Skip to content
1887

Abstract

We studied the genomic evolution and transmission dynamics of multidrug-resistant ST15 (Institut Pasteur scheme) , examining resistance gene acquisition, clonal diversification, geographic distribution and origin of this high-risk clone. One hundred and fifty-two (=152) ST15 genomes from 18 countries (1997–2024), including 42 isolates from U.S. Military Treatment Facilities and 110 publicly available genomes in GenBank, were analysed. Whole-genome sequencing, assembly and annotation were performed using established bioinformatics pipelines. Phylogenetic analysis based on core-genome SNPs – filtered for recombination with – was combined with mobile element and resistance gene identification. ST15 isolates separated into two main clades with distinct subclades and variable resistance profiles. Homologous recombination drove the diversification of resistance determinants, including multiple alleles. Key resistance genes, such as , were disseminated via known transposons (Tn or Tn), while plasmid exchange, including module acquisitions, also played a role in the spread of . Patristic analysis identified Argentina as the likely origin for the emergence of ST15, aligning with early 1997 isolates. Recombination, transposon-mediated gene transfer and plasmid exchange have been central in driving the evolution and global dissemination of ST15.

Funding
This study was supported by the:
  • Saudi Arabian Ministry of Education scholarship
    • Principal Award Recipient: EradahAbu Sabah
  • Australian Government Research Training Program
    • Principal Award Recipient: LiamA. Tobin
  • United States Defense Health Program (DHP) Operation and Maintenance (O&M)
    • Principal Award Recipient: PatrickT. McGANN
  • Australian Institute for Microbiology and Infection
    • Principal Award Recipient: MehradHamidian
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.001450
2025-07-17
2026-04-14

Metrics

Loading full text...

Full text loading...

/deliver/fulltext/mgen/11/7/mgen001450.html?itemId=/content/journal/mgen/10.1099/mgen.0.001450&mimeType=html&fmt=ahah

References

  1. Cain AK, Hamidian M. Portrait of a killer: uncovering resistance mechanisms and global spread of Acinetobacter baumannii. PLoS Pathog 2023; 19:e1011520 [View Article] [PubMed]
    [Google Scholar]
  2. Hamidian M, Hawkey J, Wick R, Holt KE, Hall RM. Evolution of a clade of Acinetobacter baumannii global clone 1, lineage 1 via acquisition of carbapenem- and aminoglycoside-resistance genes and dispersion of ISAba1. Microb Genom 2019; 5:e000242 [View Article] [PubMed]
    [Google Scholar]
  3. Adams MD, Chan ER, Molyneaux ND, Bonomo RA. Genomewide analysis of divergence of antibiotic resistance determinants in closely related isolates of Acinetobacter baumannii. Antimicrob Agents Chemother 2010; 54:3569–3577 [View Article] [PubMed]
    [Google Scholar]
  4. Hamidian M, Hall RM. Genetic structure of four plasmids found in Acinetobacter baumannii isolate D36 belonging to lineage 2 of global clone 1. PLoS One 2018; 13:e0204357 [View Article] [PubMed]
    [Google Scholar]
  5. Hamidian M, Nigro SJ. Emergence, molecular mechanisms and global spread of carbapenem-resistant Acinetobacter baumannii. Microb Genom 2019; 5: [View Article]
    [Google Scholar]
  6. Pournaras S, Gogou V, Giannouli M, Dimitroulia E, Dafopoulou K et al. Single-locus-sequence-based typing of blaOXA-51-like genes for rapid assignment of Acinetobacter baumannii clinical isolates to international clonal lineages. J Clin Microbiol 2014; 52:1653–1657 [View Article] [PubMed]
    [Google Scholar]
  7. Sánchez-Urtaza S, Ocampo-Sosa A, Molins-Bengoetxea A, El-Kholy MA, Hernandez M et al. Molecular characterization of multidrug resistant Acinetobacter baumannii clinical isolates from Alexandria, Egypt. Front Cell Infect Microbiol 2023; 13:1208046 [View Article] [PubMed]
    [Google Scholar]
  8. Nazari M, Azizi O, Solgi H, Fereshteh S, Shokouhi S et al. Emergence of carbapenem resistant Acinetobacter baumannii clonal complexes CC2 and CC10 among fecal carriages in an educational hospital. Int J Environ Health Res 2022; 32:1478–1488 [View Article] [PubMed]
    [Google Scholar]
  9. Villalón P, Ortega M, Sáez-Nieto JA, Carrasco G, Medina-Pascual MJ et al. Dynamics of a sporadic nosocomial Acinetobacter calcoaceticus - Acinetobacter baumannii complex population. Front Microbiol 2019; 10:593 [View Article] [PubMed]
    [Google Scholar]
  10. Rodríguez CH, Balderrama Yarhui N, Nastro M, Nuñez Quezada T, Castro Cañarte G et al. Molecular epidemiology of carbapenem-resistant Acinetobacter baumannii in South America. J Med Microbiol 2016; 65:1088–1091 [View Article] [PubMed]
    [Google Scholar]
  11. Brito BP, Koong J, Wozniak A, Opazo-Capurro A, To J et al. Genomic analysis of carbapenem-resistant Acinetobacter baumannii strains recovered from Chilean hospitals reveals lineages specific to South America and multiple routes for acquisition of antibiotic resistance genes. Microbiol Spectr 2022; 10:e0246322 [View Article] [PubMed]
    [Google Scholar]
  12. Camargo CH, Cunha MPV, de Barcellos TAF, Bueno MS, Bertani AM de J et al. Genomic and phenotypic characterisation of antimicrobial resistance in carbapenem-resistant Acinetobacter baumannii hyperendemic clones CC1, CC15, CC79 and CC25. Int J Antimicrob Agents 2020; 56:106195 [View Article] [PubMed]
    [Google Scholar]
  13. Bello-Lopez E, Kawabata A, Cantero J, Mendoza S, Pertile E et al. Genomic epidemiology reveals antibiotic resistance transfer and polyclonal dissemination of Acinetobacter baumannii in a Paraguayan hospital. Microbiology 20252025 [View Article]
    [Google Scholar]
  14. Levy-Blitchtein S, Roca I, Plasencia-Rebata S, Vicente-Taboada W, Velásquez-Pomar J et al. Emergence and spread of carbapenem-resistant Acinetobacter baumannii international clones II and III in Lima, Peru. Emerg Microbes Infect 2018; 7:119 [View Article] [PubMed]
    [Google Scholar]
  15. Calhoun JH, Murray CK, Manring MM. Multidrug-resistant organisms in military wounds from Iraq and Afghanistan. Clin Orthop Relat Res 2008; 466:1356–1362 [View Article] [PubMed]
    [Google Scholar]
  16. Andrews S. A quality control tool for high throughput sequence data 2010 http://www.bioinformatics.babraham.ac.uk/projects/fastqc/
    [Google Scholar]
  17. Kong Y. Btrim: a fast, lightweight adapter and quality trimming program for next-generation sequencing technologies. Genomics 2011; 98:152–153 [View Article] [PubMed]
    [Google Scholar]
  18. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article] [PubMed]
    [Google Scholar]
  19. Siguier P, Perochon J, Lestrade L, Mahillon J, Chandler M. ISfinder: the reference centre for bacterial insertion sequences. Nucleic Acids Res 2006; 34:D32–6 [View Article] [PubMed]
    [Google Scholar]
  20. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990; 215:403–410 [View Article] [PubMed]
    [Google Scholar]
  21. Seemann T. ABRicate; 2017 https://github.com/tseemann/abricate
  22. Florensa AF, Kaas RS, Clausen PTLC, Aytan-Aktug D, Aarestrup FM. ResFinder - an open online resource for identification of antimicrobial resistance genes in next-generation sequencing data and prediction of phenotypes from genotypes. Microb Genom 2022; 8:000748 [View Article] [PubMed]
    [Google Scholar]
  23. Alcock BP, Huynh W, Chalil R, Smith KW, Raphenya AR et al. CARD 2023: expanded curation, support for machine learning, and resistome prediction at the comprehensive antibiotic resistance database. Nucleic Acids Res 2023; 51:D690–D699 [View Article] [PubMed]
    [Google Scholar]
  24. The UniProt Consortium UniProt: the universal protein knowledge base in 2023. Nucleic Acids Res 2022; 51:D523–D531
    [Google Scholar]
  25. Seemann T. mlst; 2019 https://github.com/tseemann/mlst
  26. Wyres KL, Cahill SM, Holt KE, Hall RM, Kenyon JJ. Identification of Acinetobacter baumannii loci for capsular polysaccharide (KL) and lipooligosaccharide outer core (OCL) synthesis in genome assemblies using curated reference databases compatible with Kaptive. Microb Genom 2020; 6:e000339 [View Article] [PubMed]
    [Google Scholar]
  27. Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res 2015; 25:1043–1055 [View Article] [PubMed]
    [Google Scholar]
  28. Croucher NJ, Page AJ, Connor TR, Delaney AJ, Keane JA et al. Rapid phylogenetic analysis of large samples of recombinant bacterial whole genome sequences using Gubbins. Nucleic Acids Res 2015; 43:e15-e15 [View Article] [PubMed]
    [Google Scholar]
  29. Lam MMC, Koong J, Holt KE, Hall RM, Hamidian M. Detection and typing of plasmids in Acinetobacter baumannii using rep genes encoding replication initiation proteins. Microbiol Spectr 2023; 11:e0247822 [View Article] [PubMed]
    [Google Scholar]
  30. Wishart DS, Han S, Saha S, Oler E, Peters H et al. PHASTEST: faster than PHASTER, better than PHAST. Nucleic Acids Res 2023; 51:W443–W450 [View Article] [PubMed]
    [Google Scholar]
  31. Wickham H. ggplot2: Elegant Graphics for Data Analysis Springer Publishing Company, Incorporated; 2016
    [Google Scholar]
  32. Fourment M, Gibbs MJ. PATRISTIC: a program for calculating patristic distances and graphically comparing the components of genetic change. BMC Evol Biol 2006; 6:1 [View Article] [PubMed]
    [Google Scholar]
  33. Cameranesi MM, Paganini J, Limansky AS, Moran-Barrio J, Salcedo SP et al. Acquisition of plasmids conferring carbapenem and aminoglycoside resistance and loss of surface-exposed macromolecule structures as strategies for the adaptation of Acinetobacter baumannii CC104/CC15 strains to the clinical setting. Microb Genom 2020; 6:mgen000360 [View Article] [PubMed]
    [Google Scholar]
  34. Brown S, Young HK, Amyes SGB. Characterisation of OXA-51, a novel class D carbapenemase found in genetically unrelated clinical strains of Acinetobacter baumannii from Argentina. Clin Microbiol Infect 2005; 11:15–23 [View Article] [PubMed]
    [Google Scholar]
  35. Nigro SJ, Hall RM. Does the intrinsic oxaAb (blaOXA-51-like) gene of Acinetobacter baumannii confer resistance to carbapenems when activated by ISAba1?. J Antimicrob Chemother 2018; 73:3518–3520 [View Article] [PubMed]
    [Google Scholar]
  36. Nigro SJ, Hall RM. Loss and gain of aminoglycoside resistance in global clone 2 Acinetobacter baumannii in Australia via modification of genomic resistance islands and acquisition of plasmids. J Antimicrob Chemother 2016; 71:2432–2440 [View Article] [PubMed]
    [Google Scholar]
  37. Nigro SJ, Hall RM. GIsul2, a genomic island carrying the sul2 sulphonamide resistance gene and the small mobile element CR2 found in the Enterobacter cloacae subspecies cloacae type strain ATCC 13047 from 1890, Shigella flexneri ATCC 700930 from 1954 and Acinetobacter baumannii ATCC 17978 from 1951. J Antimicrob Chemother 2011; 66:2175–2176 [View Article] [PubMed]
    [Google Scholar]
  38. Hamidian M, Hall RM. Origin of the AbGRI1 antibiotic resistance island found in the comM gene of Acinetobacter baumannii GC2 isolates. J Antimicrob Chemother 2017; 72:2944–2947 [View Article] [PubMed]
    [Google Scholar]
  39. Hamidian M, Hall RM. ISAba1 targets a specific position upstream of the intrinsic ampC gene of Acinetobacter baumannii leading to cephalosporin resistance. J Antimicrob Chemother 2013; 68:2682–2683 [View Article] [PubMed]
    [Google Scholar]
  40. Hamidian M, Hall RM. Resistance to third-generation cephalosporins in Acinetobacter baumannii due to horizontal transfer of a chromosomal segment containing ISAba1-ampC. J Antimicrob Chemother 2014; 69:2865–2866 [View Article] [PubMed]
    [Google Scholar]
  41. Hernández-González IL, Mateo-Estrada V, Castillo-Ramirez S. The promiscuous and highly mobile resistome of Acinetobacter baumannii. Microb Genom 2022; 8:000762 [View Article] [PubMed]
    [Google Scholar]
  42. Lam MMC, Hamidian M. Examining the role of Acinetobacter baumannii plasmid types in disseminating antimicrobial resistance. NPJ Antimicrob Resist 2024; 2:1 [View Article] [PubMed]
    [Google Scholar]
  43. Potron A, Poirel L, Croizé J, Chanteperdrix V, Nordmann P. Genetic and biochemical characterization of the first extended-spectrum CARB-type beta-lactamase, RTG-4, from Acinetobacter baumannii. Antimicrob Agents Chemother 2009; 53:3010–3016 [View Article] [PubMed]
    [Google Scholar]
  44. Tobin LA, Cain AK, Djordjevic SP, Hamidian M. Transposons carrying the aacc2e aminoglycoside and blatem beta-lactam resistance genes in Acinetobacter. Microb Drug Resist 2024; 30:273–278
    [Google Scholar]
  45. Tobin LA, Abu Sabah E, Lebreton F, Myers GSA, McGann PT et al. Genomic analysis of early ST32 Acinetobacter baumannii strains recovered in US military treatment facilities reveals distinct lineages and links to the origins of the Tn6168 ampC transposon. J Antimicrob Chemother 2025; 80:666–675 [View Article] [PubMed]
    [Google Scholar]
  46. Prity FT, Tobin LA, Maharajan R, Paulsen IT, Cain AK et al. The evolutionary tale of eight novel plasmids in a colistin-resistant environmental Acinetobacter baumannii isolate. Microb Genom 2023; 9:mgen001010 [View Article] [PubMed]
    [Google Scholar]
  47. Blackwell GA, Hall RM. The tet39 determinant and the msrE-mphE genes in Acinetobacter plasmids are each part of discrete modules flanked by inversely oriented pdif (xerc-xerd) sites. Antimicrob Agents Chemother 2017; 61:e00780–00717
    [Google Scholar]
  48. Hamidian M, Ambrose SJ, Hall RM. A large conjugative Acinetobacter baumannii plasmid carrying the sul2 sulphonamide and strAB streptomycin resistance genes. Plasmid 2016; 87–88:43–50 [View Article] [PubMed]
    [Google Scholar]
  49. Harmer CJ, Lebreton F, Stam J, McGann PT, Hall RM. Mechanisms of IS26-mediated amplification of the aphA1 gene leading to tobramycin resistance in an Acinetobacter baumannii isolate. Microbiol Spectr 2022; 10:e0228722 [View Article] [PubMed]
    [Google Scholar]
  50. McGann P, Courvalin P, Snesrud E, Clifford RJ, Yoon E-J et al. Amplification of aminoglycoside resistance gene aphA1 in Acinetobacter baumannii results in tobramycin therapy failure. mBio 2014; 5:e00915 [View Article] [PubMed]
    [Google Scholar]
  51. Mann R, Rafei R, Gunawan C, Harmer CJ, Hamidian M. Variants of Tn6924, a novel Tn7 family transposon carrying the blandm metallo-β-lactamase and 14 copies of the aphA6 amikacin resistance genes found in Acinetobacter baumannii. Microbiol Spectr 2022; 10:e0174521
    [Google Scholar]
/content/journal/mgen/10.1099/mgen.0.001450
Loading
/content/journal/mgen/10.1099/mgen.0.001450
Loading

Data & Media loading...

Supplements

Supplementary material 1

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An error occurred
Approval was partially successful, following selected items could not be processed due to error