Molecular Insights Into the Evolutionary Pathway of O1 Atypical El Tor Variants

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In this report, we suggest a genetic mechanism of how the V. cholerae atypical El Tor variants were generated from classical and prototype El Tor biotype strains. An intermediary strain, containing the CTX-1 and CTX-2 prophages, was identified among the clinical isolates that were collected in 1991, when the atypical strains emerged. This strain can be converted into various Wave 2 atypical El Tor strains by eliminating prototype components, CTX-1 and RS1. Further, new types of the CTX phage genome can be generated from the intermediary strain by inter-chromosomal recombination between CTX phages and recombination between the CTX phage and RS1. These new CTX phages can be transduced into other El Tor strains, transforming them into Wave 3 atypical strains. This is a demonstrated instance of how a single-segment-genome CTX phage re-organizes its genome through recombination between different types of phage, leading to generation of new phage variants and atypical El Tor strains.

Vyšlo v časopise: Molecular Insights Into the Evolutionary Pathway of O1 Atypical El Tor Variants. PLoS Pathog 10(9): e32767. doi:10.1371/journal.ppat.1004384
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1004384

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Zdroje

1. KaperJB, MorrisJGJr, LevineMM (1995) Cholera. Clin Microbiol Rev 8: 48–86.

2. SackDA, SackRB, NairGB, SiddiqueAK (2004) Cholera. Lancet 363: 223–233.

3. ChoiSY, LeeJH, KimEJ, LeeHR, JeonYS, et al. (2010) Classical RS1 and environmental RS1 elements in Vibrio cholerae O1 El Tor strains harbouring a tandem repeat of CTX prophage: revisiting Mozambique in 2005. J Med Microbiol 59: 302–308.

4. BoydEF, HeilpernAJ, WaldorMK (2000) Molecular analyses of a putative CTXΦ precursor and evidence for independent acquisition of distinct CTXΦs by toxigenic Vibrio cholerae. J Bacteriol 182: 5530–5538.

5. NairGB, QadriF, HolmgrenJ, SvennerholmAM, SafaA, et al. (2006) Cholera due to altered El Tor strains of Vibrio cholerae O1 in Bangladesh. J Clin Microbiol 44: 4211–4213.

6. SafaA, NairGB, KongRY (2010) Evolution of new variants of Vibrio cholerae O1. Trends Microbiol 18: 46–54.

7. MoritaM, OhnishiM, ArakawaE, YamamotoS, NairGB, et al. (2010) Emergence and genetic diversity of El Tor Vibrio cholerae O1 that possess classical biotype ctxB among travel-associated cases of cholera in Japan. J Med Microbiol 59: 708–712.

8. LeeJH, ChoiSY, JeonYS, LeeHR, KimEJ, et al. (2009) Classification of hybrid and altered Vibrio cholerae strains by CTX prophage and RS1 element structure. J Microbiol 47: 783–788.

9. AnsaruzzamanM, BhuiyanNA, NairBG, SackDA, LucasM, et al. (2004) Cholera in Mozambique, variant of Vibrio cholerae. Emerg Infect Dis 10: 2057–2059.

10. MutrejaA, KimDW, ThomsonNR, ConnorTR, LeeJH, et al. (2011) Evidence for several waves of global transmission in the seventh cholera pandemic. Nature 477: 462–465.

11. NguyenBM, LeeJH, CuongNT, ChoiSY, HienNT, et al. (2009) Cholera outbreaks caused by an altered Vibrio cholerae O1 El Tor biotype strain producing classical cholera toxin B in Vietnam in 2007 to 2008. J Clin Microbiol 47: 1568–1571.

12. ChoiSY, LeeJH, JeonYS, LeeHR, KimEJ, et al. (2010) Multilocus variable-number tandem repeat analysis of Vibrio cholerae O1 El Tor strains harbouring classical toxin B. J Med Microbiol 59: 763–769.

13. NahaA, PazhaniGP, GangulyM, GhoshS, RamamurthyT, et al. (2012) Development and evaluation of a PCR assay for tracking the emergence and dissemination of Haitian variant ctxB in Vibrio cholerae O1 strains isolated from Kolkata, India. J Clin Microbiol 50: 1733–1736.

14. ChinCS, SorensonJ, HarrisJB, RobinsWP, CharlesRC, et al. (2011) The origin of the Haitian cholera outbreak strain. N Engl J Med 364: 33–42.

15. ShakyaG, KimDW, ClemensJD, MallaS, UpadhyayaBP, et al. (2012) Phenotypic and genetic characterization of Vibrio cholerae O1 clinical isolates collected through national antimicrobial resistance surveillance network in Nepal. World J Microbiol Biotechnol 28: 2671–2678.

16. PatraT, ChatterjeeS, RaychoudhuriA, MukhopadhyayAK, RamamurthyT, et al. (2011) Emergence and progression of Vibrio cholerae O1 El Tor variants and progenitor strains of Mozambique variants in Kolkata, India. Int J Med Microbiol 301: 310–317.

17. UddenSM, ZahidMS, BiswasK, AhmadQS, CraviotoA, et al. (2008) Acquisition of classical CTX prophage from Vibrio cholerae O141 by El Tor strains aided by lytic phages and chitin-induced competence. Proc Natl Acad Sci U S A 105: 11951–11956.

18. KimEJ, LeeD, MoonSH, LeeCH, KimDW (2014) CTX prophages in Vibrio cholerae O1 strains. J Microbiol Biotechnol 24: 725–731.

19. SurD, LopezAL, KanungoS, PaisleyA, MannaB, et al. (2009) Efficacy and safety of a modified killed-whole-cell oral cholera vaccine in India: an interim analysis of a cluster-randomised, double-blind, placebo-controlled trial. Lancet 374: 1694–1702.

20. LeeJH, HanKH, ChoiSY, LucasME, MondlaneC, et al. (2006) Multilocus sequence typing (MLST) analysis of Vibrio cholerae O1 El Tor isolates from Mozambique that harbour the classical CTX prophage. J Med Microbiol 55: 165–170.

21. WaldorMK, MekalanosJJ (1996) Lysogenic conversion by a filamentous phage encoding cholera toxin. Science 272: 1910–1914.

22. FaruqueSM, TamVC, ChowdhuryN, DiraphatP, DziejmanM, et al. (2007) Genomic analysis of the Mozambique strain of Vibrio cholerae O1 reveals the origin of El Tor strains carrying classical CTX prophage. Proc Natl Acad Sci U S A 104: 5151–5156.

23. GrimCJ, HasanNA, TavianiE, HaleyB, ChunJ, et al. (2010) Genome sequence of hybrid Vibrio cholerae O1 MJ-1236, B-33, and CIRS101 and comparative genomics with V. cholerae. J Bacteriol 192: 3524–3533.

24. DavisBM, WaldorMK (2000) CTXΦ contains a hybrid genome derived from tandemly integrated elements. Proc Natl Acad Sci U S A 97: 8572–8577.

25. ChunJ, GrimCJ, HasanNA, LeeJH, ChoiSY, et al. (2009) Comparative genomics reveals mechanism for short-term and long-term clonal transitions in pandemic Vibrio cholerae. Proc Natl Acad Sci U S A 106: 15442–15447.

26. ChoYJ, YiH, LeeJH, KimDW, ChunJ (2010) Genomic evolution of Vibrio cholerae. Curr Opin Microbiol 13: 646–651.

27. HalderK, DasB, NairGB, BhadraRK (2010) Molecular evidence favouring step-wise evolution of Mozambique Vibrio cholerae O1 El Tor hybrid strain. Microbiology 156: 99–107.

28. HendriksenRS, PriceLB, SchuppJM, GilleceJD, KaasRS, et al. (2011) Population genetics of Vibrio cholerae from Nepal in 2010: evidence on the origin of the Haitian outbreak. mBio 2: e00157–11.

29. SiddiqueAK, NairGB, AlamM, SackDA, HuqA, et al. (2010) El Tor cholera with severe disease: a new threat to Asia and beyond. Epidemiol Infect 138: 347–352.

30. DonnenbergMS, KaperJB (1991) Construction of an eae deletion mutant of enteropathogenic Escherichia coli by using a positive-selection suicide vector. Infect Immun 59: 4310–4317.

31. DasB, BischerourJ, BarreFX (2011) VGJΦ integration and excision mechanisms contribute to the genetic diversity of Vibrio cholerae epidemic strains. Proc Natl Acad Sci U S A 108: 2516–2521.

32. KimDW, LenzenG, PageAL, LegrainP, SansonettiPJ, et al. (2005) The Shigella flexneri effector OspG interferes with innate immune responses by targeting ubiquitin-conjugating enzymes. Proc Natl Acad Sci U S A 102: 14046–14051.