [Google Scholar]
  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 Biotechnol68:647–655 [CrossRef][PubMed]
    [Google Scholar]
  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 Bacteriol158:551–561[PubMed]
    [Google Scholar]
  46. Shahbabian K., Jamalli A., Zig L., Putzer H..( 2009;). RNase Y, a novel endoribonuclease, initiates riboswitch turnover in Bacillus subtilis. EMBO J28:3523–3533 [CrossRef][PubMed]
    [Google Scholar]
  47. Stahl U., Esser K..( 1983;). Plasmid heterogeneity in various strains of Bacillus megaterium. Eur J Appl Biotechnol17:248–251 [CrossRef]
    [Google Scholar]
  48. Strey J., Wittchen K. D., Meinhardt F..( 1999;). Regulation of beta-galactosidase expression in Bacillus megaterium DSM319 by a XylS/AraC-type transcriptional activator. J Bacteriol181:3288–3292[PubMed]
    [Google Scholar]
  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 SSSR251:977–980[PubMed]
    [Google Scholar]
  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 Bacteriol180:2201–2211[PubMed]
    [Google Scholar]
  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 Res17:3469–3478 [CrossRef][PubMed]
    [Google Scholar]
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