CoChat
Sign Up
Cited by 725Salmonella and Campylobacter epidemiologyAntibiotic Resistance in BacteriaBacterial Genetics and Biotechnology

Detection of mobile genetic elements associated with antibiotic resistance in Salmonella enterica using a newly developed web tool: MobileElementFinder

Open access
Johansson, Markus H K, Bortolaia, Valeria, Tansirichaiya, Supathep, Aarestrup, Frank M, Roberts, Adam P, Petersen, Thomas N·2021·Journal of Antimicrobial Chemotherapy
DOI 10.1093/jac/dkaa390PMC PMC7729385
Open this paper in CoChat — free accountOpen PDF

Abstract

Objectives: Antimicrobial resistance (AMR) in clinically relevant bacteria is a growing threat to public health globally. In these bacteria, antimicrobial resistance genes are often associated with mobile genetic elements (MGEs), which promote their mobility, enabling them to rapidly spread throughout a bacterial community. Methods: The tool MobileElementFinder was developed to enable rapid detection of MGEs and their genetic context in assembled sequence data. MGEs are detected based on sequence similarity to a database of 4452 known elements augmented with annotation of resistance genes, virulence factors and detection of plasmids. Results: MobileElementFinder was applied to analyse the mobilome of 1725 sequenced Salmonella enterica isolates of animal origin from Denmark, Germany and the USA. We found that the MGEs were seemingly conserved according to multilocus ST and not restricted to either the host or the country of origin. Moreover, we identified putative translocatable units for specific aminoglycoside, sulphonamide and tetracycline genes. Several putative composite transposons were predicted that could mobilize, among others, AMR, metal resistance and phosphodiesterase genes associated with macrophage survivability. This is, to our knowledge, the first time the phosphodiesterase-like pdeL has been found to be potentially mobilized into S. enterica. Conclusions: MobileElementFinder is a powerful tool to study the epidemiology of MGEs in a large number of genome sequences and to determine the potential for genomic plasticity of bacteria. This web service provides a convenient method of detecting MGEs in assembled sequence data. MobileElementFinder can be accessed at https://cge.cbs.dtu.dk/services/MobileElementFinder/.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1093/jac/dkaa390

Cites

2 of 2 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Some AMR determinants in probiotics reflect intrinsic or species-associated background resistance, whereas others are acquired, horizontally transferable and clinically relevant.

    “Some determinants reflect intrinsic or species-associated background resistance, whereas others are acquired, horizontally transferable and clinically relevant.”

    From Integrated Phenotypic and Sequencing-Based Resistome Assessment of Antimicrobial Resistance Determinants in a Sample of Commercial Farm-Animal Probiotic Products (2026) · cites this paper as [14]

    The Introduction (page not provided) says bacteria can acquire AMR through horizontal gene transfer and identifies AMR as a threat to human health. The Discussion, “Association of MGEs and AMR genes” (page not provided), describes potentially mobile AMR genes in Salmonella enterica. The paper does not establish the claimed distinction between intrinsic or species-associated background resistance and acquired resistance in probiotics. (LLM, conf=0.86)

    Experimental — accuracy not yet measured

  • Intrinsic determinants in Enterococcus faecium must be interpreted differently from mobile glycopeptide, oxazolidinone, colistin, ESBL or carbapenemase genes.

    “Intrinsic determinants in Enterococcus faecium, for example, must be interpreted differently from mobile glycopeptide, oxazolidinone, colistin, extended-spectrum β-lactamase (ESBL) or carbapenemase genes [11,12,13,14].”

    From Integrated Phenotypic and Sequencing-Based Resistome Assessment of Antimicrobial Resistance Determinants in a Sample of Commercial Farm-Animal Probiotic Products (2026) · cites this paper as [14]

    The Discussion section, “Association of MGEs and AMR genes” (page unavailable), reports that blaCTX-M-65 was near an insertion sequence likely to have mobilized it, supporting the mobile ESBL-gene part of the sentence. The paper studies Salmonella enterica; it does not discuss intrinsic determinants in Enterococcus faecium, how to interpret them, or the listed glycopeptide, oxazolidinone, colistin and carbapenemase genes. (LLM, conf=0.80)

    Experimental — accuracy not yet measured

  • The mere presence of an AMR-associated database hit does not necessarily imply public-health risk.

    “the mere presence of an AMR-associated database hit does not necessarily imply public-health risk.”

    From Integrated Phenotypic and Sequencing-Based Resistome Assessment of Antimicrobial Resistance Determinants in a Sample of Commercial Farm-Animal Probiotic Products (2026) · cites this paper as [14]

    The Methods section classifies AMR–mobile-element associations as potential mobilization, and the Discussion says experimental verification is needed to establish whether the genes are on translocatable units. I searched for discussion of database hits and public-health risk, but our copy does not address whether an AMR-associated hit, by itself, implies such risk. (LLM, conf=0.72)

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 42

  1. [2]Peterson E, Kaur P. Antibiotic resistance mechanisms in bacteria: relationships between resistance determinants of antibiotic producers, environmental bacteria, and clinical pathogens. Front Microbiol 2018; 9: 2928. 30555448 PMC6283892
  2. [3]Partridge SR, Kwong SM, Firth N et al Mobile genetic elements associated with antimicrobial resistance. Clin Microbiol Rev 2018; 31: e00088– 17. 30068738 PMC6148190
  3. [4]van Hoek AHAM, Mevius D, Guerra B et al Acquired antibiotic resistance genes: an overview. Front Microbiol 2011; 2: 203. 22046172 PMC3202223
  4. [5]Harmer C J Pong C H Hall R M. Structures bounded by directly-oriented members of the IS26 family are pseudo-compound transposons. Plasmid 2020; 111: 102530. 32871211
  5. [6]Vandecraen J, Chandler M, Aertsen A et al The impact of insertion sequences on bacterial genome plasticity and adaptability. Crit Rev Microbiol 2017; 43: 709– 30. 28407717
  6. [7]Harmer CJ, Moran RA, Hall RM. Movement of IS26-associated antibiotic resistance genes occurs via a translocatable unit that includes a single IS26 and preferentially inserts adjacent to another IS26. mBio 2014; 5: e01801– 14. 25293759 PMC4196232
  7. [8]Wozniak RAF, Waldor MK. Integrative and conjugative elements: mosaic mobile genetic elements enabling dynamic lateral gene flow. Nat Rev Microbiol 2010; 8: 552– 63. 20601965
  8. [9]Carraro N, Burrus V. The dualistic nature of integrative and conjugative elements. Mob Genet Elements 2015; 5: 98– 102. 26942046 PMC4755238
  9. [10]Wright LD, Grossman AD. Autonomous replication of the conjugative transposon Tn916. J Bacteriol 2016; 198: 3355– 66. 27698087 PMC5116939
  10. [11]Delavat F, Moritz R, van der Meer JR. Transient replication in specialized cells favors transfer of an integrative and conjugative element. mBio 2019; 10: e01133– 19. 31186329 PMC6561031
  11. [12]Frost LS, Leplae R, Summers AO et al Mobile genetic elements: the agents of open source evolution. Nat Rev Microbiol 2005; 3: 722– 32. 16138100
  12. [13]Liu M, Li X, Xie Y et al ICEberg 2.0: an updated database of bacterial integrative and conjugative elements. Nucleic Acids Res 2019; 47: D660– 5. 30407568 PMC6323972
  13. [14]Varani AM, Siguier P, Gourbeyre E et al ISsaga is an ensemble of web-based methods for high throughput identification and semi-automatic annotation of insertion sequences in prokaryotic genomes. Genome Biol 2011; 12: R30. 21443786 PMC3129680
  14. [15]Siguier P, Perochon J, Lestrade L et al ISfinder: the reference centre for bacterial insertion sequences. Nucleic Acids Res 2006; 34: D32– 6. 16381877 PMC1347377
  15. [16]Carattoli A, Zankari E, García-Fernández A et al In silico detection and typing of plasmids using PlasmidFinder and plasmid multilocus sequence typing. Antimicrob Agents Chemother 2014; 58: 3895– 903. 24777092 PMC4068535
  16. [17]Sheppard AE, Stoesser N, German-Mesner I et al TETyper: a bioinformatic pipeline for classifying variation and genetic contexts of transposable elements from short-read whole-genome sequencing data. Microb Genom 2018; 4: e000232. PMC6412039 30465646
  17. [18]Durrant MG, Li MM, Siranosian BA et al A bioinformatic analysis of integrative mobile genetic elements highlights their role in bacterial adaptation. Cell Host Microbe 2020; 27: 140– 53.e9. 31862382 PMC6952549
  18. [19]Chen S, Zhao S, White DG et al Characterization of multiple-antimicrobial-resistant Salmonella serovars isolated from retail meats. Appl Environ Microbiol 2004; 70: 1– 7. 14711619 PMC321239
  19. [20]Jajere SM. A review of Salmonella enterica with particular focus on the pathogenicity and virulence factors, host specificity and antimicrobial resistance including multidrug resistance. Vet World 2019; 12: 504– 21. 31190705 PMC6515828
  20. [21]Tansirichaiya S, Rahman MA, Roberts AP. The Transposon Registry. Mob DNA 2019; 10: 40. 31624505 PMC6785933
  21. [22]Karp BE, Tate H, Plumblee JR et al National antimicrobial resistance monitoring system: two decades of advancing public health through integrated surveillance of antimicrobial resistance. Foodborne Pathog Dis 2017; 14: 545– 57. 28792800 PMC5650714
  22. [23]Munck N, Leekitcharoenphon P, Litrup E et al Four European Salmonella Typhimurium datasets collected to develop WGS-based source attribution methods. Sci Data 2020; 7: 75. 32127544 PMC7054362
  23. [26]Bankevich A, Nurk S, Antipov D et al SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012; 19: 455– 77. 22506599 PMC3342519
  24. [28]Zankari E, Hasman H, Cosentino S et al Identification of acquired antimicrobial resistance genes. J Antimicrob Chemother 2012; 67: 2640– 4. 22782487 PMC3468078
  25. [29]Larsen MV, Cosentino S, Rasmussen S et al Multilocus sequence typing of total-genome-sequenced bacteria. J Clin Microbiol 2012; 50: 1355– 61. 22238442 PMC3318499
  26. [30]Jolley KA, Bray JE, Maiden MCJJ. Open-access bacterial population genomics: BIGSdb software, the PubMLST.org website and their applications. Wellcome Open Res 2018; 3: 124. 30345391 PMC6192448
  27. [32]Alikhan N-F, Zhou Z, Sergeant MJ et al A genomic overview of the population structure of Salmonella. PLoS Genet 2018; 14: e1007261. 29621240 PMC5886390
  28. [33]Dangel A, Berger A, Messelhäußer U et al Genetic diversity and delineation of Salmonella agona outbreak strains by next generation sequencing, Bavaria, Germany, 1993 to 2018. Euro Surveill 2019; 24: 1800303. PMC6505185 31064635
  29. [36]Letunic I, Bork P. Interactive Tree Of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Res 2019; 47: W256– 9. 30931475 PMC6602468
  30. [37]Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30: 2068– 9. 24642063
  31. [39]Cury J, Jové T, Touchon M et al Identification and analysis of integrons and cassette arrays in bacterial genomes. Nucleic Acids Res 2016; 44: 4539– 50. 27130947 PMC4889954
  32. [40]Treangen TJ, Salzberg SL. Repetitive DNA and next-generation sequencing: computational challenges and solutions. Nat Rev Genet 2012; 13: 36– 46. PMC3324860 22124482
  33. [41]Levings RS, Djordjevic SP, Hall RM. SGI2, a relative of Salmonella genomic island SGI1 with an independent origin. Antimicrob Agents Chemother 2008; 52: 2529– 37. 18443113 PMC2443934
  34. [42]Arai N, Sekizuka T, Tamamura Y et al Salmonella genomic island 3 is an integrative and conjugative element and contributes to copper and arsenic tolerance of Salmonella enterica. Antimicrob Agents Chemother 2019; 63: e00429– 19. 31209002 PMC6709492
  35. [43]Adams MD, Bishop B, Wright MS. Quantitative assessment of insertion sequence impact on bacterial genome architecture. Microb Genom 2016; 2: e000062. 28348858 PMC5343135
  36. [44]Foley SL, Lynne AM, Nayak R. Salmonella challenges: prevalence in swine and poultry and potential pathogenicity of such isolates. J Anim Sci 2008; 86: E149– 62. 17911227
  37. [45]Didelot X, Bowden R, Street T et al Recombination and population structure in Salmonella enterica. PLoS Genet 2011; 7: e1002191. 21829375 PMC3145606
  38. [46]Reinders A, Hee CS, Ozaki S et al Expression and genetic activation of cyclic di-GMP-specific phosphodiesterases in Escherichia coli. J Bacteriol 2016; 198: 448– 62. 26553851 PMC4719445
  39. [47]Petersen E, Mills E, Miller SI. Cyclic-di-GMP regulation promotes survival of a slow-replicating subpopulation of intracellular Salmonella Typhimurium. Proc Natl Acad Sci USA 2019; 116: 6335– 40. 30862737 PMC6442585
  40. [48]Machida Y, Machida C, Ohtsubo E. A novel type of transposon generated by insertion element IS102 present in a pSC101 derivative. Cell 1982; 30: 29– 36. 6290079
  41. [49]Prudhomme M, Turlan C, Claverys J-PP et al Diversity of Tn4001 transposition products: the flanking IS256 elements can form tandem dimers and IS circles. J Bacteriol 2002; 184: 433– 43. 11751820 PMC139565
  42. [50]Tansirichaiya S, Mullany P, Roberts AP. PCR-based detection of composite transposons and translocatable units from oral metagenomic DNA. FEMS Microbiol Lett 2016; 363: fnw195. 27521260 PMC5024762

Cited by

Sorted by citations

Authors
Johansson, M. H. K., Bortolaia, V., Tansirichaiya, S., Aarestrup, F. M., Roberts, A. P., & Petersen, T. N.
Affiliations
  • Technical University of Denmark (DK)
  • UiT The Arctic University of Norway (NO)
  • Liverpool School of Tropical Medicine (GB)
Corresponding author
Johansson, Markus H K
ORCID
Venue
Journal of Antimicrobial Chemotherapy
Publisher
Oxford University Press (OUP)
Published
2020-10-03
Volume
76
Issue
1
Pages
101-109
ISSN
  • 0305-7453 (ISSN-L)
  • 1460-2091
DOI
10.1093/jac/dkaa390
PMC
PMC7729385
OpenAlex
W3090034530
Cited by
725
References
2
Citations by year
2026: 172 · 2025: 153 · 2024: 152 · 2023: 118 · 2022: 91 · 2021: 36 · 2020: 3
FWCI
41.03
Type
journal article
Language
en
Open access
Licence
Locations
  • Journal of Antimicrobial Chemotherapy (publishedVersion, cc-by-nc)
  • PubMed Central (publishedVersion, cc-by-nc)
  • PubMed (publishedVersion)
  • LSTM Online Archive (Liverpool School of Tropical Medicine) (acceptedVersion)
  • Technical University of Denmark, DTU Orbit (Technical University of Denmark, DTU) (submittedVersion, cc-by-nc)
  • NORA - Norwegian Open Research Archives (submittedVersion, other-oa)
Funders
  • The Novo Nordisk Foundation (NNF16OC0021856)
  • Global Surveillance of Antimicrobial Resistance
Topics
  • Life Sciences › Agricultural and Biological Sciences › Food Science › Salmonella and Campylobacter epidemiology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Medicine › Antibiotic Resistance in Bacteria
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
Keywords
mobile genetic elements, antimicrobial resistance, Salmonella enterica, mobilome, composite transposon, transposon mobility, aminoglycoside resistance genes, tetracycline resistance genes, metal resistance genes, genome plasticity, virulence factors, plasmids, web-based tool
MeSH terms
Animals, Anti-Bacterial Agents, Drug Resistance, Microbial, Germany, Plasmids, Salmonella enterica, Interspersed Repetitive Sequences

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review