Whole-Genome Analysis of Salmonella enterica Serovar Typhimurium T000240 Reveals the Acquisition of a Genomic Island Involved in Multidrug Resistance via IS1 Derivatives on the Chromosome

ABSTRACT Salmonella enterica serovar Typhimurium is frequently associated with life-threatening systemic infections, and the recent global emergence of multidrug resistance in S. enterica isolates from agricultural and clinical settings has raised concerns. In this study, we determined the whole-genome sequence of fluoroquinolone-resistant S. enterica serovar Typhimurium T000240 strain (DT12) isolated from human gastroenteritis in 2000. Comparative genome analysis revealed that T000240 displays high sequence similarity to strain LT2, which was originally isolated in 1940, indicating that progeny of LT2 might be reemerging. T000240 possesses a unique 82-kb genomic island, designated as GI-DT12, which is composed of multidrug resistance determinants, including a Tn2670-like composite transposon (class 1 integron [intI1, blaoxa-30 , aadA1, qacEΔ1, and sul1], mercury resistance proteins, and chloramphenicol acetyltransferase), a Tn10-like tetracycline resistance protein (tetA), the aerobactin iron-acquisition siderophore system (lutA and lucABC), and an iron transporter (sitABCD). Since GI-DT12 is flanked by IS1 derivatives, IS1-mediated recombination likely played a role in the acquisition of this genomic island through horizontal gene transfer. The aminoglycoside-(3)-N-acetyltransferase (aac(3)) gene and a class 1 integron harboring the dfrA1 gene cassette responsible for gentamicin and trimethoprim resistance, respectively, were identified on plasmid pSTMDT12_L and appeared to have been acquired through homologous recombination with IS26. This study represents the first characterization of the unique genomic island GI-DT12 that appears to be associated with possible IS1-mediated recombination in S. enterica serovar Typhimurium. It is expected that future whole-genome studies will aid in the characterization of the horizontal gene transfer events for the emerging S. enterica serovar Typhimurium strains.

[1]  S. Djordjevic,et al.  RSF1010-like plasmids in Australian Salmonella enterica serovar Typhimurium and origin of their sul2-strA-strB antibiotic resistance gene cluster. , 2010, Microbial drug resistance.

[2]  L. Ng,et al.  Ceftiofur Resistance in Salmonella enterica Serovar Heidelberg from Chicken Meat and Humans, Canada , 2010, Emerging infectious diseases.

[3]  T. Johnson,et al.  Pathogenomics of the Virulence Plasmids of Escherichia coli , 2009, Microbiology and Molecular Biology Reviews.

[4]  T. Cebula,et al.  Antimicrobial Resistance-Conferring Plasmids with Similarity to Virulence Plasmids from Avian Pathogenic Escherichia coli Strains in Salmonella enterica Serovar Kentucky Isolates from Poultry , 2009, Applied and Environmental Microbiology.

[5]  Hui Guo,et al.  MapView: visualization of short reads alignment on a desktop computer , 2009, Bioinform..

[6]  H. Andrews-Polymenis,et al.  ‘Form variation’ of the O12 antigen is critical for persistence of Salmonella Typhimurium in the murine intestine , 2008, Molecular microbiology.

[7]  R. Durbin,et al.  Mapping Quality Scores Mapping Short Dna Sequencing Reads and Calling Variants Using P

, 2022 .

[8]  M. Mendoza,et al.  Characterization of pUO-StVR2, a Virulence-Resistance Plasmid Evolved from the pSLT Virulence Plasmid of Salmonella enterica Serovar Typhimurium , 2008, Antimicrobial Agents and Chemotherapy.

[9]  Matthew Berriman,et al.  Artemis and ACT: viewing, annotating and comparing sequences stored in a relational database , 2008, Bioinform..

[10]  M. Molyneux,et al.  Epidemics of invasive Salmonella enterica serovar enteritidis and S. enterica Serovar typhimurium infection associated with multidrug resistance among adults and children in Malawi. , 2008, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[11]  M. Mendoza,et al.  Salmonella enterica serotype Typhimurium carrying hybrid virulence-resistance plasmids (pUO-StVR): a new multidrug-resistant group endemic in Spain. , 2008, International journal of medical microbiology : IJMM.

[12]  Mark J. P. Chaisson,et al.  Short read fragment assembly of bacterial genomes. , 2008, Genome research.

[13]  J. Bardowski,et al.  Complete Nucleotide Sequence of the pCTX-M3 Plasmid and Its Involvement in Spread of the Extended-Spectrum β-Lactamase Gene blaCTX-M-3 , 2007, Antimicrobial Agents and Chemotherapy.

[14]  M. Marahiel,et al.  Siderophore-Based Iron Acquisition and Pathogen Control , 2007, Microbiology and Molecular Biology Reviews.

[15]  F. Aarestrup,et al.  International Spread of Multidrug-resistant Salmonella Schwarzengrund in Food Products , 2007, Emerging infectious diseases.

[16]  S. Nair,et al.  Multidrug-Resistant Salmonella enterica Serovar Paratyphi A Harbors IncHI1 Plasmids Similar to Those Found in Serovar Typhi , 2007, Journal of bacteriology.

[17]  J. Terajima,et al.  Characterization of Isolates of Salmonella enterica Serovar Typhimurium Displaying High-Level Fluoroquinolone Resistance in Japan , 2005, Journal of Clinical Microbiology.

[18]  A. Pühler,et al.  The 120 592 bp IncF plasmid pRSB107 isolated from a sewage-treatment plant encodes nine different antibiotic-resistance determinants, two iron-acquisition systems and other putative virulence-associated functions. , 2005, Microbiology.

[19]  Thomas Ludwig,et al.  RAxML-III: a fast program for maximum likelihood-based inference of large phylogenetic trees , 2005, Bioinform..

[20]  T. Chiller,et al.  Evidence of an association between use of anti-microbial agents in food animals and anti-microbial resistance among bacteria isolated from humans and the human health consequences of such resistance. , 2004, Journal of veterinary medicine. B, Infectious diseases and veterinary public health.

[21]  S. Makino,et al.  Molecular Characterization of a Prophage of Salmonella enterica Serotype Typhimurium DT104 , 2004, Journal of Clinical Microbiology.

[22]  E. Baron,et al.  Characterization of Salmonella enterica Serotype Newport Isolated from Humans and Food Animals , 2003, Journal of Clinical Microbiology.

[23]  P. Nordmann,et al.  Decreased Susceptibility to Cefepime in a Clinical Strain of Escherichia coli Related to Plasmid- and Integron-Encoded OXA-30 β-Lactamase , 2003, Antimicrobial Agents and Chemotherapy.

[24]  Jiann-Hwa Chen,et al.  The IS1 elements in Shigella boydii: horizontal transfer, vertical inactivation and target duplication. , 2003, FEMS microbiology letters.

[25]  S. Payne,et al.  Contribution of the Shigella flexneri Sit, Iuc, and Feo Iron Acquisition Systems to Iron Acquisition In Vitro and in Cultured Cells , 2003, Infection and Immunity.

[26]  K. Raymond,et al.  Enterobactin: An archetype for microbial iron transport , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[27]  H. Izumiya,et al.  Life-Threatening Infantile Diarrhea from Fluoroquinolone-Resistant Salmonella enteric Typhimurium with Mutations in Both gyrA and parC , 2003, Emerging infectious diseases.

[28]  Shuping Zhang,et al.  Molecular Pathogenesis of Salmonella enterica Serotype Typhimurium-Induced Diarrhea , 2003, Infection and Immunity.

[29]  P. Fedorka-Cray,et al.  Antimicrobial use and resistance in animals. , 2002, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[30]  W. Rabsch,et al.  Salmonella enterica Serotype Typhimurium and Its Host-Adapted Variants , 2002, Infection and Immunity.

[31]  R. Wilson,et al.  Complete genome sequence of Salmonella enterica serovar Typhimurium LT2 , 2001, Nature.

[32]  M. Borodovsky,et al.  GeneMarkS: a self-training method for prediction of gene starts in microbial genomes. Implications for finding sequence motifs in regulatory regions. , 2001, Nucleic acids research.

[33]  K. Yuen,et al.  β-Lactamases in Shigella flexneriIsolates from Hong Kong and Shanghai and a Novel OXA-1-Like β-Lactamase, OXA-30 , 2000, Antimicrobial Agents and Chemotherapy.

[34]  E. Myers,et al.  Basic local alignment search tool. , 1990, Journal of molecular biology.

[35]  D. Warrell,et al.  Life-threatening bacteraemia in HIV-1 seropositive adults admitted to hospital in Nairobi, Kenya , 1990, The Lancet.

[36]  E. Scherzinger,et al.  Complete nucleotide sequence and gene organization of the broad-host-range plasmid RSF1010. , 1989, Gene.

[37]  V. Lorenzo,et al.  IS1-mediated mobility of the aerobactin system of pColV-K30 in Escherichia coli , 1988, Molecular and General Genetics MGG.

[38]  V. de Lorenzo,et al.  Characterization of iucA and iucC genes of the aerobactin system of plasmid ColV-K30 in Escherichia coli , 1986, Journal of bacteriology.

[39]  E. S. Anderson,et al.  Bacteriophage-typing designations of Salmonella typhimurium , 1977, Journal of Hygiene.

[40]  S. Falkow,et al.  Molecular Nature of Two Nonconjugative Plasmids Carrying Drug Resistance Genes , 1974, Journal of bacteriology.

[41]  H. Saedler,et al.  Multiple copies of the insertion-DNA sequences IS1 and IS2 in the chromosome of E. coli K-12 , 1973, Molecular and General Genetics MGG.

[42]  P. Fratamico,et al.  Complete nucleotide sequences of 84.5- and 3.2-kb plasmids in the multi-antibiotic resistant Salmonella enterica serovar Typhimurium U302 strain G8430. , 2007, Plasmid.

[43]  A. Kropinski,et al.  Sequence of the Genome of Salmonella Bacteriophage P22 , 2000 .

[44]  Daniel H. Huson,et al.  BIOINFORMATICS ORIGINAL PAPER doi:10.1093/bioinformatics/btm153 Genome analysis OSLay: optimal syntenic layout of unfinished assemblies , 2022 .