Cited by 209Salmonella and Campylobacter epidemiologyAntibiotic Resistance in BacteriaBacterial Genetics and Biotechnology

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Characterization of Variant Salmonella Genomic Island 1 Multidrug Resistance Regions from Serovars Typhimurium DT104 and Agona

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Boyd, David, Cloeckaert, Axel, Chaslus-Dancla, Elisabeth, Mulvey, Michael R.·2002·Antimicrobial Agents and Chemotherapy

DOI 10.1128/aac.46.6.1714-1722.2002PMC PMC127246

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Abstract

Strains of multidrug-resistant Salmonella enterica serovar Typhimurium DT104 (DT104) and S. enterica serovar Agona (Agona) have been found to harbor Salmonella genomic island 1 (SGI1), a 43-kb genomic region that contains many of the drug resistance genes. Such strains are resistant to ampicillin (pse-1), chloramphenicol/florfenicol (floR), streptomycin/spectinomycin (aadA2), sulfonamides (sul1), and tetracycline [tet(G)] (commonly called the ACSSuT phenotype). All five resistance genes are found in a 13-kb multidrug resistance (MDR) region consisting of an unusual class I integron structure related to In4. We examined DT104 and Agona strains that exhibited other resistance phenotypes to determine if the resistance genes were associated with variant SGI1 MDR regions. All strains were found to harbor variant SGI1-like elements by using a combination of Southern hybridization, PCR mapping, and sequencing. Variant SGI1-like elements were found with MDR regions consisting of (i) an integron consisting of the SGI1 MDR region with the addition of a region containing a putative transposase gene (orf513) and dfrA10 located between duplicated qacE Δ 1/sulI genes (SGI1-A; ACSSuTTm); (ii) an integron with either an aadA2(SSu) or a pse-1(ASu) cassette (SGI1-C and SGI1-B, respectively); (iii) an integron consisting of the SGI1-C MDR region plus an orf513/dfrA10 region as in SGI1-A (SGI1-D; ASSuTm; ampicillin resistance due to a TEM β-lactamase); and (iv) an integron related to that in SGI1 but which contains a 10-kb inversion between two copies of IS 6100, one which is inserted in floR(SGI1-E; ASSuT). We hypothesize that the MDR of SGI1 is subject to recombinational events that lead to the various resistance phenotypes in the Salmonella strains in which it is found.

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Combinatorial genetic evolution of multiresistance
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SGI1-K, a Variant of the SGI1 Genomic Island Carrying a Mercury Resistance Region, in Salmonella enterica Serovar Kentucky
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“(3, 18) have gained an additional dfrA10 trimethoprim resis-”
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Plasmid-Mediated High-Level Gentamicin Resistance among Enteric Bacteria Isolated from Pet Turtles in Louisiana
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“aac(3)-IIa aacIIaF 900 GGG AAT TCA GAG GAG ATA TCG CGA TGC ATA CG X13543 ( ) aacIIaR CAT TGT CGA CGG CCT CTA ACC aac(3)-VIa aacVIaF 465 CGC TCA GGC GAT ATG GTG AT L22613 ( ) aacVIaR CAT AAT GGA GCG CGG TGA CT armA metF 777 CAA ATG GAT AAG AAT GAT GAT GAT AY220558 (18) metR TTA TTT CTG AAA TCC ACT rmtA RMTA-F 634 CTA G…”
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Molecular Characterization of Multidrug-Resistant Strains of Salmonella enterica Serotype Typhimurium and Monophasic Variant ( S. 4,[5],12:i:–) Isolated from Human Infections in Italy
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Antibiotic resistance, integrons and Salmonella genomic island 1 among non-typhoidal Salmonella serovars in The Netherlands
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SGI2, a Relative ofSalmonellaGenomic Island SGI1 with an Independent Origin
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“a Primer pairs linking thdF-int (U7-L12/LJ-R1), S044-yidY (104-RJ/104-D), S026-intI1 (S026-FW/int-RV), and IS6100-S044 (DB-T1/MDR-B) and their product sizes have been reported elsewhere (3, 9, 22).”
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Association of IS26-composite transposons and complex In4-type integrons generates novel multidrug resistance loci in Salmonella genomic island 1
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Global dissemination patterns of common gene cassette arrays in class 1 integrons
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Identifying antimicrobial resistance genes of human clinical relevance within Salmonella isolated from food animals in Great Britain
Anjum, M. F., Choudhary, S., Morrison, V., Snow, L. C., Mafura, M. T., Slickers, P., Ehricht, R., & Woodward, M. J. (2011) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dkq498 · Cited by 66
Transmission of Salmonella between Swine Farms by the Housefly (Musca domestica)
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Characterization of multiple-antimicrobial-resistant Salmonella enterica Subsp. enterica isolated from indigenous vegetables and poultry in Malaysia
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“The findings might be due to the fact that the S. Agona with class I integrons integrated into their chromosome are able to persist even in the absence of antimicrobial selection (Cloeckaert et al. 2000; Boyd et al. 2002) with no apparent fitness cost to the cell.”
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Potential associations between fecal shedding ofSalmonellain feedlot cattle treated for apparent respiratory disease and subsequent adverse health outcomes
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Salmonella genomic island 1 (SGI1) reshapes the mating apparatus of IncC conjugative plasmids to promote self-propagation
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Salmonella Genomic Island 1 Multidrug Resistance Gene Clusters in Salmonella enterica Serovar Agona Isolated in Belgium in 1992 to 2002
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Mechanisms and Spread of Bacterial Resistance to Antimicrobial Agents
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Emergence of Salmonella genomic island 1 (SGI1) among Proteus mirabilis clinical isolates in Dijon, France
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Detection of antibiotic resistance genes in different Salmonella serovars by oligonucleotide microarray analysis
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“In contrast, this study describes a microarray format for the detection of various antibiotic resistance genes in different multidrug resistant Salmonella strains (Boyd et al., 2002; Cloeckaert and Schwarz, 2001) using longer oligonucleotides (50- and 60mers) in combination with a direct genomic DNA labeling method.”
Self-citation
Salmonella Genomic Island 1 (SGI1), Variant SGI1-I, and New Variant SGI1-O in Proteus mirabilis Clinical and Food Isolates from China
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“The orf513 gene from common region 1 (CR1) found in some SGI1 variants was not detected (2).”
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The new variant of Salmonella genomic island 1 (SGI1-V) from a Proteus mirabilis French clinical isolate harbours blaVEB-6 and qnrA1 in the multiple antibiotic resistance region
Siébor, E., & Neuwirth, C. (2011) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dkr335 · Cited by 51
Antimicrobial susceptibility and molecular detection of chloramphenicol and florfenicol resistance among Escherichia coli isolates from diseased chickens
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“More recently, florfenicol resistance conferred by the floR genes, referred to in the published literature as pp-flo, cmlA-like, floSt, flo, or floR, has also been detected in the Salmonella enteria serovar Typhimurium definitive phage type (DT) 104 [2,3,8-10,20], Salmonella enterica serovar Agona [9,14], E.”
Background
Trends in Serotype Distribution and Antimicrobial Susceptibility in Salmonella enterica Isolates from Humans in Belgium, 2009 to 2013
Ceyssens, P., Mattheus, W., Vanhoof, R., & Bertrand, S. (2014) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.04203-14 · Cited by 48
“Kentucky isolate (11-4366) was pan-resistant against the entire panel of tested antibiotics.”
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Secondary Chromosomal Attachment Site and Tandem Integration of the Mobilizable Salmonella Genomic Island 1
Doublet, B., Golding, G. R., Mulvey, M. R., & Cloeckaert, A. (2008) · PLoS ONE · doi:10.1371/journal.pone.0002060 · Cited by 46
“Thus, SGI1 represents a non replicative element which needs to integrate in the chromosome to persist in the host strain [4,6,13].”
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Complete nucleotide sequences of 84.5- and 3.2-kb plasmids in the multi-antibiotic resistant Salmonella enterica serovar Typhimurium U302 strain G8430
Chen, C., Nace, G. W., Solow, B. T., & Fratamico, P. M. (2006) · Plasmid · doi:10.1016/j.plasmid.2006.05.005 · Cited by 47
Stability, Entrapment and Variant Formation of Salmonella Genomic Island 1
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“These variants showed similar transfer activity to that of wt SGI1 (Table 2) and supposedly they are identical to the previously described variants SGI1-B and SGI1-C [3], which were detected in several Salmonella serotypes such as Typhimurium DT104, Agona and Paratyphi B and were suggested to arise by a single crossov…”
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Poultry-Associated Salmonella enterica subsp. enterica Serovar 4,12:d:− Reveals High Clonality and a Distinct Pathogenicity Gene Repertoire
Huehn, S., Bunge, C., Junker, E., Helmuth, R., & Malorny, B. (2008) · Applied and Environmental Microbiology · doi:10.1128/aem.02187-08 · Cited by 45
“The recently described Salmonella genomic island 1 in various serovars (4) could be only found in serovar Typhimurium phage type DT104 strains.”
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Identification and Characterization of Class 1 Integron Resistance Gene Cassettes among Salmonella Strains Isolated from Imported Seafood
Khan, A. A., Ponce‐Rivas, E., Nawaz, M. S., Cheng, C.-M., Khan, J. A., & West, C. S. (2008) · Applied and Environmental Microbiology · doi:10.1128/aem.02054-08 · Cited by 45
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Multiple-Antibiotic Resistance in Salmonella enterica Serotype Paratyphi B Isolates Collected in France between 2000 and 2003 Is Due Mainly to Strains Harboring Salmonella Genomic Islands 1, 1-B, and 1-C
Weill, F., Fabre, L., Grandry, B., Grimont, P. A. D., & Casin, I. (2005) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.49.7.2793-2801.2005 · Cited by 45
“enterica serotype Typhimurium DT104 (3).”
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Characterization of 13 multi-drug resistant Salmonella serovars from different broiler chickens associated with those of human isolates
Chiu, L.-H., Chiu, C., Horn, Y.-M., Chiou, C., Lee, C.-Y., Yeh, C.-M., Yu, C.-Y., Wu, C., Chang, C., & Chu, C. (2010) · BMC Microbiology · doi:10.1186/1471-2180-10-86 · Cited by 44
New Integron-Associated Gene Cassette Encoding a 3- N -Aminoglycoside Acetyltransferase
Levings, R. S., Partridge, S. R., Lightfoot, D., Hall, R. M., & Djordjevic, S. P. (2005) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.49.3.1238-1241.2005 · Cited by 44
Molecular epidemiology of emergent multidrug-resistant Salmonella enterica serotype Typhimurium strains carrying the virulence resistance plasmid pUO-StVR2
Herrero-Fresno, A., Rodicio, M. R., González‐Hevia, M. A., & Mendoza, M. C. (2005) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dki400 · Cited by 44
Harmonization of the multiple-locus variable-number tandem repeat analysis method between Denmark and Norway for typing Salmonella Typhimurium isolates and closer examination of the VNTR loci
Lindstedt, B.-A., Torpdahl, M., Nielsen, E. M., Vardund, T., Aas, L., & Kapperud, G. (2006) · Journal of Applied Microbiology · doi:10.1111/j.1365-2672.2006.03134.x · Cited by 43
“…phage types DT104 and DT120, and also in several Salm. enterica serovars including Agona, Albany, Meleagridis, Newport, Cerro, Derby, Dusseldorf, Infantis, Kiambu, Emek and Paratyphi B (Boyd et al. 2002; Carattoli et al. 2002; Doublet et al. 2003, 2004a,b,c; Ebner et al. 2004; Levings et al. 2005).”
Background
Florfenicol Resistance Gene floR Is Part of a Novel Transposon
Doublet, B., Schwarz, Š., Kehrenberg, C., & Cloeckaert, A. (2005) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.49.5.2106-2108.2005 · Cited by 43
Self-citation
Characterization of a Salmonella enterica serovar Agona strain harbouring a class 1 integron containing novel OXA-type -lactamase (blaOXA-53) and 6'-N-aminoglycoside acetyltransferase genes [aac(6')-I30]
Mulvey, M. R. (2004) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dkh347 · Cited by 43
“Further, the resistance genes are clustered near one end of SGI1 and located in a complex class 1 integron.(3,4) Resistance to third-generation b-lactams in Salmonella has been reported worldwide and most often results from the production of plasmid-mediated Ambler class A or class C (AmpCtype) extended-spectrum b-lac…”
BackgroundSelf-citation
Genome Sequencing Reveals the Complex Polysaccharide-Degrading Ability of Novel Deep-Sea Bacterium Flammeovirga pacifica WPAGA1
Gao, B., Jin, M., Li, L., Qu, W., & Zeng, R. (2017) · Frontiers in Microbiology · doi:10.3389/fmicb.2017.00600 · Cited by 42
Acquisition of multidrug resistance transposon Tn6061 and IS6100-mediated large chromosomal inversions in Pseudomonas aeruginosa clinical isolates
Coyne, S., Courvalin, P. M., & Galimand, M. (2010) · Microbiology · doi:10.1099/mic.0.033639-0 · Cited by 41
“An IS6100mediated chromosomal inversion has been described in SGI1-E, a variant of SGI1 in which floR is disrupted by a duplicated IS6100 (Boyd et al., 2002).”
Background
Characterization of the highly variable region surrounding the blaCTX-M-9 gene in non-related Escherichia coli from Barcelona
García-Fernández, A., Navarro, F., Miró, E., Mirelis, B., Campoy, S., & Coll, P. (2005) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dki345 · Cited by 40
A novel family of integrases associated with prophages and genomic islands integrated within the tRNA-dihydrouridine synthase A (dusA) gene
Farrugia, D. N., Elbourne, L. D. H., Mabbutt, B. C., & Paulsen, I. T. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv337 · Cited by 37
“However, of the more than 80 characterized tRNA-modifying enzymes in Proteobacteria (74), only a few have been reported as being targeted by mobile elements, including the Enterobacterial tRNA modification GTPase (thdF/mnmE) by Salmonella genomic island 1 (SGI1) (60), the Polaromonas naphthalenivorans CJ2 MiaB-like tR…”
BackgroundInfluential
The complete nucleotide sequence of an IncP-2 megaplasmid unveils a mosaic architecture comprising a putative novel blaVIM-2-harbouring transposon in Pseudomonas aeruginosa
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Destabilization of IncA and IncC plasmids by SGI1 and SGI2 type Salmonella genomic islands
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Genomic comparison of diverse Salmonella serovars isolated from swine
Gupta, S. K., Sharma, P., McMillan, E. A., Jackson, C. R., Hiott, L. M., Woodley, T. A., Humayoun, S. B., Barrett, J. B., Frye, J. G., & McClelland, M. (2019) · PLoS ONE · doi:10.1371/journal.pone.0224518 · Cited by 37
In117, an Unusual In0-Like Class 1 Integron Containing CR1 and bla CTX-M-2 and Associated with a Tn 21 -Like Element
Valverde, A., Cantón, R., Galán, J. C., Nordmann, P., Baquero, F., & Coque, T. M. (2006) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.50.2.799-802.2006 · Cited by 36
Emergence of Multidrug-resistantSalmonellaParatyphi B dT+, Canada
Mulvey, M. R., Boyd, D. A., Cloeckaert, A., Ahmed, R., Ng, L.-K., & Laboratories, T. P. P. H. (2004) · Emerging infectious diseases · doi:10.3201/eid1007.030862 · Cited by 35
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Prevalence and Characterization of Multidrug-Resistant (Type ACSSuT) Salmonella enterica Serovar Typhimurium Strains in Isolates from Four Gosling Farms and a Hatchery Farm
Yu, C.-Y., Chou, S.-J., Yeh, C.-M., Chao, M.-R., Huang, K.-C., Chang, Y., Chiou, C., Weill, F., Chiu, C., Chu, C.-H., et al. (2007) · Journal of Clinical Microbiology · doi:10.1128/jcm.00709-07 · Cited by 35
“Since multidrug-resistant (type ACSSuT) phage type DT104 was discovered in 1984 (35), a 43-kb multidrug resistance DNA region responsible for the ACSSuT type has been found and named Salmonella genomic island 1 (SGI1), which is inserted between the thdF and yidY genes and contains two conserved-segment (CS) regions (7…”
Background
Prevalence and Characterization of Salmonella Isolated from Chicken Meat in Turkey
Sırıken, B., Türk, H., Yıldırım, T., Durupınar, B., & Erol, İ. (2015) · Journal of Food Science · doi:10.1111/1750-3841.12829 · Cited by 34
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“Regarding NTS, since the 1990 release of the MDR strain S. Typhimurium DT104, the number of strains exhibiting the MDR phenotype has grown in numerous nations (Boyd et al ., 2002).”
Background
Unmasking the ancestral activity of integron integrases reveals a smooth evolutionary transition during functional innovation
Escudero, J. A., Loot, C., Parissi, V., Nivina, A., Bouchier, C., & Mazel, D. (2016) · Nature Communications · doi:10.1038/ncomms10937 · Cited by 33
Multidrug-Resistant Salmonella enterica Isolated from Food Animal and Foodstuff May Also Be Less Susceptible to Heavy Metals
Figueiredo, R., Card, R. M., Nuñéz-García, J., Mendonça, N., Silva, G., & Anjum, M. F. (2018) · Foodborne Pathogens and Disease · doi:10.1089/fpd.2017.2418 · Cited by 33
“It showed that the isolates harbored AMR genes known to be present on mobile elements, such as plasmids and SGI1 (Boyd et al. , 2002; Hopkins et al. , 2007; Anjum et al. , 2011; Kirchner et al. , 2013; Szmolka et al. , 2012).”

Authors: Boyd, D., Cloeckaert, A., Chaslus-Dancla, E., & Mulvey, M. R.
Affiliations: Health Canada (CA)
Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement (FR)
ORCID: Boyd, David
Cloeckaert, Axel
Venue: Antimicrobial Agents and Chemotherapy
Publisher: American Society for Microbiology
Published: 2002-06
Volume: 46
Issue: 6
Pages: 1714-1722
ISSN: 0066-4804 (ISSN-L)
1098-6596
DOI: 10.1128/aac.46.6.1714-1722.2002
PMC: PMC127246
OpenAlex: W2123741711
Cited by: 209
References: 52
Citations by year: 2026: 5 · 2025: 1 · 2024: 4 · 2023: 2 · 2022: 3 · 2021: 5 · 2020: 4 · 2019: 9 · 2018: 5 · 2017: 5 · 2016: 6 · 2015: 6 · 2014: 5 · 2013: 7 · 2012: 5
FWCI: 26.02
Type: journal article
Language: en
Open access: green
europepmc.org
Licence: journals.asm.org/non-commercial-tdm-license (tdm)
Locations: Antimicrobial Agents and Chemotherapy (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Agricultural and Biological Sciences › Food Science › Salmonella and Campylobacter epidemiology
Health Sciences › Medicine › Microbiology (medical) › Antibiotic Resistance in Bacteria
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
Keywords: Salmonella genomic island 1, multidrug resistance, Salmonella Typhimurium DT104, Salmonella Agona, class 1 integron, aadA2, floR, qacEΔ1, transposase genes, gene rearrangement, antimicrobial resistance genes
MeSH terms: Amino Acid Sequence, Anti-Bacterial Agents, Culture Media, DNA, Bacterial, Drug Resistance, Microbial, Microbial Sensitivity Tests, Terminology as Topic, Phenotype, Salmonella Infections, Sequence Homology, Nucleic Acid, Genomic Library, Drug Resistance, Multiple, Salmonella enterica

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Characterization of Variant Salmonella Genomic Island 1 Multidrug Resistance Regions from Serovars Typhimurium DT104 and Agona

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