1887

Abstract

Colicins, a class of antimicrobial compounds produced by bacteria, are thought to be important mediators of intra- and interspecific interactions, and are a significant factor in maintaining microbial diversity. Colicins B and M are among the most common colicins produced by , and are usually encoded adjacently on the same plasmid. In this study, the characterization of a collection of isolated from Australian vertebrates revealed that a significant fraction of colicin BM strains lack an intact colicin B activity gene. The colicin B and M gene region was sequenced in 60 strains and it was found (with one exception) that all plasmids lacking an intact colicin B activity gene have an identical colicin gene structure, possessing a complete colicin B immunity gene and a 130 bp remnant of the B activity gene. A phylogenetic analysis of the colicin M and B operons and characterization of the plasmids suggested that ColBM plasmids with a truncated B activity gene have evolved on at least three separate occasions. Colicin B immunity was found to be non-functional in strains that have lost colicin B activity, and colicin M was still produced despite the absence of the SOS box believed to regulate its production in colicin BM strains. The presence of a remnant of the microcin V operon next to the truncated colicin B activity gene indicated that these plasmids evolved as a consequence of gene transfer between colicin BM and microcin V plasmids. We suggest that these transfer events most likely involved the transfer of some microcin V genes and associated virulence factors onto ColBM plasmids.

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2009-05-01
2020-09-24
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References

  1. Boyd E. F., Hill C. W., Rich S. M., Hartl D. L.. 1996; Mosaic structure of plasmids from natural populations of Escherichia coli . Genetics143:1091–1100
    [Google Scholar]
  2. Braun V.. 1995; Energy-coupled transport and signal-transduction through the Gram-negative outer-membrane via TonB-ExbB-ExbD-dependent receptor proteins. FEMS Microbiol Rev16:295–307
    [Google Scholar]
  3. Braun V., Schaller K., Wabl M. R.. 1974; Isolation, characterization and action of colicin-M. Antimicrob Agents Chemother5:520–533
    [Google Scholar]
  4. Braun V., Patzer S. I., Hantke K.. 2002; Ton-dependent colicins and microcins: modular design and evolution. Biochimie84:365–380
    [Google Scholar]
  5. Clermont O., Bonacorsi S., Bingen E.. 2000; Rapid and simple determination of the Escherichia coli phylogenetic group. Appl Environ Microbiol66:4555–4558
    [Google Scholar]
  6. Czaran T. L., Hoekstra R. F., Pagie L.. 2002; Chemical warfare between microbes promotes biodiversity. Proc Natl Acad Sci U S A99:786–790
    [Google Scholar]
  7. de Souza M. L., Wackett L. P., Sadowsky M. J.. 1998; The atzABC genes encoding atrazine catabolism are located on a self-transmissible plasmid in Pseudomonas sp. strain ADP. Appl Environ Microbiol64:2323–2326
    [Google Scholar]
  8. Gillor O., Kirkup B. C., Riley M. A.. 2004; Colicins and microcins: the next generation antimicrobials. In Advances in Applied Microbiology vol. 54 pp129–146 Edited by Laskin A. I., Bennett J. W., Gadd G. M.. Amsterdam: Elsevier;
  9. Gillor O., Etzion A., Riley M. A.. 2008a; The dual role of bacteriocins as anti- and probiotics. Appl Microbiol Biotechnol81:591–606
    [Google Scholar]
  10. Gillor O., Vriezen J. A. C., Riley M. A.. 2008b; The role of SOS boxes in enteric bacteriocin regulation. Microbiology154:1783–1792
    [Google Scholar]
  11. Gordon D. M., Cowling A.. 2003; The distribution and genetic structure of Escherichia coli in Australian vertebrates: host and geographic effects. Microbiology149:3575–3586
    [Google Scholar]
  12. Gordon D. M., O'Brien C. L.. 2006; Bacteriocin diversity and the frequency of multiple bacteriocin production in Escherichia coli . Microbiology152:3239–3244
    [Google Scholar]
  13. Gordon D. M., Riley M. A.. 1999; A theoretical and empirical investigation of the invasion dynamics of colicinogeny. Microbiology145:655–661
    [Google Scholar]
  14. Gordon D. M., Riley M. A., Pinou T.. 1998; Temporal changes in the frequency of colicinogeny in Escherichia coli from house mice. Microbiology144:2233–2240
    [Google Scholar]
  15. Gordon D. M., Stern S. E., Collignon P. J.. 2005; Influence of the age and sex of human hosts on the distribution of Escherichia coli ECOR groups and virulence traits. Microbiology151:15–23
    [Google Scholar]
  16. Gordon D. M., Oliver E., Littlefield-Wyer J.. 2007; The diversity of bacteriocins in Gram-negative bacteria. In Bacteriocins: Ecology and Evolution pp5–18 Edited by Riley M. A., Chavan M. A.. New York: Springer;
  17. Harkness R. E., Braun V.. 1989a; Inhibition of lipopolysaccharide O-antigen synthesis by colicin-M. J Biol Chem264:14716–14722
    [Google Scholar]
  18. Harkness R. E., Braun V.. 1989b; Colicin-M inhibits peptidoglycan biosynthesis by interfering with lipid carrier recycling. J Biol Chem264:6177–6182
    [Google Scholar]
  19. Harkness R. E., Ölschläger T.. 1991; The biology of colicin-M. FEMS Microbiol Rev8:27–41
    [Google Scholar]
  20. Jeziorowski A., Gordon D. M.. 2007; Evolution of microcin V and colicin Ia plasmids in Escherichia coli . J Bacteriol189:7045–7052
    [Google Scholar]
  21. Johnson T. J., Johnson S. J., Nolan L. K.. 2006a; Complete DNA sequence of a ColBM plasmid from avian pathogenic Escherichia coli suggests that it evolved from closely related ColV virulence plasmids. J Bacteriol188:5975–5983
    [Google Scholar]
  22. Johnson T. J., Siek K. E., Johnson S. J., Nolan L. K.. 2006b; DNA sequence of a ColV plasmid and prevalence of selected plasmid-encoded virulence genes among avian Escherichia coli strains. J Bacteriol188:745–758
    [Google Scholar]
  23. Kirkup B. C., Riley M. A.. 2004; Antibiotic-mediated antagonism leads to a bacterial game of rock-paper-scissors in vivo . Nature428:412–414
    [Google Scholar]
  24. Köck J., Ölschläger T., Kamp R. M., Braun V.. 1987; Primary structure of colicin-M, an inhibitor of murein biosynthesis. J Bacteriol169:3358–3361
    [Google Scholar]
  25. 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 Genet251:407–411
    [Google Scholar]
  26. Ölschläger T., Braun V.. 1987; Sequence, expression and localization of the immunity protein for colicin-M. J Bacteriol169:4765–4769
    [Google Scholar]
  27. Ölschläger T., Schramm E., Braun V.. 1984; Cloning and expression of the activity and immunity genes of colicin-B and colicin-M on ColBM plasmids. Mol Gen Genet196:482–487
    [Google Scholar]
  28. Osborn A. M., Tatley F. M. D., Steyn L. M., Pickup R. W., Saunders J. R.. 2000; Mosaic plasmids and mosaic replicons: evolutionary lessons from the analysis of genetic diversity in IncFII-related replicons. Microbiology146:2267–2275
    [Google Scholar]
  29. Posada D., Crandall K. A.. 1998; modeltest: testing the model of DNA substitution. Bioinformatics14:817–818
    [Google Scholar]
  30. Pressler U., Braun V., Wittmannliebold B., Benz R.. 1986; Structural and functional properties of colicin-B. J Biol Chem261:2654–2659
    [Google Scholar]
  31. Pugsley A. P.. 1985; Escherichia coli- K12 strains for use in the identification and characterization of colicins. J Gen Microbiol131:369–376
    [Google Scholar]
  32. Pugsley A. P., Oudega B.. 1987; Methods of studying colicins and their plasmids. In Plasmids: a Practical Approach pp105–161 Edited by Hardy K. G. Oxford: IRL Press;
  33. Ratledge C., Dover L. G.. 2000; Iron metabolism in pathogenic bacteria. Annu Rev Microbiol54:881–941
    [Google Scholar]
  34. Riley M. A., Gordon D. M.. 1992; A survey of Col plasmids in natural isolates of Escherichia coli and an investigation into the stability of Col-plasmid lineages. J Gen Microbiol138:1345–1352
    [Google Scholar]
  35. Riley M. A., Gordon D. M.. 1999; The ecological role of bacteriocins in bacterial competition. Trends Microbiol7:129–133
    [Google Scholar]
  36. Riley M. A., Wertz J. E.. 2002; Bacteriocin diversity: ecological and evolutionary perspectives. Biochimie84:357–364
    [Google Scholar]
  37. Riley M. A., Goldstone C. M., Wertz J. E., Gordon D.. 2003; A phylogenetic approach to assessing the targets of microbial warfare. J Evol Biol16:690–697
    [Google Scholar]
  38. Rodriguez-Siek K. E., Giddings C. W., Doetkott C., Johnson T. J., Nolan L. K.. 2005; Characterizing the APEC pathotype. Vet Res36:241–256
    [Google Scholar]
  39. Sasarman A., Massie B., Zollinger M., Gagnetellier H., Shareck F., Garzon S., Morisset R.. 1980; Naturally-occurring RcolBM plasmids belonging to the IncfIII incompatibility group. J Gen Microbiol119:475–483
    [Google Scholar]
  40. Schaller K., Holtje J. V., Braun V.. 1982; Colicin-M is an inhibitor of murein biosynthesis. J Bacteriol152:994–1000
    [Google Scholar]
  41. Schramm E., Mende J., Braun V., Kamp R. M.. 1987; Nucleotide-sequence of the colicin-B activity gene cba : consensus pentapeptide among TonB-dependent colicins and receptors. J Bacteriol169:3350–3357
    [Google Scholar]
  42. Schramm E., Ölschläger T., Troger W., Braun V.. 1988; Sequence expression and localization of the immunity protein for colicin-B. Mol Gen Genet211:176–182
    [Google Scholar]
  43. Skyberg J. A., Johnson T. J., Johnson J. R., Clabots C., Logue C. A., Nolan L. K.. 2006; Acquisition of avian pathogenic Escherichia coli plasmids by a commensal E. coli isolate enhances its abilities to kill chicken embryos, grow in human urine and colonize the murine kidney. Infect Immun74:6287–6292
    [Google Scholar]
  44. Skyberg J. A., Johnson T. J., Nolan L. K.. 2008; Mutational and transcriptional analyses of an avian pathogenic Escherichia coli CoIV plasmid. BMC Microbiol8:24
    [Google Scholar]
  45. Swofford D. L.. 1993; paup – a computer program for phylogenetic inference using maximum parsimony. J Gen Physiol102:A9–A9
    [Google Scholar]
  46. Tamura K., Dudley J., Nei M., Kumar S.. 2007; mega4: molecular evolutionary genetics analysis (mega) software version 4.0. Mol Biol Evol24:1596–1599
    [Google Scholar]
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