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References

  1. Abdul-Raouf UM, Beuchat LR, Ammar MS. 1993. Survival and growth of Escherichia coli O 157:H7 i n g round, r oasted beef as affected by pH, acidulants, and temperature. Appl. Environ. Microbiol. 59: 2364-2368.
    Pubmed PMC
  2. Amisano G, Fornasero S, Migliaretti G, Caramello S, Tarasco V, Savino F. 2011. Diarrheagenic Escherichia coli in acute gastroenteritis in infants in North-West Italy. New Microbiol. 34: 45-51.
    Pubmed
  3. Bergan J, Dyve Lingelem AB, Simm R, Skotland T, Sandvig K. 2012. Shiga toxins. Toxicon 60: 1085-1107.
    Pubmed CrossRef
  4. Beutin L, Stroehe UH, Manning PA. 1993. Isolation of enterohemolysin (Ehly2)-associated sequences encoded on temperate phages of Escherichia coli. Gene 132: 95-99.
    CrossRef
  5. Boyd EF, Brüssow H. 2002. Common themes among bacteriophage-encoded virulence factors and diversity among the bacteriophages involved. Trends Microbiol. 10: 521-529.
    CrossRef
  6. Gerrish RS, Lee JE, Reed J, Williams J, Farrell LD, Spiegel KM, Shields MS. 2007. PCR versus hybridization for detecting virulence genes of enterohemorrhagic Escherichia coli. Emerg. Infect. Dis. 13: 1253-1258.
    Pubmed PMC CrossRef
  7. Gould LH, Mody RK, Ong KL, Clogher P, Cronquist AB, Garman KN, et al.; the Emerging Infections Program FoodNet Working Group. 2013. Increased recognition of non-O157 Shiga toxin–producing Escherichia coli infections in the United States during 2000–2010: epidemiologic features and comparison with E. coli O157 infections. Foodborne Pathog. Dis. 10: 453-460.
    Pubmed CrossRef
  8. Hedican EB, Medus C, Besser JM, Juni BA, Koziol B, Taylor C, Smith KE. 2009. Characteristics of O157 versus non-O157 Shiga toxin-producing Escherichia coli infections in Minnesota, 2000–2006. Clin. Infect. Dis. 49: 358-364.
    Pubmed CrossRef
  9. Huang A, Friesen J, Brunton JL. 1987. Characterization of a bacteriophage that carries the genes for production of Shigalike toxin 1 in Escherichia coli. J. Bacteriol. 169: 4308-4312.
    Pubmed PMC CrossRef
  10. Jamal M, Chaudhry WN, Hussain T, Das CR, Andleeb S. 2015. Characterization of new Myoviridae bacteriophage WZ1 against multi-drug resistant (MDR) Shigella dysenteriae. J. Basic Microbiol. 55: 420-431.
    Pubmed CrossRef
  11. Kim EJ. 2015. Characterization and infection receptor analysis of bacteriophages for Escherichia coli O157:H7 and non-O157 Shiga toxin-producing E. coli. Master’s dissertation, Gachon University, Sungnam, South Korea.
  12. Kim EJ, Lee H, Lee JH, Ryu S, Park JH. 2016. Morphological features and lipopolysaccharide attachment of coliphages specific to Escherichia coli O157:H7 and to a broad range of E. coli hosts. Appl. Biol. Chem. 59: 109-116.
    CrossRef
  13. Koodi L, Dhople AM. 2001. Acid tolerance of Escherichia coli O157:H7 and its survival in apple juice. Microbios 104: 167-175.
  14. Lacey RW. 1984. Mechanisms of resistance to beta-lactam antibiotics in Staphylococcus aureus. Scand. J. Infect. Dis. 42: 64-71.
  15. Law D. 2000. Virulence factors of Escherichia coli O157 and other Shiga toxin-producing E. coli. J. Appl. Microbiol. 88:729-745.
    Pubmed CrossRef
  16. Lee YD, Kim JY, Park JH. 2013. Characteristics of coliphage ECP4 and potential use as a sanitizing agent for biocontrol of Escherichia coli O157: H7. Food Control 34: 255-260.
    CrossRef
  17. Li S, L iu L , Zhu J, Z ou L , Li M , Cong Y, Hu F . 2010. Characterization and genome sequencing of a novel coliphage isolated from engineered Escherichia coli. Intervirology 53:211-220.
    Pubmed CrossRef
  18. Nataro JP, Kaper JB. 1998. Diarrheagenic Escherichia coli. Clin. Microbiol. Rev. 11: 142-201.
    Pubmed PMC
  19. O’Brien AD, Newland JW, Miller SF, Holmes RK, Smith HW, Forma, SB. 1984. Shiga-like toxin-converting phages from Escherichia coli strains that cause hemorrhagic colitis or infantile diarrhea. Science 226: 694-696.
    Pubmed CrossRef
  20. Park M, L ee JH, Shin H, Kim M, Choi J, K ang DH, Ryu S . 2012. Characterization and comparative genomic analysis of a novel bacteriophage, SFP10, simultaneously inhibiting both Salmonella enterica and Escherichia coli O157:H7. Appl. Environ. Microbiol. 78: 58-69.
    Pubmed PMC CrossRef
  21. Paton AW, Paton JC. 2002. Direct detection and characterization of Shiga toxigenic Escherichia coli by multiplex PCR for stx1, stx2, eae, ehxA, and saa. J. Clin. Microbiol. 40: 271-274.
    Pubmed PMC CrossRef
  22. Paton AW, Srimanote P, Woodrow MC, Paton JC. 2001. Characterization of Saa, a novel autoagglutinating adhesin produced by locus of enterocyte effacement-negative Shigatoxigenic Escherichia coli strains that are virulent for humans. Infect. Immun. 69: 6999-7009.
    Pubmed PMC CrossRef
  23. Rode TM, Axelsson L, Granum PE, Heir E, Holck A, Trine ML. 2011. High stability of Stx2 phage in food and under food-processing conditions. Appl. Environ. Microbiol. 77:5336-5341.
    Pubmed PMC CrossRef
  24. Sambrook J, Russell DW. 2001. Molecular Cloning: A Laboratory Manual, Vol. 999. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, USA.
  25. Sánchez S, García-Sánchez A, Martínez R, Blanco J, Blanco JE, Blanco M, Rey J. 2009. Detection and characterisation of Shiga toxin-producing Escherichia coli other than Escherichia coli O157: H7 in wild ruminants. Vet. J. 180: 384-388.
    Pubmed CrossRef
  26. Schmidt H, Beutin L, Karch H. 1995. Molecular analysis of the plasmid-encoded hemolysin of Escherichia coli O157:H7 strain EDL 933. Infect. Immun. 63: 1055-1061.
    Pubmed PMC
  27. Skippington E, Ragan MA. 2011. Lateral genetic transfer and the construction of genetic exchange communities. FEMS Microbiol. Rev. 35: 707-735.
    Pubmed CrossRef
  28. Wagner PL, Waldor MK. 2002. Bacteriophage control of bacterial virulence. Infect. Immun. 70: 3985-3993.
    Pubmed PMC CrossRef

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Article

Note

J. Microbiol. Biotechnol. 2016; 26(12): 2060-2065

Published online December 28, 2016 https://doi.org/10.4014/jmb.1609.09039

Copyright © The Korean Society for Microbiology and Biotechnology.

Virulence Factors and Stability of Coliphages Specific to Escherichia coli O157:H7 and to Various E. coli Infection

Eun-Jin Kim 1, Hyun-Joo Chang 2, Soojin Kwak 2 and Jong-Hyun Park 1*

1Department of Food Science and Biotechnology, Gachon University, Sungnam 13120, Republic of Korea, 2Research Group of Food Safety, Korea Food Research Institute, Sungnam 13539, Republic of Korea

Received: September 22, 2016; Accepted: September 30, 2016

Abstract

Characteristics of E. coli O157:H7-specific infection bacteriophages (O157 coliphages) and
broad-host-range bacteriophages for other E. coli serotypes (broad-host coliphages) were
compared. The burst sizes of the two groups ranged from 40 to 176 PFU/infected cell.
Distributions of the virulence factors stx1, stx2, ehxA, and saa between the two groups were not
differentiated. Broad-host-range coliphages showed lower stability at 70oC, in relation to O157
coliphages. However, O157 coliphages showed high acid and ethanol tolerance by reduction
of only 22% and 11% phages, respectively, under pH 3 and 70% ethanol for 1 h exposure.
Therefore, these results revealed that the O157 coliphages might be more stable under harsh
environments, which might explain their effective infection of the acid-tolerant E. coli O157:H7.

Keywords: E.coli O157:H7, host spectrum, bacteriophage, virulence gene, stability

References

  1. Abdul-Raouf UM, Beuchat LR, Ammar MS. 1993. Survival and growth of Escherichia coli O 157:H7 i n g round, r oasted beef as affected by pH, acidulants, and temperature. Appl. Environ. Microbiol. 59: 2364-2368.
    Pubmed KoreaMed
  2. Amisano G, Fornasero S, Migliaretti G, Caramello S, Tarasco V, Savino F. 2011. Diarrheagenic Escherichia coli in acute gastroenteritis in infants in North-West Italy. New Microbiol. 34: 45-51.
    Pubmed
  3. Bergan J, Dyve Lingelem AB, Simm R, Skotland T, Sandvig K. 2012. Shiga toxins. Toxicon 60: 1085-1107.
    Pubmed CrossRef
  4. Beutin L, Stroehe UH, Manning PA. 1993. Isolation of enterohemolysin (Ehly2)-associated sequences encoded on temperate phages of Escherichia coli. Gene 132: 95-99.
    CrossRef
  5. Boyd EF, Brüssow H. 2002. Common themes among bacteriophage-encoded virulence factors and diversity among the bacteriophages involved. Trends Microbiol. 10: 521-529.
    CrossRef
  6. Gerrish RS, Lee JE, Reed J, Williams J, Farrell LD, Spiegel KM, Shields MS. 2007. PCR versus hybridization for detecting virulence genes of enterohemorrhagic Escherichia coli. Emerg. Infect. Dis. 13: 1253-1258.
    Pubmed KoreaMed CrossRef
  7. Gould LH, Mody RK, Ong KL, Clogher P, Cronquist AB, Garman KN, et al.; the Emerging Infections Program FoodNet Working Group. 2013. Increased recognition of non-O157 Shiga toxin–producing Escherichia coli infections in the United States during 2000–2010: epidemiologic features and comparison with E. coli O157 infections. Foodborne Pathog. Dis. 10: 453-460.
    Pubmed CrossRef
  8. Hedican EB, Medus C, Besser JM, Juni BA, Koziol B, Taylor C, Smith KE. 2009. Characteristics of O157 versus non-O157 Shiga toxin-producing Escherichia coli infections in Minnesota, 2000–2006. Clin. Infect. Dis. 49: 358-364.
    Pubmed CrossRef
  9. Huang A, Friesen J, Brunton JL. 1987. Characterization of a bacteriophage that carries the genes for production of Shigalike toxin 1 in Escherichia coli. J. Bacteriol. 169: 4308-4312.
    Pubmed KoreaMed CrossRef
  10. Jamal M, Chaudhry WN, Hussain T, Das CR, Andleeb S. 2015. Characterization of new Myoviridae bacteriophage WZ1 against multi-drug resistant (MDR) Shigella dysenteriae. J. Basic Microbiol. 55: 420-431.
    Pubmed CrossRef
  11. Kim EJ. 2015. Characterization and infection receptor analysis of bacteriophages for Escherichia coli O157:H7 and non-O157 Shiga toxin-producing E. coli. Master’s dissertation, Gachon University, Sungnam, South Korea.
  12. Kim EJ, Lee H, Lee JH, Ryu S, Park JH. 2016. Morphological features and lipopolysaccharide attachment of coliphages specific to Escherichia coli O157:H7 and to a broad range of E. coli hosts. Appl. Biol. Chem. 59: 109-116.
    CrossRef
  13. Koodi L, Dhople AM. 2001. Acid tolerance of Escherichia coli O157:H7 and its survival in apple juice. Microbios 104: 167-175.
  14. Lacey RW. 1984. Mechanisms of resistance to beta-lactam antibiotics in Staphylococcus aureus. Scand. J. Infect. Dis. 42: 64-71.
  15. Law D. 2000. Virulence factors of Escherichia coli O157 and other Shiga toxin-producing E. coli. J. Appl. Microbiol. 88:729-745.
    Pubmed CrossRef
  16. Lee YD, Kim JY, Park JH. 2013. Characteristics of coliphage ECP4 and potential use as a sanitizing agent for biocontrol of Escherichia coli O157: H7. Food Control 34: 255-260.
    CrossRef
  17. Li S, L iu L , Zhu J, Z ou L , Li M , Cong Y, Hu F . 2010. Characterization and genome sequencing of a novel coliphage isolated from engineered Escherichia coli. Intervirology 53:211-220.
    Pubmed CrossRef
  18. Nataro JP, Kaper JB. 1998. Diarrheagenic Escherichia coli. Clin. Microbiol. Rev. 11: 142-201.
    Pubmed KoreaMed
  19. O’Brien AD, Newland JW, Miller SF, Holmes RK, Smith HW, Forma, SB. 1984. Shiga-like toxin-converting phages from Escherichia coli strains that cause hemorrhagic colitis or infantile diarrhea. Science 226: 694-696.
    Pubmed CrossRef
  20. Park M, L ee JH, Shin H, Kim M, Choi J, K ang DH, Ryu S . 2012. Characterization and comparative genomic analysis of a novel bacteriophage, SFP10, simultaneously inhibiting both Salmonella enterica and Escherichia coli O157:H7. Appl. Environ. Microbiol. 78: 58-69.
    Pubmed KoreaMed CrossRef
  21. Paton AW, Paton JC. 2002. Direct detection and characterization of Shiga toxigenic Escherichia coli by multiplex PCR for stx1, stx2, eae, ehxA, and saa. J. Clin. Microbiol. 40: 271-274.
    Pubmed KoreaMed CrossRef
  22. Paton AW, Srimanote P, Woodrow MC, Paton JC. 2001. Characterization of Saa, a novel autoagglutinating adhesin produced by locus of enterocyte effacement-negative Shigatoxigenic Escherichia coli strains that are virulent for humans. Infect. Immun. 69: 6999-7009.
    Pubmed KoreaMed CrossRef
  23. Rode TM, Axelsson L, Granum PE, Heir E, Holck A, Trine ML. 2011. High stability of Stx2 phage in food and under food-processing conditions. Appl. Environ. Microbiol. 77:5336-5341.
    Pubmed KoreaMed CrossRef
  24. Sambrook J, Russell DW. 2001. Molecular Cloning: A Laboratory Manual, Vol. 999. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, USA.
  25. Sánchez S, García-Sánchez A, Martínez R, Blanco J, Blanco JE, Blanco M, Rey J. 2009. Detection and characterisation of Shiga toxin-producing Escherichia coli other than Escherichia coli O157: H7 in wild ruminants. Vet. J. 180: 384-388.
    Pubmed CrossRef
  26. Schmidt H, Beutin L, Karch H. 1995. Molecular analysis of the plasmid-encoded hemolysin of Escherichia coli O157:H7 strain EDL 933. Infect. Immun. 63: 1055-1061.
    Pubmed KoreaMed
  27. Skippington E, Ragan MA. 2011. Lateral genetic transfer and the construction of genetic exchange communities. FEMS Microbiol. Rev. 35: 707-735.
    Pubmed CrossRef
  28. Wagner PL, Waldor MK. 2002. Bacteriophage control of bacterial virulence. Infect. Immun. 70: 3985-3993.
    Pubmed KoreaMed CrossRef