1887

Abstract

Type II toxin–antitoxin systems (TAs) are bicistronic operons ubiquitous in prokaryotic genomes, displaying multilevel association with cell physiology. Various possible functions have been assigned to TAs, ranging from beneficial for their hosts, such as a stress response, dormancy and protection against genomic parasites, to detrimental or useless functions, such as selfish alleles. As there is a link between several features (e.g. virulence, lifestyle) and the phylogeny of this species, we hypothesized a similar association with TAs. Using PCR we studied the distribution of 15 chromosomal and plasmidic type II TA loci in 84 clinical isolates in relation to their main phylogenetic groups (A, B1, B2 and D). In addition, we performed searching of these TA loci in 60 completely sequenced genomes deposited in GenBank. The highest number of TA loci per strain was observed in group A (mean 8.2, range 5–12) and the lowest in group B2 (mean 4.2, range 2–8). Moreover, significant differences in the prevalence of nine chromosomal TAs among phylogroups were noted. In conclusion, the presence of some chromosomal TAs in is phylogroup-related rather than a universal feature of the species. In addition, their limited collection in group B2 clearly distinguish it from the other phylogroups.

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2015-01-01
2024-12-07
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References

  1. Alikhan N. F., Petty N. K., Ben Zakour N. L., Beatson S. A. 2011; BLAST Ring Image Generator (BRIG): simple prokaryote genome comparisons. BMC Genomics 12:402 [View Article][PubMed]
    [Google Scholar]
  2. Anonymous 2013; Standard operating procedure for PulseNet PFGE of Escherichia coli O157 : H7, Escherichia coli non-O157 (STEC), Salmonella serotypes, Shigella sonnei and Shigella flexneri. http://www.cdc.gov/pulsenet/PDF/ecoli-shigella-salmonella-pfge-protocol-508c.pdf
    [Google Scholar]
  3. Bergthorsson U., Ochman H. 1998; Distribution of chromosome length variation in natural isolates of Escherichia coli. Mol Biol Evol 15:6–16 [View Article][PubMed]
    [Google Scholar]
  4. Bukh A. S., Schønheyder H. C., Emmersen J. M. G., Søgaard M., Bastholm S., Roslev P. 2009; Escherichia coli phylogenetic groups are associated with site of infection and level of antibiotic resistance in community-acquired bacteraemia: a 10 year population-based study in Denmark. J Antimicrob Chemother 64:163–168 [View Article][PubMed]
    [Google Scholar]
  5. Carlos C., Pires M. M., Stoppe N. C., Hachich E. M., Sato M. I. Z., Gomes T. A. T., Amaral L. A., Ottoboni L. M. M. 2010; Escherichia coli phylogenetic group determination and its application in the identification of the major animal source of fecal contamination. BMC Microbiol 10:161 [View Article][PubMed]
    [Google Scholar]
  6. Chaudhuri R. R., Henderson I. R. 2012; The evolution of the Escherichia coli phylogeny. Infect Genet Evol 12:214–226 [View Article][PubMed]
    [Google Scholar]
  7. Clermont O., Bonacorsi S., Bingen E. 2000; Rapid and simple determination of the Escherichia coli phylogenetic group. Appl Environ Microbiol 66:4555–4558 [View Article][PubMed]
    [Google Scholar]
  8. Clermont O., Lescat M., O’Brien C. L., Gordon D. M., Tenaillon O., Denamur E. 2008; Evidence for a human-specific Escherichia coli clone. Environ Microbiol 10:1000–1006 [View Article][PubMed]
    [Google Scholar]
  9. Cruz J. W., Rothenbacher F. P., Maehigashi T., Lane W. S., Dunham C. M., Woychik N. A. 2014; Doc toxin is a kinase that inactivates elongation factor Tu. J Biol Chem 289:7788–7798 [View Article][PubMed]
    [Google Scholar]
  10. Dong T., Schellhorn H. E. 2010; Role of RpoS in virulence of pathogens. Infect Immun 78:887–897 [View Article][PubMed]
    [Google Scholar]
  11. Escobar-Páramo P., Clermont O., Blanc-Potard A.-B., Bui H., Le Bouguénec C., Denamur E. 2004; A specific genetic background is required for acquisition and expression of virulence factors in Escherichia coli. Mol Biol Evol 21:1085–1094 [View Article][PubMed]
    [Google Scholar]
  12. Fitzgerald-Hughes D., Bolkvadze D., Balarjishvili N., Leshkasheli L., Ryan M., Burke L., Stevens N., Humphreys H., Kutateladze M. 2014; Susceptibility of extended-spectrum-β-lactamase-producing Escherichia coli to commercially available and laboratory-isolated bacteriophages. J Antimicrob Chemother 69:1148–1150 [View Article][PubMed]
    [Google Scholar]
  13. Goeders N., Van Melderen L. 2014; Toxin-antitoxin systems as multilevel interaction systems. Toxins (Basel) 6:304–324 [View Article][PubMed]
    [Google Scholar]
  14. Gordon D. M., Cowling A. 2003; The distribution and genetic structure of Escherichia coli in Australian vertebrates: host and geographic effects. Microbiology 149:3575–3586 [View Article][PubMed]
    [Google Scholar]
  15. Hong S. H., Wang X., O’Connor H. F., Benedik M. J., Wood T. K. 2012; Bacterial persistence increases as environmental fitness decreases. Microb Biotechnol 5:509–522 [View Article][PubMed]
    [Google Scholar]
  16. Hu Y., Benedik M. J., Wood T. K. 2012; Antitoxin DinJ influences the general stress response through transcript stabilizer CspE. Environ Microbiol 14:669–679 [View Article][PubMed]
    [Google Scholar]
  17. Jayaraman R. 2008; Bacterial persistence: some new insights into an old phenomenon. J Biosci 33:795–805 [View Article][PubMed]
    [Google Scholar]
  18. Johnson J. R., Delavari P., Kuskowski M., Stell A. L. 2001; Phylogenetic distribution of extraintestinal virulence-associated traits in Escherichia coli. J Infect Dis 183:78–88 [View Article][PubMed]
    [Google Scholar]
  19. Kaspy I., Rotem E., Weiss N., Ronin I., Balaban N. Q., Glaser G. 2013; HipA-mediated antibiotic persistence via phosphorylation of the glutamyl-tRNA-synthetase. Nat Commun 4:3001 [View Article][PubMed]
    [Google Scholar]
  20. Kolodkin-Gal I., Verdiger R., Shlosberg-Fedida A., Engelberg-Kulka H. 2009; A differential effect of E. coli toxin-antitoxin systems on cell death in liquid media and biofilm formation. PLoS ONE 4:e6785 [View Article][PubMed]
    [Google Scholar]
  21. Leplae R., Geeraerts D., Hallez R., Guglielmini J., Drèze P., Van Melderen L. 2011; Diversity of bacterial type II toxin-antitoxin systems: a comprehensive search and functional analysis of novel families. Nucleic Acids Res 39:5513–5525 [View Article][PubMed]
    [Google Scholar]
  22. Lewis K. 2010; Persister cells. Annu Rev Microbiol 64:357–372 [View Article][PubMed]
    [Google Scholar]
  23. Lin C.-Y., Awano N., Masuda H., Park J.-H., Inouye M. 2013; Transcriptional repressor HipB regulates the multiple promoters in Escherichia coli. J Mol Microbiol Biotechnol 23:440–447 [View Article][PubMed]
    [Google Scholar]
  24. Magnuson R. D. 2007; Hypothetical functions of toxin-antitoxin systems. J Bacteriol 189:6089–6092 [View Article][PubMed]
    [Google Scholar]
  25. Makarova K. S., Wolf Y. I., Koonin E. V. 2009; Comprehensive comparative-genomic analysis of type 2 toxin-antitoxin systems and related mobile stress response systems in prokaryotes. Biol Direct 4:19 [View Article][PubMed]
    [Google Scholar]
  26. Makarova K. S., Wolf Y. I., Koonin E. V. 2013; Comparative genomics of defense systems in archaea and bacteria. Nucleic Acids Res 41:4360–4377 [View Article][PubMed]
    [Google Scholar]
  27. Mine N., Guglielmini J., Wilbaux M., Van Melderen L. 2009; The decay of the chromosomally encoded ccdO157 toxin-antitoxin system in the Escherichia coli species. Genetics 181:1557–1566 [View Article][PubMed]
    [Google Scholar]
  28. Norton J. P., Mulvey M. A. 2012; Toxin-antitoxin systems are important for niche-specific colonization and stress resistance of uropathogenic Escherichia coli. PLoS Pathog 8:e1002954 [View Article][PubMed]
    [Google Scholar]
  29. Nowrouzian F. L., Wold A. E., Adlerberth I. 2005; Escherichia coli strains belonging to phylogenetic group B2 have superior capacity to persist in the intestinal microflora of infants. J Infect Dis 191:1078–1083 [View Article][PubMed]
    [Google Scholar]
  30. Olson M. E., Ceri H., Morck D. W., Buret A. G., Read R. R. 2002; Biofilm bacteria: formation and comparative susceptibility to antibiotics. Can J Vet Res 66:86–92[PubMed]
    [Google Scholar]
  31. Pandey D. P., Gerdes K. 2005; Toxin-antitoxin loci are highly abundant in free-living but lost from host-associated prokaryotes. Nucleic Acids Res 33:966–976 [View Article][PubMed]
    [Google Scholar]
  32. Rankin D. J., Turner L. A., Heinemann J. A., Brown S. P. 2012; The coevolution of toxin and antitoxin genes drives the dynamics of bacterial addiction complexes and intragenomic conflict. Proc Biol Sci 279:3706–3715 [View Article][PubMed]
    [Google Scholar]
  33. Rozen S., Skaletsky H. J. 1998; Primer3. Code available at http://www-genome.wi.mit.edu/genome_software/other/primer3.html.
    [Google Scholar]
  34. Saavedra De Bast M., Mine N., Van Melderen L. 2008; Chromosomal toxin-antitoxin systems may act as antiaddiction modules. J Bacteriol 190:4603–4609 [View Article][PubMed]
    [Google Scholar]
  35. Sala A., Bordes P., Fichant G., Genevaux P. 2013; Toxin-antitoxin loci in Mycobacterium tuberculosis. In Prokaryotic Toxin-Antitoxins pp. 295–314 Edited by Gerdes K. Berlin: Springer; [View Article]
    [Google Scholar]
  36. Soo V. W. C., Wood T. K. 2013; Antitoxin MqsA represses curli formation through the master biofilm regulator CsgD. Sci Rep 3:3186 [View Article][PubMed]
    [Google Scholar]
  37. Tenaillon O., Skurnik D., Picard B., Denamur E. 2010; The population genetics of commensal Escherichia coli. Nat Rev Microbiol 8:207–217 [View Article][PubMed]
    [Google Scholar]
  38. Touchon M., Charpentier S., Clermont O., Rocha E. P. C., Denamur E., Branger C. 2011; CRISPR distribution within the Escherichia coli species is not suggestive of immunity-associated diversifying selection. J Bacteriol 193:2460–2467 [View Article][PubMed]
    [Google Scholar]
  39. Tsilibaris V., Maenhaut-Michel G., Mine N., Van Melderen L. 2007; What is the benefit to Escherichia coli of having multiple toxin-antitoxin systems in its genome?. J Bacteriol 189:6101–6108 [View Article][PubMed]
    [Google Scholar]
  40. Unterholzner S. J., Poppenberger B., Rozhon W. 2013; Toxin-antitoxin systems: biology, identification, and application. Mobile Genet Elements 3:e26219 [View Article][PubMed]
    [Google Scholar]
  41. Van Melderen L. 2010; Toxin-antitoxin systems: why so many, what for?. Curr Opin Microbiol 13:781–785 [View Article][PubMed]
    [Google Scholar]
  42. Van Melderen L., Saavedra De Bast M. 2009; Bacterial toxin-antitoxin systems: more than selfish entities?. PLoS Genet 5:e1000437 [View Article][PubMed]
    [Google Scholar]
  43. Vieira G., Sabarly V., Bourguignon P.-Y., Durot M., Le Fèvre F., Mornico D., Vallenet D., Bouvet O., Denamur E.& other authors ( 2011; Core and panmetabolism in Escherichia coli. J Bacteriol 193:1461–1472 [View Article][PubMed]
    [Google Scholar]
  44. Walk S. T., Alm E. W., Calhoun L. M., Mladonicky J. M., Whittam T. S. 2007; Genetic diversity and population structure of Escherichia coli isolated from freshwater beaches. Environ Microbiol 9:2274–2288 [View Article][PubMed]
    [Google Scholar]
  45. Wang X., Wood T. K. 2011; Toxin-antitoxin systems influence biofilm and persister cell formation and the general stress response. Appl Environ Microbiol 77:5577–5583 [View Article][PubMed]
    [Google Scholar]
  46. White A. P., Surette M. G. 2006; Comparative genetics of the rdar morphotype in Salmonella. J Bacteriol 188:8395–8406 [View Article][PubMed]
    [Google Scholar]
  47. White A. P., Sibley K. A., Sibley C. D., Wasmuth J. D., Schaefer R., Surette M. G., Edge T. A., Neumann N. F. 2011; Intergenic sequence comparison of Escherichia coli isolates reveals lifestyle adaptations but not host specificity. Appl Environ Microbiol 77:7620–7632 [View Article][PubMed]
    [Google Scholar]
  48. Williams J. J., Hergenrother P. J. 2012; Artificial activation of toxin-antitoxin systems as an antibacterial strategy. Trends Microbiol 20:291–298 [View Article][PubMed]
    [Google Scholar]
  49. Yamaguchi Y., Inouye M. 2011; Regulation of growth and death in Escherichia coli by toxin-antitoxin systems. Nat Rev Microbiol 9:779–790 [View Article][PubMed]
    [Google Scholar]
  50. Zhao J., Wang Q., Li M., Heijstra B. D., Wang S., Liang Q., Qi Q. 2013; Escherichia coli toxin gene hipA affects biofilm formation and DNA release. Microbiology 159:633–640 [View Article][PubMed]
    [Google Scholar]
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