1887

Abstract

Bacteriocins are a large and functionally diverse family of toxins found in all major lineages of Bacteria. Colicins, those bacteriocins produced by , serve as a model system for investigations of bacteriocin structure–function relationships, genetic organization, and their ecological role and evolutionary history. Colicin expression is often dependent on host regulatory pathways (such as the SOS system), is usually confined to times of stress, and results in death of the producing cells. This study investigates the role of the SOS system in mediating this unique form of toxin expression. A comparison of all the sequenced enteric bacteriocin promoters reveals that over 75 % are regulated by dual, overlapping SOS boxes, which serve to bind two LexA repressor proteins. Furthermore, a highly conserved poly-A motif is present in both of the binding sites examined, indicating enhanced affinity of the LexA protein for the binding site. The use of gene expression analysis and deletion mutations further demonstrates that these unique LexA cooperative binding regions result in a fine tuning of bacteriocin production, limiting it to times of stress. These results suggest that the evolution of dual SOS boxes elegantly accomplishes the task of increasing the amount of toxin produced by a cell while decreasing the rate of uninduced production, effectively reducing the cost of colicin production. This hypothesis may explain why such a promoter motif is present at such high frequencies in natural populations of bacteriocin-producing enteric bacteria.

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2008-06-01
2019-10-19
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References

  1. Barbic, A., Zimmer, D. P. & Crothers, D. M. ( 2003; ). Structural origins of adenine-tract bending. Proc Natl Acad Sci U S A 100, 2369–2373.[CrossRef]
    [Google Scholar]
  2. Braun, V., Pilsl, H. & Gross, P. ( 1994; ). Colicins: structures, modes of action, transfer through membranes, and evolution. Arch Microbiol 161, 199–206.[CrossRef]
    [Google Scholar]
  3. Cascales, E., Buchanan, S. K., Duche, D., Kleanthous, C., Lloubes, R., Postle, K., Riley, M., Slatin, S. & Cavard, D. ( 2007; ). Colicin biology. Microbiol Mol Biol Rev 71, 158–229.[CrossRef]
    [Google Scholar]
  4. Crooks, G. E., Hon, G., Chandonia, J.-M. & Brenner, S. E. ( 2004; ). WebLogo: a sequence logo generator. Genome Res 14, 1188–1190.[CrossRef]
    [Google Scholar]
  5. Davidov, Y., Rozen, R., Smulski, D. R., Van Dyk, T. K., Vollmer, A. C., Elsemore, D. A., LaRossa, R. A. & Belkin, S. ( 2000; ). Improved bacterial SOS promoter : : lux fusions for genotoxicity detection. Mutat Res 466, 97–107.[CrossRef]
    [Google Scholar]
  6. Ebina, Y., Takahara, Y., Kishi, F., Nakazawa, A. & Brent, R. ( 1983; ). LexA protein is a repressor of the colicin E1 gene. J Biol Chem 258, 13258–13261.
    [Google Scholar]
  7. Erill, I., Escribano, M., Campoy, S. & Barbe, J. ( 2003; ). In silico analysis reveals substantial variability in the gene contents of the gamma proteobacteria LexA-regulon. Bioinformatics 19, 2225–2236.[CrossRef]
    [Google Scholar]
  8. Fernandez 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.
    [Google Scholar]
  9. Gascuel, O. & Steel, M. ( 2006; ). Neighbor-joining revealed. Mol Biol Evol 23, 1997–2000.[CrossRef]
    [Google Scholar]
  10. Gordon, D. M. & O'Brien, C. L. ( 2006; ). Bacteriocin diversity and the frequency of multiple bacteriocin production in Escherichia coli. Microbiology 152, 3239–3244.[CrossRef]
    [Google Scholar]
  11. Gratia, A. ( 1925; ). Sur un remarquable exemple d'antagonisme entre deux souches de colilbacille. Comp Rend Soc Biol 93, 1040–1041 (in French).
    [Google Scholar]
  12. Kelley, W. L. ( 2006; ). Lex marks the spot: the virulent side of SOS and a closer look at the LexA regulon. Mol Microbiol 62, 1228–1238.[CrossRef]
    [Google Scholar]
  13. Kim, B. & Little, J. W. ( 1992; ). Dimerization of a specific DNA-binding protein on the DNA. Science 255, 203–206.[CrossRef]
    [Google Scholar]
  14. Kolaczkowski, B. & Thornton, J. W. ( 2004; ). Performance of maximum parsimony and likelihood phylogenetics when evolution is heterogeneous. Nature 431, 980–984.[CrossRef]
    [Google Scholar]
  15. Kumar, S., Tamura, K. & Nei, M. ( 2004; ). mega3: integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Brief Bioinform 5, 150–163.[CrossRef]
    [Google Scholar]
  16. Lazdunski, C. J., Bouveret, E., Rigal, A., Journet, L., Lloubes, R. & Benedetti, H. ( 1998; ). Colicin import into Escherichia coli cells. J Bacteriol 180, 4993–5002.
    [Google Scholar]
  17. Lewis, L. K., Harlow, G. R., Gregg-Jolly, L. A. & Mount, D. W. ( 1994; ). Identification of high affinity binding sites for LexA which define new DNA damage-inducible genes in Escherichia coli. J Mol Biol 241, 507–523.[CrossRef]
    [Google Scholar]
  18. Little, J. W. & Mount, D. W. ( 1982; ). The SOS regulatory system of Escherichia coli. Cell 29, 11–22.[CrossRef]
    [Google Scholar]
  19. Lloubes, R., Granger-Schnarr, M., Lazdunski, C. & Schnarr, M. ( 1988; ). LexA repressor induces operator-dependent DNA bending. J Mol Biol 204, 1049–1054.[CrossRef]
    [Google Scholar]
  20. Lloubes, R., Lazdunski, C., Granger-Schnarr, M. & Schnarr, M. ( 1993; ). DNA sequence determinants of LexA-induced DNA bending. Nucleic Acids Res 21, 2363–2367.[CrossRef]
    [Google Scholar]
  21. Lu, F. M. & Chak, K. F. ( 1996; ). Two overlapping SOS-boxes in ColE operons are responsible for the viability of cells harboring the Col plasmid. Mol Gen Genet 251, 407–411.[CrossRef]
    [Google Scholar]
  22. 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.[CrossRef]
    [Google Scholar]
  23. Mrak, P., Podlesek, Z., van Putten, J. P. M. & Zgur-Bertok, D. ( 2007; ). Heterogeneity in expression of the Escherichia coli colicin K activity gene cka is controlled by the SOS system and stochastic factors. Mol Genet Genomics 277, 391–401.[CrossRef]
    [Google Scholar]
  24. Mulec, J., Podlesek, Z., Mrak, P., Kopitar, A., Ihan, A. & Zgur-Bertok, D. ( 2003; ). A ckagfp transcriptional fusion reveals that the colicin K activity gene is induced in only 3 percent of the population. J Bacteriol 185, 654–659.[CrossRef]
    [Google Scholar]
  25. Norman, A., Hansen, L. H. & Sorensen, S. J. ( 2005; ). Construction of a ColD cda promoter-based SOS-green fluorescent protein whole-cell biosensor with higher sensitivity toward genotoxic compounds than constructs based on recA, umuDC, or sul4 promoters. Appl Environ Microbiol 71, 2338–2346.[CrossRef]
    [Google Scholar]
  26. Perez-Martin, J. & de Lorenzo, V. ( 1997; ). Clues and consequences of DNA bending in transcription. Annu Rev Microbiol 51, 593–628.[CrossRef]
    [Google Scholar]
  27. Prieto, A. I., Ramos-Morales, F. & Casadesus, J. ( 2004; ). Bile-induced DNA damage in Salmonella enterica. Genetics 168, 1787–1794.[CrossRef]
    [Google Scholar]
  28. Pugsley, A. P. ( 1985; ). Escherichia coli K12 strains for use in the identification and characterization of colicins. J Gen Microbiol 131, 369–376.
    [Google Scholar]
  29. Pugsley, A. P. & Schwartz, M. ( 1983; ). A genetic approach to the study of mitomycin-induced lysis of Escherichia coli K-12 strains which produce colicin E2. Mol Gen Genet 190, 366–372.[CrossRef]
    [Google Scholar]
  30. Riley, M. A. & Wertz, J. E. ( 2002; ). Bacteriocins: evolution, ecology, and application. Annu Rev Microbiol 56, 117–137.[CrossRef]
    [Google Scholar]
  31. Riley, M. A., Pinou, T., Wertz, J. E., Tan, Y. & Valletta, C. M. ( 2001; ). Molecular characterization of the klebicin B plasmid of Klebsiella pneumoniae. Plasmid 45, 209–221.[CrossRef]
    [Google Scholar]
  32. Ronen, M., Rosenberg, R., Shraiman, B. I. & Alon, U. ( 2002; ). Assigning numbers to the arrows: parameterizing a gene regulation network by using accurate expression kinetics. Proc Natl Acad Sci U S A 99, 10555–10560.[CrossRef]
    [Google Scholar]
  33. Ronquist, F. & Huelsenbeck, J. P. ( 2003; ). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.[CrossRef]
    [Google Scholar]
  34. Rosen, R., Davidov, Y., LaRossa, R. A. & Belkin, S. ( 2000; ). Microbial sensors of ultraviolet radiation based on recA′ : : lux fusions. Appl Biochem Biotechnol 89, 151–160.[CrossRef]
    [Google Scholar]
  35. Salles, B. & Weinstock, G. M. ( 1989; ). Mutation of the promoter and LexA binding sites of cea, the gene encoding colicin E1. Mol Gen Genet 215, 483–489.[CrossRef]
    [Google Scholar]
  36. Smarda, J. & Smajs, D. ( 1998; ). Colicins – exocellular lethal proteins of Escherichia coli. Folia Microbiol (Praha) 43, 563–582.[CrossRef]
    [Google Scholar]
  37. Thompson, J. D., Higgins, D. G. & Gibson, T. J. ( 1994; ). clustal w: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22, 4673–4680.[CrossRef]
    [Google Scholar]
  38. Ujvari, A. & Martin, C. T. ( 2000; ). Evidence for DNA bending at the T7 RNA polymerase promoter. J Mol Biol 295, 1173–1184.[CrossRef]
    [Google Scholar]
  39. van der Lelie, D., Regniers, L., Borremans, B., Provoost, A. & Verschaeve, L. ( 1997; ). The VITOTOX test, an SOS bioluminescence Salmonella typhimurium test to measure genotoxicity kinetics. Mutat Res 389, 279–290.[CrossRef]
    [Google Scholar]
  40. Van Dyk, T. K. & Rosson, R. A. ( 1998; ). Photorhabdus luminescens luxCDABE promoter probe vectors. Methods Mol Biol 102, 85–95.
    [Google Scholar]
  41. Van Dyk, T. K., DeRose, E. J. & Gonye, G. E. ( 2001a; ). LuxArray, a high-density, genomewide transcription analysis of Escherichia coli using bioluminescent reporter strains. J Bacteriol 183, 5496–5505.[CrossRef]
    [Google Scholar]
  42. Van Dyk, T. K., Wei, Y., Hanafey, M. K., Dolan, M., Reeve, M. J., Rafalski, J. A., Rothman-Denes, L. B. & LaRossa, R. A. ( 2001b; ). A genomic approach to gene fusion technology. Proc Natl Acad Sci U S A 98, 2555–2560.[CrossRef]
    [Google Scholar]
  43. Vankemmelbeke, M., Healy, B., Moore, G. R., Kleanthous, C., Penfold, C. N. & James, R. ( 2005; ). Rapid detection of colicin E9-induced DNA damage using Escherichia coli cells carrying SOS promoter–lux fusions. J Bacteriol 187, 4900–4907.[CrossRef]
    [Google Scholar]
  44. Walker, G. C. ( 1987; ). The SOS response of Escherichia coli. In Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology, pp. 1346–1357. Edited by F. C. Neidhardt, J. L. Ingraham, K. B. Low, B. Magasanik, M. Schaechter & H. E. Umbarger. Washington, DC: American Society for Microbiology.
  45. Walker, G. C. ( 1995; ). SOS-regulated proteins in translesion DNA synthesis and mutagenesis. Trends Biochem Sci 20, 416–420.[CrossRef]
    [Google Scholar]
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