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Research article

Molecular and Cellular Microbiology (MCM)  |  Clinical Microbiology and Biomedical Sciences

Molecular Characterization of Salmonella Genomic Island 1 in Proteus mirabilis Isolates from Chungcheong Province, Korea

Ji Youn Sung 1, Semi Kim 2, GyeCheol Kwon 2 and Sun Hoe Koo 2*

1Department of Biomedical Laboratory Science, Far East University, Eumseong 27601, Republic of Korea, 2Department of Laboratory Medicine, College of Medicine, Chungnam National University, Daejeon 35015, Republic of Korea

Received: August 18, 2017; Accepted: September 16, 2017

J. Microbiol. Biotechnol. 2017; 27(11): 2052-2059

Published November 28, 2017 https://doi.org/10.4014/jmb.1708.08040

Copyright © The Korean Society for Microbiology and Biotechnology.

Abstract

The emergence and dissemination of Salmonella genomic island 1 (SGI1) are strongly associated with the occurrence of multidrug-resistant (MDR) enterobacteria in humans and animals. Diverse SGI1s have been reported among Salmonella enterica and Proteus mirabilis in several countries. We aimed to characterize SGI1 in P. mirabilis isolates from humans and chickens in Chungcheong Province, Korea. A total of 44 P. mirabilis isolates were recovered from humans (n = 20) and chickens (n = 24). Antimicrobial susceptibility was determined by disk diffusion assay. To detect and characterize SGI1s, PCR amplification and PCR mapping experiments were performed. Repetitive extragenic palindromic-PCR (REP-PCR) was performed to assess the clonality of the isolates. The four P. mirabilis strains (16.7%) from chicken harbored a SGI1, whereas none of the isolates from clinical specimens contained SGI1. The SGI1s detected in our study were all confirmed as SGI1-PmABB harboring aminoglycoside-resistant genes (aacCA5 and aadA7). In P. mirabilis isolates, the presence of SGI1-PmABB was significantly correlated with high resistance rates of the isolates to antimicrobial agents, such as gentamicin, streptomycin, and spectinomycin. Moreover, the four SGI1-bearing isolates showed the same REP-PCR patterns and that suggested both horizontal and clonal spread of the isolates. This study is the first attempt to determine SGI1s in P. mirabilis isolates in Korea. We confirmed that P. mirabilis isolates carrying SGI1-PmABB were distributed at poultry farms in Korea. The present study emphasizes the need for continuous monitoring of SGI1s to prevent spreading of the MDR genomic islands among P. mirabilis isolates from humans and animals.

Keywords

Salmonella genomic island 1, P. mirabilis, chicken, antimicrobial agents, resistance

References

  1. Boyd D, Peters GA, Cloeckaert A, Boumedine KS, ChaslusDancla E, Imberechts H, et al. 2001. Complete nucleotide sequence of a 43-kilobase genomic island associated with the multidrug resistance region of Salmonella enterica serovar Typhimurium DT104 and its identification in phage type DT120 and serovar Agona. J. Bacteriol. 183: 5725-5732.
    Pubmed PMC CrossRef
  2. Levings RS, Djordjevic SP, Hall RM. 2008. SGI2, a relative of Salmonella genomic island SGI1 with an independent origin. Antimicrob. Agents Chemother. 52: 2529-2537.
    Pubmed PMC CrossRef
  3. Doublet B, Praud K, Weill FX, Cloeckaert A. 2009. Association of IS26-composite transposons and complex In4-type integrons generates novel multidrug resistance loci in Salmonella genomic island 1. J. Antimicrob. Chemother. 63: 282-289.
    Pubmed CrossRef
  4. Le Hello S, Weill FX, Guibert V, Praud K, Cloeckaert A, Doublet B. 2012. Early strains of multidrug-resistant Salmonella enterica serovar Kentucky sequence type 198 from Southeast Asia harbor Salmonella genomic island 1-J variants with a novel insertion sequence. Antimicrob. Agents Chemother. 56: 5096-5102.
    Pubmed PMC CrossRef
  5. Doublet B, Praud K, Bertrand S, Collard JM, Weill FX, Cloeckaert A. 2008. Novel insertion sequence- and transposonmediated genetic rearrangements in genomic island SGI1 of Salmonella enterica serovar Kentucky. Antimicrob. Agents Chemother. 52: 3745-3754.
    Pubmed PMC CrossRef
  6. Doublet B, Chu C, Chiu CH, Fan YC, Cloeckaert A. 2009. Truncated tni module adjacent to the complex integron of Salmonella genomic island 1 in Salmonella enterica serovar Virchow. Antimicrob. Agents Chemother. 53: 824-827.
    Pubmed PMC CrossRef
  7. Chu C, Doublet B, Lee YL, Cloeckaert A, Chiou CS, Chen SW, et al. 2012. Salmonella genomic island 1-J variants associated with change in the antibiotic resistance gene cluster in multidrug-resistant Salmonella enterica serovar Virchow isolated from humans, Taiwan, 2004–2006. Clin. Microbiol. Infect. 18: 47-53.
    Pubmed CrossRef
  8. Douard G, Praud K, Cloeckaert A, Doublet B. 2010. The Salmonella genomic island 1 is specifically mobilized in trans by the IncA/C multidrug resistance plasmid family. PLoS One 5: e15302.
    Pubmed PMC CrossRef
  9. Wang JT, Chen PC, Chang SC, Shiau YR, Wang HY, Lai JF, et al. 2014. Antimicrobial susceptibilities of Proteus mirabilis: a longitudinal nationwide study from the Taiwan surveillance of antimicrobial resistance (TSAR) program. BMC Infect. Dis.14: 486.
    Pubmed PMC CrossRef
  10. Doublet B, Poirel L, Praud K, Nordmann P, Cloeckaert A. 2010. European clinical isolate of Proteus mirabilis harboring the Salmonella genomic island 1 variant SGI1-O. J. Antimicrob. Chemother. 65: 2260-2262. 11 . Bi S, Yan H, Chen M, Zhang Z, Shi L , Wang H. 201 1. New variant Salmonella genomic island 1-U in Proteus mirabilis clinical and food isolates from South China. J. Antimicrob. Chemother. 66: 1178-1179.
  11. Siebor E, Neuwirth C. 2011. The new variant of Salmonella genomic island 1 (SGI1-V) from a Proteus mirabilis French clinical isolate harbors blaVEB-6 and qnrA1 in the multiple antibiotic resistance region. J. Antimicrob. Chemother. 66: 2513-2520.
    Pubmed CrossRef
  12. Siebor E, Neuwirth C. 2013. Emergence of Salmonella genomic island 1 (SGI1) among Proteus mirabilis clinical isolates in Dijon, France. J. Antimicrob. Chemother. 68: 1750-1756.
    Pubmed CrossRef
  13. Schultz E, Haenni M, Mereghetti L, Siebor E, Neuwirth C, Madec JY, et al. 2015. Survey of multidrug resistance integrative mobilizable elements SGI1 and PGI1 in Proteus mirabilis in humans and dogs in France, 2010-13. J. Antimicrob. Chemother. 70: 2543-2546.
    Pubmed CrossRef
  14. Soliman AM, Ahmed AM, Shimamoto T, El-Domany RA, Nariya H, Shimamoto T. 2017. First report in Africa of two clinical isolates of Proteus mirabilis carrying Salmonella genomic island (SGI1) variants, SGI1-PmABB and SGI1-W. Infect. Genet. Evol. 51: 132-137.
    Pubmed CrossRef
  15. Lei CW, Zhang AY, Liu BH, Wang HN, Yang LQ, Guan ZB, et al. 2015. Two novel Salmonella genomic island 1 variants in Proteus mirabilis isolates from swine farms in China. Antimicrob. Agents Chemother. 59: 4336-4338.
    Pubmed PMC CrossRef
  16. Clinical and Laboratory Standards Institute. 2014. Performance standards for antimicrobial susceptibility testing. Twenty fourth informational supplement, M100-S24. Clinical and Laboratory Standards Institute, Wayne, PA.
  17. Bou G, Cerveró G, Domínguez MA, Quereda C, MartínezBeltrán J. 2000. PCR-based DNA fingerprinting (REP-PCR, AP-PCR) and pulsed-field gel electrophoresis characterization of a nosocomial outbreak caused by imipenem- and meropenem-resistant Acinetobacter baumannii. Clin. Microbiol. Infect. 6: 635-643.
    Pubmed CrossRef
  18. Lei CW, Zhang AY, Liu BH, Wang HN, Guan ZB, Xu CW, et al. 2014. Molecular characteristics of Salmonella genomic island 1 in Proteus mirabilis isolates from poultry farms in China. Antimicrob. Agents Chemother. 58: 7570-7572.
    Pubmed PMC CrossRef
  19. Siebor E, de Curraize C, Amoureux L, Neuwirth C. 2016. Mobilization of the Salmonella genomic island SGI1 and the Proteus genomic island PGI1 by the A/C2 plasmid carrying blaTEM-24 harbored by various clinical species of Enterobacteriaceae. J. Antimicrob. Chemother. 71: 2167-2170.
    Pubmed CrossRef
  20. Qin S, Qi H, Zhang Q, Zhao D, Liu ZZ, Tian H, et al. 201 5. Emergence of extensively drug-resistant Proteus mirabilis harboring a conjugative NDM-1 plasmid and a novel Salmonella genomic island 1 variant, SGI1-Z. Antimicrob. Agents Chemother. 59: 6601-6604.
    Pubmed PMC CrossRef

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Article

Research article

J. Microbiol. Biotechnol. 2017; 27(11): 2052-2059

Published online November 28, 2017 https://doi.org/10.4014/jmb.1708.08040

Copyright © The Korean Society for Microbiology and Biotechnology.

Molecular Characterization of Salmonella Genomic Island 1 in Proteus mirabilis Isolates from Chungcheong Province, Korea

Ji Youn Sung 1, Semi Kim 2, GyeCheol Kwon 2 and Sun Hoe Koo 2*

1Department of Biomedical Laboratory Science, Far East University, Eumseong 27601, Republic of Korea, 2Department of Laboratory Medicine, College of Medicine, Chungnam National University, Daejeon 35015, Republic of Korea

Received: August 18, 2017; Accepted: September 16, 2017

Abstract

The emergence and dissemination of Salmonella genomic island 1 (SGI1) are strongly
associated with the occurrence of multidrug-resistant (MDR) enterobacteria in humans and
animals. Diverse SGI1s have been reported among Salmonella enterica and Proteus mirabilis in
several countries. We aimed to characterize SGI1 in P. mirabilis isolates from humans and
chickens in Chungcheong Province, Korea. A total of 44 P. mirabilis isolates were recovered
from humans (n = 20) and chickens (n = 24). Antimicrobial susceptibility was determined by
disk diffusion assay. To detect and characterize SGI1s, PCR amplification and PCR mapping
experiments were performed. Repetitive extragenic palindromic-PCR (REP-PCR) was
performed to assess the clonality of the isolates. The four P. mirabilis strains (16.7%) from
chicken harbored a SGI1, whereas none of the isolates from clinical specimens contained SGI1.
The SGI1s detected in our study were all confirmed as SGI1-PmABB harboring
aminoglycoside-resistant genes (aacCA5 and aadA7). In P. mirabilis isolates, the presence of
SGI1-PmABB was significantly correlated with high resistance rates of the isolates to
antimicrobial agents, such as gentamicin, streptomycin, and spectinomycin. Moreover, the
four SGI1-bearing isolates showed the same REP-PCR patterns and that suggested both
horizontal and clonal spread of the isolates. This study is the first attempt to determine SGI1s
in P. mirabilis isolates in Korea. We confirmed that P. mirabilis isolates carrying SGI1-PmABB
were distributed at poultry farms in Korea. The present study emphasizes the need for
continuous monitoring of SGI1s to prevent spreading of the MDR genomic islands among
P. mirabilis isolates from humans and animals.

Keywords: Salmonella genomic island 1, P. mirabilis, chicken, antimicrobial agents, resistance

References

  1. Boyd D, Peters GA, Cloeckaert A, Boumedine KS, ChaslusDancla E, Imberechts H, et al. 2001. Complete nucleotide sequence of a 43-kilobase genomic island associated with the multidrug resistance region of Salmonella enterica serovar Typhimurium DT104 and its identification in phage type DT120 and serovar Agona. J. Bacteriol. 183: 5725-5732.
    Pubmed KoreaMed CrossRef
  2. Levings RS, Djordjevic SP, Hall RM. 2008. SGI2, a relative of Salmonella genomic island SGI1 with an independent origin. Antimicrob. Agents Chemother. 52: 2529-2537.
    Pubmed KoreaMed CrossRef
  3. Doublet B, Praud K, Weill FX, Cloeckaert A. 2009. Association of IS26-composite transposons and complex In4-type integrons generates novel multidrug resistance loci in Salmonella genomic island 1. J. Antimicrob. Chemother. 63: 282-289.
    Pubmed CrossRef
  4. Le Hello S, Weill FX, Guibert V, Praud K, Cloeckaert A, Doublet B. 2012. Early strains of multidrug-resistant Salmonella enterica serovar Kentucky sequence type 198 from Southeast Asia harbor Salmonella genomic island 1-J variants with a novel insertion sequence. Antimicrob. Agents Chemother. 56: 5096-5102.
    Pubmed KoreaMed CrossRef
  5. Doublet B, Praud K, Bertrand S, Collard JM, Weill FX, Cloeckaert A. 2008. Novel insertion sequence- and transposonmediated genetic rearrangements in genomic island SGI1 of Salmonella enterica serovar Kentucky. Antimicrob. Agents Chemother. 52: 3745-3754.
    Pubmed KoreaMed CrossRef
  6. Doublet B, Chu C, Chiu CH, Fan YC, Cloeckaert A. 2009. Truncated tni module adjacent to the complex integron of Salmonella genomic island 1 in Salmonella enterica serovar Virchow. Antimicrob. Agents Chemother. 53: 824-827.
    Pubmed KoreaMed CrossRef
  7. Chu C, Doublet B, Lee YL, Cloeckaert A, Chiou CS, Chen SW, et al. 2012. Salmonella genomic island 1-J variants associated with change in the antibiotic resistance gene cluster in multidrug-resistant Salmonella enterica serovar Virchow isolated from humans, Taiwan, 2004–2006. Clin. Microbiol. Infect. 18: 47-53.
    Pubmed CrossRef
  8. Douard G, Praud K, Cloeckaert A, Doublet B. 2010. The Salmonella genomic island 1 is specifically mobilized in trans by the IncA/C multidrug resistance plasmid family. PLoS One 5: e15302.
    Pubmed KoreaMed CrossRef
  9. Wang JT, Chen PC, Chang SC, Shiau YR, Wang HY, Lai JF, et al. 2014. Antimicrobial susceptibilities of Proteus mirabilis: a longitudinal nationwide study from the Taiwan surveillance of antimicrobial resistance (TSAR) program. BMC Infect. Dis.14: 486.
    Pubmed KoreaMed CrossRef
  10. Doublet B, Poirel L, Praud K, Nordmann P, Cloeckaert A. 2010. European clinical isolate of Proteus mirabilis harboring the Salmonella genomic island 1 variant SGI1-O. J. Antimicrob. Chemother. 65: 2260-2262. 11 . Bi S, Yan H, Chen M, Zhang Z, Shi L , Wang H. 201 1. New variant Salmonella genomic island 1-U in Proteus mirabilis clinical and food isolates from South China. J. Antimicrob. Chemother. 66: 1178-1179.
  11. Siebor E, Neuwirth C. 2011. The new variant of Salmonella genomic island 1 (SGI1-V) from a Proteus mirabilis French clinical isolate harbors blaVEB-6 and qnrA1 in the multiple antibiotic resistance region. J. Antimicrob. Chemother. 66: 2513-2520.
    Pubmed CrossRef
  12. Siebor E, Neuwirth C. 2013. Emergence of Salmonella genomic island 1 (SGI1) among Proteus mirabilis clinical isolates in Dijon, France. J. Antimicrob. Chemother. 68: 1750-1756.
    Pubmed CrossRef
  13. Schultz E, Haenni M, Mereghetti L, Siebor E, Neuwirth C, Madec JY, et al. 2015. Survey of multidrug resistance integrative mobilizable elements SGI1 and PGI1 in Proteus mirabilis in humans and dogs in France, 2010-13. J. Antimicrob. Chemother. 70: 2543-2546.
    Pubmed CrossRef
  14. Soliman AM, Ahmed AM, Shimamoto T, El-Domany RA, Nariya H, Shimamoto T. 2017. First report in Africa of two clinical isolates of Proteus mirabilis carrying Salmonella genomic island (SGI1) variants, SGI1-PmABB and SGI1-W. Infect. Genet. Evol. 51: 132-137.
    Pubmed CrossRef
  15. Lei CW, Zhang AY, Liu BH, Wang HN, Yang LQ, Guan ZB, et al. 2015. Two novel Salmonella genomic island 1 variants in Proteus mirabilis isolates from swine farms in China. Antimicrob. Agents Chemother. 59: 4336-4338.
    Pubmed KoreaMed CrossRef
  16. Clinical and Laboratory Standards Institute. 2014. Performance standards for antimicrobial susceptibility testing. Twenty fourth informational supplement, M100-S24. Clinical and Laboratory Standards Institute, Wayne, PA.
  17. Bou G, Cerveró G, Domínguez MA, Quereda C, MartínezBeltrán J. 2000. PCR-based DNA fingerprinting (REP-PCR, AP-PCR) and pulsed-field gel electrophoresis characterization of a nosocomial outbreak caused by imipenem- and meropenem-resistant Acinetobacter baumannii. Clin. Microbiol. Infect. 6: 635-643.
    Pubmed CrossRef
  18. Lei CW, Zhang AY, Liu BH, Wang HN, Guan ZB, Xu CW, et al. 2014. Molecular characteristics of Salmonella genomic island 1 in Proteus mirabilis isolates from poultry farms in China. Antimicrob. Agents Chemother. 58: 7570-7572.
    Pubmed KoreaMed CrossRef
  19. Siebor E, de Curraize C, Amoureux L, Neuwirth C. 2016. Mobilization of the Salmonella genomic island SGI1 and the Proteus genomic island PGI1 by the A/C2 plasmid carrying blaTEM-24 harbored by various clinical species of Enterobacteriaceae. J. Antimicrob. Chemother. 71: 2167-2170.
    Pubmed CrossRef
  20. Qin S, Qi H, Zhang Q, Zhao D, Liu ZZ, Tian H, et al. 201 5. Emergence of extensively drug-resistant Proteus mirabilis harboring a conjugative NDM-1 plasmid and a novel Salmonella genomic island 1 variant, SGI1-Z. Antimicrob. Agents Chemother. 59: 6601-6604.
    Pubmed KoreaMed CrossRef