Phage-mediated Shiga toxin (Stx) horizontal gene transfer and expression in non-Shiga toxigenic Enterobacter and Escherichia coli strains

Pathogens and Disease

Volumn 74, Issue 5, 2016, Pages

  Khalil, Rowaida K S ^a   Skinner, Craig ^b   Patfield, Stephanie ^b   He, Xiaohua ^b  

^a Alexandria University Faculty Of Science   (Egypt)

^b WESTERN REGIONAL RESEARCH CENTER   (United States)

Author keywords

ELISA; Enterobacter cloacae; Escherichia coli O157; Horizontal gene transfer; Stx converting bacteriophages; Transduction

Indexed keywords

SHIGA TOXIN;

ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIOPHAGE; BACTERIUM DETECTION; ENTEROBACTER CLOACAE; ENTEROBACTERIACEAE INFECTION; ENZYME LINKED IMMUNOSORBENT ASSAY; FOOD POISONING; HORIZONTAL GENE TRANSFER; HOST RANGE; LYSOGENIZATION; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SEQUENCE ANALYSIS; SEROTYPE; SHIGA TOXIN PRODUCING ESCHERICHIA COLI; WESTERN BLOTTING; BACTERIOLYSIS; ENTEROBACTER; ESCHERICHIA COLI; GENE EXPRESSION; GENETIC TRANSDUCTION; GENETICS; PHYSIOLOGY; VIROLOGY;

BACTERIOLYSIS; BACTERIOPHAGES; ENTEROBACTER; ESCHERICHIA COLI; GENE EXPRESSION; GENE TRANSFER, HORIZONTAL; HOST SPECIFICITY; SHIGA TOXIN; TRANSDUCTION, GENETIC;

EID: 84979562950     PISSN: None     EISSN: 2049632X     Source Type: Journal    
DOI: 10.1093/femspd/ftw037     Document Type: Article

References (84)

1. Aertsen A, Faster D, Michiels CW. Induction of Shiga toxinconverting prophage in Escherichia coli by high hydrostatic pressure. Appl Environ Microb 2005;71:1155-62.
2. Allison HE. Stx-phages: drivers and mediators of the evolution of STEC and STEC-like pathogens. Future Microbiol 2007; 2:165-74.
3. Allison HE, Sergeant MJ, James CE et al. Immunity profiles of wild-type and recombinant Shiga-like toxin-encoding bacteriophages and characterization of novel double lysogens. Infect Immun 2003;71:3409-18.
4. Alperi A, Figuera MJ. Human isolates of Aeromonas possess Shiga toxin genes (stx1 and stx2) highly similar to the most virulent gene variants of Escherichia coli. Clin Microbiol Infect 2010;16:1563-7.
5. Anderson B, Rashid MH, Carter C et al. Enumeration of bacteriophage particles: comparative analysis of the traditional plaque assay and real-time QPCR-and nanosight-based assays. Bacteriophage 2011;1:86-93.
6. Babu MM, Aravind L. Adaptive evolution by optimizing expression levels in different environments. Trends Microbiol 2006;14:11-4.
7. Besser TE, Shaikh N, Holt NJ et al. Greater diversity of Shiga toxinencoding bacteriophage insertion sites among Escherichia coli O157:H7 isolates from cattle than in those from humans. Appl Environ Microb 2007;73:671-9.
8. Bielaszewska M, Prager R, Köck R et al. Shiga toxin gene loss and transfer in vitro and in vivo during enterohemorrhagic Escherichia coli O26 infection in humans. Appl Environ Microb 2007;73:3144-50.
9. Bloch S, Nejman-Faleńczyk B, Topka G et al. UV-sensitivity of Shiga toxin-converting bacteriophage virions Φ24B, 933W, P22, P27 and P32. Toxins 2015;7:3727-39.
10. Brabban AD, Hite E, Callaway TR. Evolution of foodborne pathogens via temperate bacteriophage-mediated gene transfer. Foodborne Pathog Dis 2005;2:287-303.
11. Carlson K. Appendix: working with bacteriophages: common techniques and methodological approaches. In: Sulakvelidze A, Kutter E (eds). Bacteriophages: Biology and Applications. Boca Raton, FL, USA: CRC Press, 2005, 439-90.
12. Chibani-Chennoufi S, Bruttin A, Dillmann ML et al. Phagehost interaction: an ecological perspective. J Bacteriol 2004;186:3677-86.
13. Choi C, Kuatsjah E, Wu E et al. The effect of cell size on the burst size of T4 bacteriophage infections of Escherichia coli B23. J Exp Microbiol Immunol 2010;14:85-91.
14. Cornick NA, Helgerson AF, Mai V et al. In vivo transduction of an Stx-encoding phage in ruminants. Appl Environ Microb 2006;72:5086-8.
15. Davin-Regli A, Jean-Marie P. Enterobacter aerogenes and Enterobacter cloacae; versatile bacterial pathogens confronting antibiotic treatment. Front Microbiol 2015;6:392.
16. de Sablet T, Bertin Y, Vareille M et al. Differential expression of stx2 variants in Shiga toxin-producing Escherichia coli belonging to seropathotypes A and C. Microbiol 2008;154:176-86.
17. Emond E, Molineau S. Bacteriophages and food fermentations. In: McGrathe S, Van Sinderen D (eds). Bacteriophages, Genetics and Molecular Biology. Norfolk, UK: Caiste Academic Press, 2007.
18. Ethelberg S, Olsen KE, Scheutz F et al. Virulence factors for hemolytic uremic syndrome, Denmark. Emerg Infect Dis 2004;10:842-7.
19. Feiner R, Argov T, Rabinovich L et al. A new perspective on lysogeny: prophages as active regulatory switches of bacteria. Nat Rev Microbiol 2015;13:641-50.
20. Gamage SD, McGannon CM, Weiss AA. Escherichia coli serogroup O107/O117 lipopolysaccharide binds and neutralizes Shiga toxin 2. J Bacteriol 2004;186:5506-12
21. Gamage SD, Strasser JE, Chalk CL et al. Nonpathogenic Escherichia coli can contribute to the production of Shiga toxin. Infect Immun 2003;71:3107-15.
22. Grau-Leal F, Quirós P, Martínez-Castillo A et al. Free Shiga toxin 1-encoding bacteriophages are less prevalent than Shiga toxin 2 phages in extraintestinal environments. Environ Microbiol 2015;17:4790-801.
23. Grotiuz G, Sirok A, Gadea P et al. Shiga toxin 2-producing Acinetobacter haemolyticus associated with a case of bloody diarrhea. J Clin Microbiol 2006;44:3838-41.
24. Gyles C, Boerlin P. Horizontally transferred genetic elements and their role in pathogenesis of bacterial disease. Vet Pathol 2013;51(2):328-340.
25. He X, Kong Q, Patfield S et al. A New Immunoassay for detecting all subtypes of Shiga toxins produced by Shiga toxinproducing E. coli in ground beef. PLoS One 2016;11:e0148092.
26. Holguín AV, Rangel G, Clavijo V et al. Phage ΦPan70, a putative temperate phage, controls Pseudomonas aeruginosa in planktonic, biofilm and burn mouse model assays. Viruses 2015;7:4602-23.
27. Imamovic L, Muniesa M. Characterizing RecA-independent induction of Shiga toxin 2-encoding phages by EDTA treatment. PLoS One 2012;7:e32393.
28. Kawano K, Okada M, Haga T et al. Relationship between pathogenicity for humans and stx genotype in Shiga toxinproducing Escherichia coli serotype O157. Eur J Clin Microbiol 2008;27:227-32.
29. Kelly BG, Vespermann A, Bolton DJ. Horizontal gene transfer of virulence determinants in selected bacterial foodborne pathogens. Food Chem Toxicol 2009;47:969-77.
30. Koitabashi T, Vuddhakul V, Radu S et al. Genetic characterization of Escherichia coli O157: H7- strains carrying the stx2 gene but not producing Shiga toxin 2. Microbiol Immunol 2006; 50:135-48.
31. Krylov VN. Role of horizontal gene transfer by bacteriophages in the origin of pathogenic bacteria. Genetika 2003;39:595-620.
32. Krzymińska S, Mokracka J, Koczura R et al. Cytotoxic activity of Enterobacter cloacae human isolates. FEMS Immunol Med Micr 2009;56:248-52.
33. Kyle JL, Cummings CA, Parker CT et al. Escherichia coli serotype O55: H7 diversity supports parallel acquisition of bacteriophage at Shiga toxin phage insertion sites during evolution of the O157: H7 lineage. J Bacteriol 2012;194:1885-96.
34. Lima SM, Peabody DS, Silva JL et al. Mutations in the hydrophobic core and in the protein-RNA interface affect the packing and stability of icosahedral viruses. Eur J Biochem 2004;271:135-45.
35. Łoś JM, Łoś M, Wegrzyn G. Bacteriophages carrying Shiga toxin genes: genomic variations, detection and potential treatment of pathogenic bacteria. Future Microbiol 2011;6:909-24.
36. Lunder M, Bratkovic T, Urleb U et al. Ultrasound in phage display: a new approach to nonspecific elution. Biotechniques 2008;44:893-900.
37. Maaß A, Heiseler T, Maaß F et al. A general strategy for antibody library screening via conversion of transient target binding into permanent reporter deposition. Protein Eng Des Sel 2014;27:41-47.
38. McAllister LJ, Bent SJ, Petty NK et al. Genomic comparison of Two O111:H- enterohemorrhagic Escherichia coli isolates from a historic hemolytic-uremic syndrome Outbreak in Australia. Infect Immun 2016;84 :775-81.
39. McDonald JE, Smith DL, Fogg PC et al. High-throughput method for rapid induction of prophages from lysogens and its application in the study of Shiga toxin-encoding Escherichia coli strains. Appl Environ Microb 2010;76:2360-5.
40. McDonough MA, Butterton JR. Spontaneous tandem amplification and deletion of the Shiga toxin operon in Shigella dysenteriae 1. Mol Microbiol 1999;34:1058-69.
41. Mauro SA, Koudelka GB. Shiga toxin: expression, distribution, and its role in the environment. Toxins 2011;3:608-25.
42. Mezzatesta ML, Gona F, Stefani S. Enterobacter cloacae complex: clinical impact and emerging antibiotic resistance. Future Microbiol 2012;7:887-902.
43. Muniesa M, Blanco JE, de Simón M et al. Diversity of stx2 converting bacteriophages induced from Shiga toxinproducing Escherichia coli strains isolated from cattle. Microbiol 2004;150:2959-71.
44. Muniesa M, De Simon M, Prats G et al. Shiga toxin 2-converting bacteriophages associated with clonal variability in Escherichia coli O157:H7 strains of human origin isolated from a single outbreak. Infect Immun 2003;71:4554-62.
45. Muniesa M, Serra-Moreno R, Jofre J. Free Shiga toxin bacteriophages isolated from sewage showed diversity although the stx genes appeared conserved. Environ Microbiol 2004; 6:716-25.
46. Neely MN, Friedman DT. Arrangement and functional identification of genes in the regulatory region of lambdoid phage H-19B, a carrier of a Shiga-like toxin. Gene 1998;223:105-13.
47. Ohnishi M, Terajima J, Kurokawa K et al. Genomic diversity of enterohemorrhagic Escherichia coli O157 revealed by whole genome PCR scanning. P Natl Acad Sci USA 2002;99:17043-8.
48. Ooka T, Seto K, Kawano K et al. Clinical significance of Escherichia albertii. Emerg Infect Dis 2012;18:488-92.
49. Orth D, Grif K, Khan AB et al. The Shiga toxin genotype rather than the amount of Shiga toxin or the cytotoxicity of Shiga toxin in vitro correlates with the appearance of the hemolytic uremic syndrome. Diagn Micr Infec Dis 2007;59:235-42.
50. Pacheco AR, Sperandio V. Shiga toxin in enterohemorrhagic E. coli: regulation and novel anti-virulence strategies. Front Cell Infect Microbiol 2012;2:1-2.
51. Paul JH, Weinbauer M. Detection of lysogeny in marine environments. In:Wilhelm SW,Weinbauer MG, Suttle CA (eds). Manual Aquatic Viral Ecology. ASLO:Waco, TX, USA, 2010, pp 30-33.
52. Probert WS, McQuaid C, Schrader K. Isolation and identification of an Enterobacter cloacae strain producing a novel subtype of Shiga Toxin type 1. J Clin Microbiol 2014;52:2346-51.
53. Rakhuba DV, Kolomiets EI, Dey ES et al. Bacteriophage receptors, mechanisms of phage adsorption and penetration into host cell. Pol J Microbiol 2010;59:145-55.
54. Rooks DJ, Yan Y, McDonald JE et al. Development and validation of a qPCR-based method for quantifying Shiga toxinencoding and other lambdoid bacteriophages. Environ Microbiol 2010;12:1194-204.
55. Sambrook J, Russell DW. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press, 2001.
56. Saunders JR, Allison H, James CE et al. Phage-mediated transfer of virulence genes. J Chem Technol Biot 2001;76:662-6.
57. Schmidt H, Montag M, Bockemuhl J et al. Shiga-like toxin IIrelated cytotoxins in Citrobacter freundii strains from humans and beef samples. Infect Immun 1993;61:534-43.
58. Shaikh N, Tarr PI. Escherichia coli O157:H7 Shiga toxin encoding bacteriophages: integrations, excisions, truncations, and evolutionary implications. J Bacteriol 2003;185:3596-605.
59. Scheutz F, Teel LD, Beutin L et al. Multicenter evaluation of a sequence-based protocol for subtyping Shiga toxins and standardizing Stx nomenclature. J Clin Microbiol 2012; 1:2951-63.
60. Skinner C, Patfield S, Khalil R et al. New monoclonal antibodies against a novel subtype of Shiga toxin 1 produced by Enterobacter cloacae and their use in analysis of human serum. mSphere 2016;1:e00099-15.
61. Skinner C, Patfield S, Stanker L et al. Development ofmonoclonal antibodies and immunoassays for sensitive and specific detection of Shiga toxin Stx2f. PLoS One 2013;8:e76563.
62. Smith DL, Rooks DJ, Fogg PC et al. Comparative genomics of Shiga toxin encoding bacteriophages. BMC Genomics 2012;13:311.
63. Strauch E, Hammerl JA, Konietzny A et al. Bacteriophage 2851 is a prototype phage for dissemination of the Shiga toxin variant gene 2c in Escherichia coli O157:H7. Infect Immun 2008;76: 5466-77.
64. Strauch E, Lurz R, Beutin L. Characterization of a Shiga Toxinencoding temperate bacteriophage of Shigella sonnei. Infect Immun 2001;69:7588-95.
65. Strauch E, Schaudinn C, Beutin L. First-time isolation and characterization of a bacteriophage encoding the Shiga toxin 2c variant, which is globally spread in strains of Escherichia coli O157. Infect Immun 2004;72:7030-9.
66. Sváb D, Bálint, Maróti G et al. A novel transducible chimeric phage from Escherichia coli O157: H7 Sakai strain encoding Stx1 production. Infect Genet Evol 2015;29:42-47.
67. Tóth I, Schmidt H, Dow M et al. Transduction of porcine enteropathogenic Escherichia coli with a derivative of a Shiga toxin 2-encoding bacteriophage in a porcine ligated ileal loop system. Appl Environ Microb 2003;69:7242-7.
68. Toóth I, Svaób D, Baólint B et al. Comparative analysis of the Shiga toxin converting bacteriophage first detected in Shigella sonnei. Infect Genet Evol 2016;37:150-7.
69. Tozzoli R, Grande L, Michelacci V et al. Shiga toxin-converting phages and the emergence of new pathogenic Escherichia coli: a world in motion. Front Cell Infect Microbiol 2014;4:80.
70. Tyler JS, Mills MJ, Friedman DI. The operator an early promoter region of the Shiga toxin type 2-encoding bacteriophage 933W and control of toxin expression. J Bacteriol 2004;186:7670-9.
71. USDA, FSIS. Detection, isolation and identification of Escherichia coli O157:H7 from meat products. Microbiology Laboratory Guidebook (MLG) 5.06, 2012.
72. Velandia CVG, Krüger A, Parma YR et al. Differences in Shiga toxin and phage production among stx2g-positive STEC strains. Front Cell Infect Microbiol 2012;2:82.
73. Veses-Garcia M, Liu X, Rigden DJ et al. Transcriptomic analysis of Shiga-toxigenic bacteriophage carriage reveals a profound regulatory effect on acid resistance in Escherichia coli. Appl Environ Microb 2015;81:8118-25.
74. Vethanayagam JG, Flower AM. Decreased gene expression from T7 promoters may be due to impaired production of active T7 RNA polymerase. Microb Cell Fact 2005;4:3.
75. Wagner PL, Acheson DW, Waldor MK. Isogenic lysogens of diverse Shiga toxin 2-encoding bacteriophages produce markedly different amount of Shiga toxin. Infect Immun 1999;67:6710-4.
76. Wagner PL, Neely MN, Zhang X et al. Role for a phage promoter in Shiga Toxin 2 expression froma pathogenic Escherichia coli strain. J Bacteriol 2001;183:2081-5.
77. Wagner PL, Livny J, NeelyMNet al. Bacteriophage control of Shiga toxin 1 production and release by Escherichia coli. Mol Microbiol 2002;44:957-70.
78. Wagner PL, Waldor MK. Bacteriophage control of bacterial virulence. Infect Immun 2002;70:3985-93.
79. Wegrzyn G, Licznerska K,Wegrzyn A. Phage λ-new insights into regulatory circuits. Adv Virus Res 2012;82:155-78.
80. Wegrzyn G, Wegrzyn A. Genetic switches during bacteriophage lambda development. Prog Nucleic Acid Re 2005; 79:1-48.
81. Wick LM, QiW, Lacher DWet al. Evolution of genomic content in the stepwise emergence of Escherichia coli O157:H7. J Bacteriol 2005;187:1783-91.
82. Yang YA. Genetic diversity of Shiga toxin-producing prophages among Escherichia coli isolated from cattle in multiple herds. Doctoral Dissertation, Michigan State University, 2014.
83. Zhang W, Bielaszewska M, Kuczius T et al. Identification characterization and distribution of a Shiga toxin 1 gene variant (stx1c) in Escherichia coli strains isolated from humans. J Clin Microbiol 2002;40:1441-6.
84. Zhang X, McDaniel AD, Wolf LE et al. Quinolone antibiotics induce Shiga toxin-encoding bacteriophages, toxin production, and death in mice. J Infect Dis 2000;181:664-70.