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References

  1. Santos MM, Piccirillo C, Castro PM, Kalogerakis N, Pintado ME. 2012. Bioconversion of oleuropein to hydroxytyrosol by lactic acid bacteria. World J. Microbiol. Biotechnol. 28: 24352440.
    Pubmed CrossRef
  2. Foulquie Moreno MR, Sarantinopoulos P, Tsakalidou E, De Vuyst L. 2006. The role and application of enterococci in food and health. Int. J. Food Microbiol. 106: 1-24.
    Pubmed CrossRef
  3. Franz CM, van Belkum MJ, Holzapfel WH, Abriouel H, Galvez A. 2007. Diversity of enterococcal bacteriocins and their grouping in a new classification scheme. FEMS Microbiol. Rev. 31: 293-310.
    Pubmed CrossRef
  4. Adams MR. 1999. Safety of industrial lactic acid bacteria. J. Biotechnol. 68: 171-178.
    CrossRef
  5. Patel G, Snydman DR, Practice ASTIDCo. 2013. Vancomycinresistant Enterococcus infections in solid organ transplantation. Am. J. Transplant. 13 Suppl 4: 59-67.
    Pubmed CrossRef
  6. Hidron AI, Edwards JR, Patel J, Horan TC, Sievert DM, Pollock DA, et al. 2008. NHSN annual update: antimicrobialresistant pathogens associated with healthcare-associated infections: annual summary of data reported to the National Healthcare Safety Network at the Centers for Disease Control and Prevention, 2006-2007. Infect. Control Hosp. Epidemiol. 29: 996-1011.
    Pubmed CrossRef
  7. Perez-Pulido R, Abriouel H, Ben Omar N, Lucas R, Martinez-Canamero M, Galvez A. 2006. Safety and potential risks of enterococci isolated from traditional fermented capers. Food Chem. Toxicol. 44: 2070-2077.
    Pubmed CrossRef
  8. DiazGranados CA, Zimmer SM, Klein M, Jernigan JA. 2005. Comparison of mortality associated with vancomycinresistant and vancomycin-susceptible enterococcal bloodstream infections: a meta-analysis. Clin. Infect. Dis. 41: 327-333.
    Pubmed CrossRef
  9. Kara A, Devrim I, Bayram N, Katipoglu N, Kiran E, Oruc Y, et al. 2015. Risk of vancomycin-resistant enterococci bloodstream infection among patients colonized with vancomycin-resistant enterococci. Braz. J. Infect. Dis. 19: 58-61.
    Pubmed CrossRef
  10. Jeong DW, Kim HR, Jung G, Han S, Kim CT, Lee JH. 2014. Bacterial community migration in the ripening of doenjang, a traditional Korean fermented soybean food. J. Microbiol. Biotechnol. 24: 648-660.
    Pubmed CrossRef
  11. Nallapareddy SR, Wenxiang H, Weinstock GM, Murray BE. 2005. Molecular characterization of a widespread, pathogenic, and antibiotic resistance-receptive Enterococcus faecalis lineage and dissemination of its putative pathogenicity island. J. Bacteriol. 187: 5709-5718.
    Pubmed PMC CrossRef
  12. Kawalec M, Pietras Z, Danilowicz E, Jakubczak A, Gniadkowski M, Hryniewicz W, et al. 2007. Clonal structure of Enterococcus faecalis isolated from Polish hospitals:characterization of epidemic clones. J. Clin. Microbiol. 45:147-153.
    Pubmed PMC CrossRef
  13. Kuch A, Willems RJ, Werner G, Coque TM, Hammerum AM, Sundsfjord A, et al. 2012. Insight into antimicrobial susceptibility and population structure of contemporary human Enterococcus faecalis isolates from Europe. J. Antimicrob. Chemother. 67: 551-558.
    Pubmed CrossRef
  14. McBride SM, Fischetti VA, Leblanc DJ, Moellering RC Jr, Gilmore MS. 2007. Genetic diversity among Enterococcus faecalis. PLoS One 2: e582.
    Pubmed PMC CrossRef
  15. Freitas AR, Coque TM, Novais C, Hammerum AM, Lester CH, Zervos MJ, et al. 2011. Human and swine hosts share vancomycin-resistant Enterococcus faecium CC17 and CC5 and Enterococcus faecalis CC2 clonal clusters harboring Tn1546 on indistinguishable plasmids. J. Clin. Microbiol. 49:925-931.
    Pubmed PMC CrossRef
  16. Campanile F, Bartoloni A, Bartalesi F, Borbone S, Mangani V, Mantella A, et al. 2003. Molecular alterations of VanA element in vancomycin-resistant enterococci isolated during a survey of colonized patients in an Italian intensive care unit. Microb. Drug Resist. 9: 191-199.
    Pubmed CrossRef
  17. Ruiz-Garbajosa P, Bonten MJ, Robinson DA, Top J, Nallapareddy SR, Torres C, et al. 2006. Multilocus sequence typing scheme for Enterococcus faecalis reveals hospitaladapted genetic complexes in a background of high rates of recombination. J. Clin. Microbiol. 44: 2220-2228.
    Pubmed PMC CrossRef
  18. Kuhn I, Burman LG, Haeggman S, Tullus K, Murray BE. 1995. Biochemical fingerprinting compared with ribotyping and pulsed-field gel electrophoresis of DNA for epidemiological typing of enterococci. J. Clin. Microbiol. 33: 2812-2817.
    Pubmed PMC
  19. Feil EJ, Li BC, Aanensen DM, Hanage WP, Spratt BG. 2004. eBURST: inferring patterns of evolutionary descent among clusters of related bacterial genotypes from multilocus sequence typing data. J. Bacteriol. 186: 1518-1530.
    Pubmed PMC CrossRef
  20. Urwin R, Maiden MC. 2003. Multi-locus sequence typing: a tool for global epidemiology. Trends Microbiol. 11: 479-487.
    Pubmed CrossRef
  21. Chung YS, Kwon KH, Shin S, Kim JH, Park YH, Yoon JW. 2014. Characterization of veterinary hospital-associated isolates of Enterococcus species in Korea. J. Microbiol. Biotechnol. 24:386-393.
    Pubmed CrossRef
  22. Stecher G, Liu L, Sanderford M, Peterson D, Tamura K, Kumar S. 2014. MEGA-MD: molecular evolutionary genetics analysis software with mutational diagnosis of amino acid variation. Bioinformatics 30: 1305-1307.
    Pubmed PMC CrossRef
  23. Nei M, Gojobori T. 1986. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol. Biol. Evol. 3: 418-426.
    Pubmed
  24. Clinical and Laboratory Standards Institute. 2007. Performance standards for antimicrobial susceptibility testing; seventeenth informational supplement. CLSI domument M100-S17. CLSI, Wayne, PA. USA.
  25. Guerrero-Ramos E, Cordero J, Molina-Gonzalez D, Poeta P, Igrejas G, Alonso-Calleja C, et al. 2016. Antimicrobial resistance and virulence genes in enterococci from wild game meat in Spain. Food Microbiol. 53: 156-164.
    Pubmed CrossRef
  26. Maasjost J, Muhldorfer K, de Jackel SC, Hafez HM. 2015. Antimicrobial susceptibility patterns of Enterococcus faecalis and Enterococcus faecium isolated from poultry flocks in Germany. Avian Dis. 59: 143-148.
    Pubmed CrossRef
  27. Furlaneto-Maia L, Rocha KR, Siqueira VL, Furlaneto MC. 2014. Comparison between automated system and PCR-based method for identification and antimicrobial susceptibility profile of clinical Enterococcus spp. Rev. Instit. Med. Trop. Sao Paulo 56: 97-103.
    Pubmed PMC CrossRef
  28. Quinones D, Kobayashi N, Nagashima S. 2009. Molecular epidemiologic analysis of Enterococcus faecalis isolates in Cuba by multilocus sequence typing. Microb. Drug Resist. 15: 287293.
    Pubmed PMC CrossRef
  29. Poulsen LL, Bisgaard M, Son NT, Trung NV, An HM, Dalsgaard A. 2012. Enterococcus faecalis clones in poultry and in humans with urinary tract infections, Vietnam. Emerg. Infect. Dis. 18: 1096-1100.
    Pubmed PMC CrossRef
  30. Ruiz-Garbajosa P, Canton R, Pintado V, Coque TM, Willems R, Baquero F, et al. 2006. Genetic and phenotypic differences among Enterococcus faecalis clones from intestinal colonisation and invasive disease. Clin. Microbiol. Infect. 12: 1193-1198.
    Pubmed CrossRef
  31. Lopez M, Rezusta A, Seral C, Aspiroz C, Marne C, Aldea MJ, et al. 2012. Detection and characterization of a ST6 clone of vanB2-Enterococcus faecalis from three different hospitals in Spain. Eur. J. Clin. Microbiol. Infect. Dis. 31: 257-260.
    Pubmed CrossRef
  32. Leavis HL, Bonten MJ, Willems RJ. 2006. Identification of high-risk enterococcal clonal complexes: global dispersion and antibiotic resistance. Curr. Opin. Microbiol. 9: 454-460.
    Pubmed CrossRef
  33. Rathnayake IU, Hargreaves M, Huygens F. 2011. Genotyping of Enterococcus faecalis and Enterococcus faecium isolates by use of a set of eight single nucleotide polymorphisms. J. Clin. Microbiol. 49: 367-372.
    Pubmed PMC CrossRef
  34. Solheim M, Brekke MC, Snipen LG, Willems RJ, Nes IF, Brede DA. 2011. Comparative genomic analysis reveals significant enrichment of mobile genetic elements and genes encoding surface structure-proteins in hospital-associated clonal complex 2 Enterococcus faecalis. BMC Microbiol. 11: 3.
    Pubmed PMC CrossRef
  35. Jamet E, Akary E, Poisson MA, Chamba JF, Bertrand X, Serror P. 2012. Prevalence and characterization of antibiotic resistant Enterococcus faecalis in French cheeses. Food Microbiol. 31: 191-198.
    Pubmed CrossRef
  36. Arias CA, Murray BE. 2012. The rise of the Enterococcus:beyond vancomycin resistance. Nat. Rev. Microbiol. 10: 266-278.
    Pubmed PMC CrossRef

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Article

Research article

J. Microbiol. Biotechnol. 2017; 27(5): 916-924

Published online May 28, 2017 https://doi.org/10.4014/jmb.1612.12033

Copyright © The Korean Society for Microbiology and Biotechnology.

Genetic Diversity and Antibiotic Resistance of Enterococcus faecalis Isolates from Traditional Korean Fermented Soybean Foods

Jong-Hoon Lee 1, Donghun Shin 1, Bitnara Lee 1, Hyundong Lee 1, Inhyung Lee 2 and Do-Won Jeong 3*

1Department of Food Science and Biotechnology, Kyonggi University, Suwon 16227, Republic of Korea, 2Department of Bio and Fermentation Convergence Technology, Kookmin University, Seoul 02707, Republic of Korea, 3Department of Food and Nutrition, Dongduk Women’s University, Seoul 02748, Republic of Korea

Received: December 20, 2016; Accepted: February 24, 2017

Abstract

Eighty-five Enterococcus faecalis isolates collected from animals (40 isolates), meju (a Korean
fermented soybean product; 27 isolates), humans (10 isolates), and various environmental
samples (8 isolates) were subjected to multilocus sequence typing (MLST) to identify genetic
differences between samples of different origins. MLST analysis resulted in 44 sequence types
(STs), and the eBURST algorithm clustered the STs into 21 clonal complexes (CCs) and 17
singletons. The predominant STs, ST695 (21.1%, 18/85) and ST694 (9.4%, 8/85), were
singletons, and only contained isolates originating from meju. None of the STs in the current
study belonged to CC2 or CC9, which comprise clinical isolates with high levels of antibiotic
resistance. The E. faecalis isolates showed the highest rates of resistance to tetracycline (32.9%),
followed by erythromycin (9.4%) and vancomycin (2.4%). All isolates from meju were
sensitive to these three antibiotics. Hence, MLST uncovered genetic diversity within E. faecalis,
and clustering of the STs using eBURST revealed a correlation between the genotypes and
origins of the isolates.

Keywords: Enterococcus faecalis, multilocus sequence typing, meju, antibiotic resistance, diversity

References

  1. Santos MM, Piccirillo C, Castro PM, Kalogerakis N, Pintado ME. 2012. Bioconversion of oleuropein to hydroxytyrosol by lactic acid bacteria. World J. Microbiol. Biotechnol. 28: 24352440.
    Pubmed CrossRef
  2. Foulquie Moreno MR, Sarantinopoulos P, Tsakalidou E, De Vuyst L. 2006. The role and application of enterococci in food and health. Int. J. Food Microbiol. 106: 1-24.
    Pubmed CrossRef
  3. Franz CM, van Belkum MJ, Holzapfel WH, Abriouel H, Galvez A. 2007. Diversity of enterococcal bacteriocins and their grouping in a new classification scheme. FEMS Microbiol. Rev. 31: 293-310.
    Pubmed CrossRef
  4. Adams MR. 1999. Safety of industrial lactic acid bacteria. J. Biotechnol. 68: 171-178.
    CrossRef
  5. Patel G, Snydman DR, Practice ASTIDCo. 2013. Vancomycinresistant Enterococcus infections in solid organ transplantation. Am. J. Transplant. 13 Suppl 4: 59-67.
    Pubmed CrossRef
  6. Hidron AI, Edwards JR, Patel J, Horan TC, Sievert DM, Pollock DA, et al. 2008. NHSN annual update: antimicrobialresistant pathogens associated with healthcare-associated infections: annual summary of data reported to the National Healthcare Safety Network at the Centers for Disease Control and Prevention, 2006-2007. Infect. Control Hosp. Epidemiol. 29: 996-1011.
    Pubmed CrossRef
  7. Perez-Pulido R, Abriouel H, Ben Omar N, Lucas R, Martinez-Canamero M, Galvez A. 2006. Safety and potential risks of enterococci isolated from traditional fermented capers. Food Chem. Toxicol. 44: 2070-2077.
    Pubmed CrossRef
  8. DiazGranados CA, Zimmer SM, Klein M, Jernigan JA. 2005. Comparison of mortality associated with vancomycinresistant and vancomycin-susceptible enterococcal bloodstream infections: a meta-analysis. Clin. Infect. Dis. 41: 327-333.
    Pubmed CrossRef
  9. Kara A, Devrim I, Bayram N, Katipoglu N, Kiran E, Oruc Y, et al. 2015. Risk of vancomycin-resistant enterococci bloodstream infection among patients colonized with vancomycin-resistant enterococci. Braz. J. Infect. Dis. 19: 58-61.
    Pubmed CrossRef
  10. Jeong DW, Kim HR, Jung G, Han S, Kim CT, Lee JH. 2014. Bacterial community migration in the ripening of doenjang, a traditional Korean fermented soybean food. J. Microbiol. Biotechnol. 24: 648-660.
    Pubmed CrossRef
  11. Nallapareddy SR, Wenxiang H, Weinstock GM, Murray BE. 2005. Molecular characterization of a widespread, pathogenic, and antibiotic resistance-receptive Enterococcus faecalis lineage and dissemination of its putative pathogenicity island. J. Bacteriol. 187: 5709-5718.
    Pubmed KoreaMed CrossRef
  12. Kawalec M, Pietras Z, Danilowicz E, Jakubczak A, Gniadkowski M, Hryniewicz W, et al. 2007. Clonal structure of Enterococcus faecalis isolated from Polish hospitals:characterization of epidemic clones. J. Clin. Microbiol. 45:147-153.
    Pubmed KoreaMed CrossRef
  13. Kuch A, Willems RJ, Werner G, Coque TM, Hammerum AM, Sundsfjord A, et al. 2012. Insight into antimicrobial susceptibility and population structure of contemporary human Enterococcus faecalis isolates from Europe. J. Antimicrob. Chemother. 67: 551-558.
    Pubmed CrossRef
  14. McBride SM, Fischetti VA, Leblanc DJ, Moellering RC Jr, Gilmore MS. 2007. Genetic diversity among Enterococcus faecalis. PLoS One 2: e582.
    Pubmed KoreaMed CrossRef
  15. Freitas AR, Coque TM, Novais C, Hammerum AM, Lester CH, Zervos MJ, et al. 2011. Human and swine hosts share vancomycin-resistant Enterococcus faecium CC17 and CC5 and Enterococcus faecalis CC2 clonal clusters harboring Tn1546 on indistinguishable plasmids. J. Clin. Microbiol. 49:925-931.
    Pubmed KoreaMed CrossRef
  16. Campanile F, Bartoloni A, Bartalesi F, Borbone S, Mangani V, Mantella A, et al. 2003. Molecular alterations of VanA element in vancomycin-resistant enterococci isolated during a survey of colonized patients in an Italian intensive care unit. Microb. Drug Resist. 9: 191-199.
    Pubmed CrossRef
  17. Ruiz-Garbajosa P, Bonten MJ, Robinson DA, Top J, Nallapareddy SR, Torres C, et al. 2006. Multilocus sequence typing scheme for Enterococcus faecalis reveals hospitaladapted genetic complexes in a background of high rates of recombination. J. Clin. Microbiol. 44: 2220-2228.
    Pubmed KoreaMed CrossRef
  18. Kuhn I, Burman LG, Haeggman S, Tullus K, Murray BE. 1995. Biochemical fingerprinting compared with ribotyping and pulsed-field gel electrophoresis of DNA for epidemiological typing of enterococci. J. Clin. Microbiol. 33: 2812-2817.
    Pubmed KoreaMed
  19. Feil EJ, Li BC, Aanensen DM, Hanage WP, Spratt BG. 2004. eBURST: inferring patterns of evolutionary descent among clusters of related bacterial genotypes from multilocus sequence typing data. J. Bacteriol. 186: 1518-1530.
    Pubmed KoreaMed CrossRef
  20. Urwin R, Maiden MC. 2003. Multi-locus sequence typing: a tool for global epidemiology. Trends Microbiol. 11: 479-487.
    Pubmed CrossRef
  21. Chung YS, Kwon KH, Shin S, Kim JH, Park YH, Yoon JW. 2014. Characterization of veterinary hospital-associated isolates of Enterococcus species in Korea. J. Microbiol. Biotechnol. 24:386-393.
    Pubmed CrossRef
  22. Stecher G, Liu L, Sanderford M, Peterson D, Tamura K, Kumar S. 2014. MEGA-MD: molecular evolutionary genetics analysis software with mutational diagnosis of amino acid variation. Bioinformatics 30: 1305-1307.
    Pubmed KoreaMed CrossRef
  23. Nei M, Gojobori T. 1986. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol. Biol. Evol. 3: 418-426.
    Pubmed
  24. Clinical and Laboratory Standards Institute. 2007. Performance standards for antimicrobial susceptibility testing; seventeenth informational supplement. CLSI domument M100-S17. CLSI, Wayne, PA. USA.
  25. Guerrero-Ramos E, Cordero J, Molina-Gonzalez D, Poeta P, Igrejas G, Alonso-Calleja C, et al. 2016. Antimicrobial resistance and virulence genes in enterococci from wild game meat in Spain. Food Microbiol. 53: 156-164.
    Pubmed CrossRef
  26. Maasjost J, Muhldorfer K, de Jackel SC, Hafez HM. 2015. Antimicrobial susceptibility patterns of Enterococcus faecalis and Enterococcus faecium isolated from poultry flocks in Germany. Avian Dis. 59: 143-148.
    Pubmed CrossRef
  27. Furlaneto-Maia L, Rocha KR, Siqueira VL, Furlaneto MC. 2014. Comparison between automated system and PCR-based method for identification and antimicrobial susceptibility profile of clinical Enterococcus spp. Rev. Instit. Med. Trop. Sao Paulo 56: 97-103.
    Pubmed KoreaMed CrossRef
  28. Quinones D, Kobayashi N, Nagashima S. 2009. Molecular epidemiologic analysis of Enterococcus faecalis isolates in Cuba by multilocus sequence typing. Microb. Drug Resist. 15: 287293.
    Pubmed KoreaMed CrossRef
  29. Poulsen LL, Bisgaard M, Son NT, Trung NV, An HM, Dalsgaard A. 2012. Enterococcus faecalis clones in poultry and in humans with urinary tract infections, Vietnam. Emerg. Infect. Dis. 18: 1096-1100.
    Pubmed KoreaMed CrossRef
  30. Ruiz-Garbajosa P, Canton R, Pintado V, Coque TM, Willems R, Baquero F, et al. 2006. Genetic and phenotypic differences among Enterococcus faecalis clones from intestinal colonisation and invasive disease. Clin. Microbiol. Infect. 12: 1193-1198.
    Pubmed CrossRef
  31. Lopez M, Rezusta A, Seral C, Aspiroz C, Marne C, Aldea MJ, et al. 2012. Detection and characterization of a ST6 clone of vanB2-Enterococcus faecalis from three different hospitals in Spain. Eur. J. Clin. Microbiol. Infect. Dis. 31: 257-260.
    Pubmed CrossRef
  32. Leavis HL, Bonten MJ, Willems RJ. 2006. Identification of high-risk enterococcal clonal complexes: global dispersion and antibiotic resistance. Curr. Opin. Microbiol. 9: 454-460.
    Pubmed CrossRef
  33. Rathnayake IU, Hargreaves M, Huygens F. 2011. Genotyping of Enterococcus faecalis and Enterococcus faecium isolates by use of a set of eight single nucleotide polymorphisms. J. Clin. Microbiol. 49: 367-372.
    Pubmed KoreaMed CrossRef
  34. Solheim M, Brekke MC, Snipen LG, Willems RJ, Nes IF, Brede DA. 2011. Comparative genomic analysis reveals significant enrichment of mobile genetic elements and genes encoding surface structure-proteins in hospital-associated clonal complex 2 Enterococcus faecalis. BMC Microbiol. 11: 3.
    Pubmed KoreaMed CrossRef
  35. Jamet E, Akary E, Poisson MA, Chamba JF, Bertrand X, Serror P. 2012. Prevalence and characterization of antibiotic resistant Enterococcus faecalis in French cheeses. Food Microbiol. 31: 191-198.
    Pubmed CrossRef
  36. Arias CA, Murray BE. 2012. The rise of the Enterococcus:beyond vancomycin resistance. Nat. Rev. Microbiol. 10: 266-278.
    Pubmed KoreaMed CrossRef