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Abstract

is a successful opportunistic pathogen that can compete for iron under iron-limiting conditions. Here, large novel transposons that carry genes for synthesis and transport of the fimsbactin siderophores present in some strains were examined. Tn, originally found in the global clone 1 (GC1) lineage 2 isolate D36, includes genes encoding proteins related to the TnsA, TnsB, TnsC transposition proteins (50–59 % identity), TnsD targeting protein (43 % identity) and TnsE (31 % identity) of Tn, and is found in the chromosome downstream of the gene, the preferred location for Tn, flanked by a 5 bp target site duplication. Tn is bounded by 29 bp inverted repeats and, like Tn, includes additional TnsB binding sites at each end. Tn or minor variants were detected in the equivalent location in complete or draft genomes of several further isolates belonging to GC1 [sequence type (ST) 1, ST81, ST94, ST328, ST623, ST717], GC2 (ST2) and ST10. However, in some of these isolates the surrounding region was clearly derived from a different lineage, indicating that the transposon may have been acquired by replacement of a segment of the chromosome. A recombination-free phylogeny revealed that there were several transposon acquisition events in GC1. The GC1 isolates were mainly lineage 2, but a potential third lineage was also detected. A related transposon, designated Tn, was detected in ATCC 17978 (ST437) and other ST437 isolates. However, the Tn targeting gene was interrupted by an ISAba12, and Tn is not downstream of .

Funding
This study was supported by the:
  • National Health and Medical Research Council (Award GNT1079616)
    • Principle Award Recipient: RuthM Hall
  • Australian Research Council (ARC) (Award DE200100111)
    • Principle Award Recipient: MohammadHamidian
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
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2021-03-22
2025-03-16
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References

  1. Zarrilli R, Pournaras S, Giannouli M, Tsakris A. Global evolution of multidrug-resistant Acinetobacter baumannii clonal lineages. Int J Antimicrob Agents 2013; 41:11–19 [View Article][PubMed]
    [Google Scholar]
  2. Adams MD, Wright MS, Karichu JK, Venepally P, Fouts DE et al. Rapid replacement of Acinetobacter baumannii strains accompanied by changes in lipooligosaccharide loci and resistance gene repertoire. mBio 2019; 10:e00356 [View Article][PubMed]
    [Google Scholar]
  3. Hamidian M, Hall RM. The AbaR antibiotic resistance islands found in Acinetobacter baumannii global clone 1 - structure, origin and evolution. Drug Resist Updat 2018; 41:26–39 [View Article][PubMed]
    [Google Scholar]
  4. Holt K, Kenyon JJ, Hamidian M, Schultz MB, Pickard DJ et al. Five decades of genome evolution in the globally distributed, extensively antibiotic-resistant Acinetobacter baumannii global clone 1. Microb Genom 2016; 2:e000052 [View Article][PubMed]
    [Google Scholar]
  5. Harding CM, Hennon SW, Feldman MF. Uncovering the mechanisms of Acinetobacter baumannii virulence. Nat Rev Microbiol 2018; 16:91–102 [View Article][PubMed]
    [Google Scholar]
  6. Mortensen BL, Skaar EP. Host-microbe interactions that shape the pathogenesis of Acinetobacter baumannii infection. Cell Microbiol 2012; 14:1336–1344 [View Article][PubMed]
    [Google Scholar]
  7. Actis LA, Tolmasky ME, Crosa LM, Crosa JH. Effect of iron-limiting conditions on growth of clinical isolates of Acinetobacter baumannii . J Clin Microbiol 1993; 31:2812–2815 [View Article][PubMed]
    [Google Scholar]
  8. Antunes LCS, Imperi F, Towner KJ, Visca P. Genome-assisted identification of putative iron-utilization genes in Acinetobacter baumannii and their distribution among a genotypically diverse collection of clinical isolates. Res Microbiol 2011; 162:279–284 [View Article][PubMed]
    [Google Scholar]
  9. Eijkelkamp BA, Hassan KA, Paulsen IT, Brown MH. Investigation of the human pathogen Acinetobacter baumannii under iron limiting conditions. BMC Genomics 2011; 12:126 [View Article][PubMed]
    [Google Scholar]
  10. Dorsey CW, Beglin MS, Actis LA. Detection and analysis of iron uptake components expressed by Acinetobacter baumannii clinical isolates. J Clin Microbiol 2003; 41:4188–4193 [View Article][PubMed]
    [Google Scholar]
  11. Dorsey CW, Tomaras AP, Connerly PL, Tolmasky ME, Crosa JH et al. The siderophore-mediated iron acquisition systems of Acinetobacter baumannii ATCC 19606 and Vibrio anguillarum 775 are structurally and functionally related. Microbiology 2004; 150:3657–3667 [View Article][PubMed]
    [Google Scholar]
  12. Penwell WF, DeGrace N, Tentarelli S, Gauthier L, Gilbert CM et al. Discovery and characterization of new hydroxamate siderophores, baumannoferrin A and B, produced by Acinetobacter baumannii . Chembiochem 2015; 16:1896–1904 [View Article][PubMed]
    [Google Scholar]
  13. Proschak A, Lubuta P, Grün P, Löhr F, Wilharm G et al. Structure and biosynthesis of fimsbactins A-F, siderophores from Acinetobacter baumannii and Acinetobacter baylyi . Chembiochem 2013; 14:633–638 [View Article][PubMed]
    [Google Scholar]
  14. Zimbler DL, Penwell WF, Gaddy JA, Menke SM, Tomaras AP et al. Iron acquisition functions expressed by the human pathogen Acinetobacter baumannii . Biometals 2009; 22:23–32 [View Article][PubMed]
    [Google Scholar]
  15. Hamidian M, Hawkey J, Holt KE, Hall RM. Genome sequence of Acinetobacter baumannii strain D36, an antibiotic-resistant isolate from lineage 2 of global clone 1. Genome Announc 2015; 3:e01478-15 [View Article][PubMed]
    [Google Scholar]
  16. Craig NL. Transposon Tn7 . Curr Top Microbiol Immunol 1996; 204:27–48 [View Article][PubMed]
    [Google Scholar]
  17. Peters JE. Tn7 . Microbiol Spectr 2014; 2:MDNA3-0010-2014
    [Google Scholar]
  18. Peters JE, Craig NL. Tn7: smarter than we thought. Nat Rev Mol Cell Biol 2001; 2:806–814 [View Article][PubMed]
    [Google Scholar]
  19. Douraghi M, Kenyon JJ, Aris P, Asadian M, Ghourchian S et al. Accumulation of antibiotic resistance genes in carbapenem-resistant Acinetobacter baumannii isolates belonging to lineage 2, global clone 1, from outbreaks in 2012-2013 at a Tehran burns hospital. mSphere 2020; 5:e00164-20 [View Article][PubMed]
    [Google Scholar]
  20. Hamidian M, Wick RR, Hartstein RM, Judd LM, Holt KE et al. Insights from the revised complete genome sequences of Acinetobacter baumannii strains AB307-0294 and ACICU belonging to global clones 1 and 2. Microb Genom 2019; 5:e000298 [View Article][PubMed]
    [Google Scholar]
  21. The UniProt Consortium UniProt: the universal protein knowledgebase. Nucleic Acids Res 2017; 45:D158–D169 [View Article][PubMed]
    [Google Scholar]
  22. 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]
  23. Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY et al. Pfam: the protein families database. Nucleic Acids Res 2014; 42:D222–D230 [View Article][PubMed]
    [Google Scholar]
  24. Hamidian M, Nigro SJ. Emergence, molecular mechanisms and global spread of carbapenem-resistant Acinetobacter baumannii . Microb Genom 2019; 5:e000306 [View Article][PubMed]
    [Google Scholar]
  25. Holt KE, Hamidian M, Kenyon JJ, Wynn MT, Hawkey J et al. Genome sequence of Acinetobacter baumannii strain A1, an early example of antibiotic-resistant global clone 1. Genome Announc 2015; 3:e00032-15 [View Article][PubMed]
    [Google Scholar]
  26. Blackwell GA, Nigro SJ, Hall RM. Evolution of AbGRI2-0, the progenitor of the AbGRI2 resistance island in global clone 2 of Acinetobacter baumannii . Antimicrob Agents Chemother 2015; 60:1421–1429 [View Article][PubMed]
    [Google Scholar]
  27. Ou H-Y, Kuang SN, He X, Molgora BM, Ewing PJ et al. Complete genome sequence of hypervirulent and outbreak-associated Acinetobacter baumannii strain LAC-4: epidemiology, resistance genetic determinants and potential virulence factors. Sci Rep 2015; 5:8643 [View Article][PubMed]
    [Google Scholar]
  28. Carver TJ, Rutherford KM, Berriman M, Rajandream M-A, Barrell BG et al. ACT: the Artemis Comparison Tool. Bioinformatics 2005; 21:3422–3423 [View Article][PubMed]
    [Google Scholar]
  29. Arciszewska LK, Craig NL. Interaction of the Tn7-encoded transposition protein TnsB with the ends of the transposon. Nucleic Acids Res 1991; 19:5021–5029 [View Article][PubMed]
    [Google Scholar]
  30. Parks AR, Peters JE. Tn7 elements: engendering diversity from chromosomes to episomes. Plasmid 2009; 61:1–14 [View Article][PubMed]
    [Google Scholar]
  31. Linz B, Mukhtar N, Shabbir MZ, Rivera I, Ivanov YV et al. Virulent epidemic pneumonia in sheep caused by the human pathogen Acinetobacter baumannii . Front Microbiol 2018; 9:2616 [View Article][PubMed]
    [Google Scholar]
  32. Lesho E, Yoon E-J, McGann P, Snesrud E, Kwak Y et al. Emergence of colistin-resistance in extremely drug-resistant Acinetobacter baumannii containing a novel pmrCAB operon during colistin therapy of wound infections. J Infect Dis 2013; 208:1142–1151 [View Article][PubMed]
    [Google Scholar]
  33. Galac MR, Snesrud E, Lebreton F, Stam J, Julius M et al. A diverse panel of clinical Acinetobacter baumannii for research and development. Antimicrob Agents Chemother 2020; 64:e00840-20 [View Article][PubMed]
    [Google Scholar]
  34. Kasimova AA, Kenyon JJ, Arbatsky NP, Shashkov AS, Popova AV et al. Acinetobacter baumannii K20 and K21 capsular polysaccharide structures establish roles for UDP-glucose dehydrogenase Ugd2, pyruvyl transferase Ptr2 and two glycosyltransferases. Glycobiology 2018; 28:876–884 [View Article][PubMed]
    [Google Scholar]
  35. Domingues S, Rosário N, Cândido Ângela, Neto D, Nielsen KM et al. Competence for natural transformation is common among clinical strains of resistant Acinetobacter spp. Microorganisms 2019; 7:30 [View Article][PubMed]
    [Google Scholar]
  36. Godeux A-S, Svedholm E, Lupo A, Haenni M, Venner S et al. Scarless removal of large resistance island AbaR results in antibiotic susceptibility and increased natural transformability in Acinetobacter baumannii . Antimicrob Agents Chemother 2020; 64:e00951-20 [View Article][PubMed]
    [Google Scholar]
  37. Wilharm G, Piesker J, Laue M, Skiebe E. DNA uptake by the nosocomial pathogen Acinetobacter baumannii occurs during movement along wet surfaces. J Bacteriol 2013; 195:4146–4153 [View Article][PubMed]
    [Google Scholar]
  38. 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]
  39. Hamidian M, Hancock DP, Hall RM. Horizontal transfer of an ISAba125-activated ampC gene between Acinetobacter baumannii strains leading to cephalosporin resistance. J Antimicrob Chemother 2013; 68:244–245 [View Article][PubMed]
    [Google Scholar]
  40. 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]
  41. 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]
  42. Kenyon JJ, Hall RM. Variation in the complex carbohydrate biosynthesis loci of Acinetobacter baumannii genomes. PLoS One 2013; 8:e62160 [View Article][PubMed]
    [Google Scholar]
  43. Hua X, Moran RA, Xu Q, He J, Fang Y et al. Acquisition of a genomic resistance island (AbGRI5) from global clone 2 through homologous recombination in a clinical Acinetobacter baumannii isolate. J Antimicrob Chemother 2021; 76:65–69 [View Article][PubMed]
    [Google Scholar]
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