Escherichia coli O157:H7 Shiga toxin-encoding bacteriophages: integrations, excisions, truncations, and evolutionary implications - PubMed (original) (raw)
Escherichia coli O157:H7 Shiga toxin-encoding bacteriophages: integrations, excisions, truncations, and evolutionary implications
Nurmohammad Shaikh et al. J Bacteriol. 2003 Jun.
Erratum in
- J Bacteriol. 2003 Nov;185(21):6495
Abstract
As it descended from Escherichia coli O55:H7, Shiga toxin (Stx)-producing E. coli (STEC) O157:H7 is believed to have acquired, in sequence, a bacteriophage encoding Stx2 and another encoding Stx1. Between these events, sorbitol-fermenting E. coli O157:H(-) presumably diverged from this clade. We employed PCR and sequence analyses to investigate sites of bacteriophage integration into the chromosome, using evolutionarily informative STEC to trace the sequence of acquisition of elements encoding Stx. Contrary to expectations from the two currently sequenced strains, truncated bacteriophages occupy yehV in almost all E. coli O157:H7 strains that lack stx(1) (stx(1)-negative strains). Two truncated variants were determined to contain either GTT or TGACTGTT sequence, in lieu of 20,214 or 18,895 bp, respectively, of the bacteriophage central region. A single-nucleotide polymorphism in the latter variant suggests that recombination in that element extended beyond the inserted octamer. An stx(2) bacteriophage usually occupies wrbA in stx(1)(+)/stx(2)(+) E. coli O157:H7, but wrbA is unexpectedly unoccupied in most stx(1)-negative/stx(2)(+) E. coli O157:H7 strains, the presumed progenitors of stx(1)(+)/stx(2)(+) E. coli O157:H7. Trimethoprim-sulfamethoxazole promotes the excision of all, and ciprofloxacin and fosfomycin significantly promote the excision of a subset of complete and truncated stx bacteriophages from the E. coli O157:H7 strains tested; bile salts usually attenuate excision. These data demonstrate the unexpected diversity of the chromosomal architecture of E. coli O157:H7 (with novel truncated bacteriophages and multiple stx(2) bacteriophage insertion sites), suggest that stx(1) acquisition might be a multistep process, and compel the consideration of multiple exogenous factors, including antibiotics and bile, when chromosome stability is examined.
Figures
FIG. 1.
Amplicons for investigation of the yehV and wrbA integration sites in E. coli O157:H7. Bacterial strains used, loci examined, and lengths of resulting amplicons are listed across the top and to the left and right of the rows of amplicons, respectively. LJ, left junction; RJ, right junction.
FIG. 2.
Structures of two forms of truncated bacteriophages of _stx1_-negative E. coli O157:H7. Inserted GTT and TGACTGTT sequences replace segments that are found in truncated stx1 bacteriophages in two sequenced strains. ORF borders, proportions, and designations and nucleotide positions relate to those in reference . An A→G SNP 108 nucleotides 5′ to the octamer in both sequenced Δ18,895 bacteriophages and primer locations used to generate data pertaining to stx1 bacteriophages are noted. A, E, I, K, L, J, F, and B are primers.
FIG. 3.
Amplicons elicited across integration sites, in response to antibiotics and bile salts. E. coli O157:H7 strain 87-20 was grown in LB without (lanes 1 and 2) or with (lanes 3 and 4) TMP-SMX, ciprofloxacin (lanes 5 and 6), or ampicillin (lanes 7 and 8) or in LB with G-6-P without (lanes 9 and 10) or with (lanes 11 and 12) fosfomycin. Samples in even-number lanes were grown in bile salts. Loci examined and lengths of resulting amplicons are listed to the right and left of the rows. LJ, left junction; RJ, right junction.
FIG. 4.
Evolutionary scenarios. Serotypes, phenotypes, genotypes, critical events, and postulated intermediate form (circle) in three different scenarios leading to the five STEC 1 forms known to exist today (boxes). One asterisk indicates that the sequence of listed events is not known but is presumed to have occurred at different times during evolution. This result would obviate the need for postulated lineage B or C to produce such an organism. Two asterisks indicate that organisms in this box would not exist if lineage A exists.
Similar articles
- Escherichia coli serotype O55:H7 diversity supports parallel acquisition of bacteriophage at Shiga toxin phage insertion sites during evolution of the O157:H7 lineage.
Kyle JL, Cummings CA, Parker CT, Quiñones B, Vatta P, Newton E, Huynh S, Swimley M, Degoricija L, Barker M, Fontanoz S, Nguyen K, Patel R, Fang R, Tebbs R, Petrauskene O, Furtado M, Mandrell RE. Kyle JL, et al. J Bacteriol. 2012 Apr;194(8):1885-96. doi: 10.1128/JB.00120-12. Epub 2012 Feb 10. J Bacteriol. 2012. PMID: 22328665 Free PMC article. - Toxigenic properties and stx phage characterization of Escherichia coli O157 isolated from animal sources in a developing country setting.
Rahman M, Nabi A, Asadulghani M, Faruque SM, Islam MA. Rahman M, et al. BMC Microbiol. 2018 Aug 31;18(1):98. doi: 10.1186/s12866-018-1235-3. BMC Microbiol. 2018. PMID: 30170562 Free PMC article. - Is Shiga Toxin-Negative Escherichia coli O157:H7 Enteropathogenic or Enterohemorrhagic Escherichia coli? Comprehensive Molecular Analysis Using Whole-Genome Sequencing.
Ferdous M, Zhou K, Mellmann A, Morabito S, Croughs PD, de Boer RF, Kooistra-Smid AM, Rossen JW, Friedrich AW. Ferdous M, et al. J Clin Microbiol. 2015 Nov;53(11):3530-8. doi: 10.1128/JCM.01899-15. Epub 2015 Aug 26. J Clin Microbiol. 2015. PMID: 26311863 Free PMC article. - Stx-phages: drivers and mediators of the evolution of STEC and STEC-like pathogens.
Allison HE. Allison HE. Future Microbiol. 2007 Apr;2(2):165-74. doi: 10.2217/17460913.2.2.165. Future Microbiol. 2007. PMID: 17661653 Review. - Shiga toxin: expression, distribution, and its role in the environment.
Mauro SA, Koudelka GB. Mauro SA, et al. Toxins (Basel). 2011 Jun;3(6):608-25. doi: 10.3390/toxins3060608. Epub 2011 Jun 14. Toxins (Basel). 2011. PMID: 22069728 Free PMC article. Review.
Cited by
- Phylogenetic and molecular analysis of food-borne shiga toxin-producing Escherichia coli.
Hauser E, Mellmann A, Semmler T, Stoeber H, Wieler LH, Karch H, Kuebler N, Fruth A, Harmsen D, Weniger T, Tietze E, Schmidt H. Hauser E, et al. Appl Environ Microbiol. 2013 Apr;79(8):2731-40. doi: 10.1128/AEM.03552-12. Epub 2013 Feb 15. Appl Environ Microbiol. 2013. PMID: 23417002 Free PMC article. - Escherichia coli serotype O55:H7 diversity supports parallel acquisition of bacteriophage at Shiga toxin phage insertion sites during evolution of the O157:H7 lineage.
Kyle JL, Cummings CA, Parker CT, Quiñones B, Vatta P, Newton E, Huynh S, Swimley M, Degoricija L, Barker M, Fontanoz S, Nguyen K, Patel R, Fang R, Tebbs R, Petrauskene O, Furtado M, Mandrell RE. Kyle JL, et al. J Bacteriol. 2012 Apr;194(8):1885-96. doi: 10.1128/JB.00120-12. Epub 2012 Feb 10. J Bacteriol. 2012. PMID: 22328665 Free PMC article. - Genotypic Features of Clinical and Bovine Escherichia coli O157 Strains Isolated in Countries with Different Associated-Disease Incidences.
Pianciola L, Rivas M. Pianciola L, et al. Microorganisms. 2018 Apr 27;6(2):36. doi: 10.3390/microorganisms6020036. Microorganisms. 2018. PMID: 29702577 Free PMC article. Review. - First step in using molecular data for microbial food safety risk assessment; hazard identification of Escherichia coli O157:H7 by coupling genomic data with in vitro adherence to human epithelial cells.
Pielaat A, Boer MP, Wijnands LM, van Hoek AH, Bouw E, Barker GC, Teunis PF, Aarts HJ, Franz E. Pielaat A, et al. Int J Food Microbiol. 2015 Nov 20;213:130-8. doi: 10.1016/j.ijfoodmicro.2015.04.009. Epub 2015 Apr 10. Int J Food Microbiol. 2015. PMID: 25910947 Free PMC article.
References
- Araujo, R., M. Muniesa, J. Mendez, A. Puig, N. Queralt, F. Lucena, and J. Jofre. 2001. Optimisation and standardisation of a method for detecting and enumerating bacteriophages infecting Bacteroides fragilis. J. Virol. Methods 93:127-136. - PubMed
- Ashkenazi, S., M. Larocco, B. E. Murray, and T. G. Cleary. 1992. The adherence of verocytotoxin-producing Escherichia coli to rabbit intestinal cells. J. Med. Microbiol. 37:304-309. - PubMed
- Bell, B. P., M. Goldoft, P. M. Griffin, M. A. Davis, D. C. Gordon, P. I. Tarr, C. A. Bartleson, J. H. Lewis, T. J. Barrett, and J. G. Wells. 1994. A multistate outbreak of Escherichia coli O157:H7-associated bloody diarrhea and hemolytic uremic syndrome from hamburgers. The Washington experience. JAMA 272:1349-1353. - PubMed
Publication types
MeSH terms
Substances
LinkOut - more resources
Full Text Sources
Other Literature Sources
Molecular Biology Databases
Research Materials