1887

Microbial Genomics logo

Volume 7, Issue 12

Phylogenomics of two ST1 antibiotic-susceptible non-clinical strains reveals multiple lineages and complex evolutionary history in global clone 1 Open Access

Abstract

is an opportunistic pathogen that is difficult to treat due to its resistance to extreme conditions, including desiccation and antibiotics. Most strains causing outbreaks around the world belong to two main global lineages, namely global clones 1 and 2 (GC1 and GC2). Here, we used a combination of Illumina short read and MinION (Oxford Nanopore) long-read sequence data with a hybrid assembly approach to complete the genome sequence of two antibiotic-sensitive GC1 strains, Ex003 and Ax270, recovered in Lebanon from water and a rectal swab of a cat, respectively. Phylogenetic analysis of Ax270 and Ex003 with 186 publicly available GC1 genomes revealed two major clades, including five main lineages (L1–L5), and four single-isolate lineages outside of the two clades. Ax270 and Ex003, along with AB307-0294 and MRSN7213 (both predicted antibiotic-susceptible isolates) represent these individual lineages. Antibiotic resistance islands and transposons interrupting the gene remain important features in L1–L5, with L1 associated with the AbaR-type resistance islands, L2 with AbaR4, L3 strains containing either AbaR4 or its variants as well as Tn::ISAba42, and L4 and L5 associated with Tn or its variants. Analysis of the capsule (KL) and outer core (OCL) polysaccharide loci further revealed a complex evolutionary history probably involving many recombination events. As more genomes become available, more GC1 lineages continue to emerge. However, genome sequence data from more diverse geographical regions are needed to draw a more accurate population structure of this globally distributed clone.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): Acinetobacter baumannii , antibiotic resistance , GC1 , global clone , ST1 and whole genome sequence
Funding
This study was supported by the:
  • National Science Foundation (Award 2040697)
    • Principle Award Recipient: AllisonJ. Lopatkin
  • Australian Research Council (Award DE180101563)
    • Principle Award Recipient: JohannaJ. Kenyon
  • Australian Research Council (Award DE200100111)
    • Principle Award Recipient: MohammadHamidian
© 2021 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.000705
2021-12-07
2024-04-25
Loading full text...

Full text loading...

/deliver/fulltext/mgen/7/12/mgen000705.html?itemId=/content/journal/mgen/10.1099/mgen.0.000705&mimeType=html&fmt=ahah

References

  1. Antunes LCS, Visca P, Towner KJ. Acinetobacter baumannii: evolution of a global pathogen. Pathog Dis 2014; 71:292–301 [View Article] [PubMed]
     [Google Scholar]
  2. Dijkshoorn L, Nemec A, Seifert H. An increasing threat in hospitals: multidrug-resistant Acinetobacter baumannii. Nat Rev Microbiol 2007; 5:939–951 [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, Nigro SJ. Emergence, molecular mechanisms and global spread of carbapenem-resistant Acinetobacter baumannii. Microb Genom 2019; 5:e000306 [View Article] [PubMed]
     [Google Scholar]
  5. 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]
  6. 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]
  7. 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]
     [Google Scholar]
  8. Popovich KJ, Snitkin ES. Whole genome sequencing-implications for infection prevention and outbreak investigations. Curr Infect Dis Rep 2017; 19:15 [View Article] [PubMed]
     [Google Scholar]
  9. Quainoo S, Coolen JPM, van Hijum SAFT, Huynen MA, Melchers WJG et al. Whole-genome sequencing of bacterial pathogens: the future of nosocomial outbreak analysis. Clin Microbiol Rev 2017; 30:1015–1063 [View Article] [PubMed]
     [Google Scholar]
  10. 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]
  11. 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]
  12. 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]
  13. Griffith ME, Lazarus DR, Mann PB, Boger JA, Hospenthal DR et al. Acinetobacter skin carriage among US army soldiers deployed in Iraq. Infect Control Hosp Epidemiol 2015; 28:720–722 [View Article]
     [Google Scholar]
  14. Rafei R, Hamze M, Pailhoriès H, Eveillard M, Marsollier L et al. Extrahuman epidemiology of Acinetobacter baumannii in Lebanon. Appl Environ Microbiol 2015; 81:2359–2367 [View Article] [PubMed]
     [Google Scholar]
  15. Al Atrouni A, Hamze M, Rafei R, Eveillard M, Joly-Guillou ML et al. Diversity of Acinetobacter species isolated from different environments in Lebanon: a nationwide study. Future Microbiol 2016; 11:1147–1156 [View Article] [PubMed]
     [Google Scholar]
  16. Bell SM, Smith DD. The CDS disc method of antibiotic sensitivity testing (Calibrated Dichotomous Sensitivity Test). Pathology 1975; 7:1–48 [View Article]
     [Google Scholar]
  17. CLSI Performance Standards for Antimicrobial Susceptibility Testing; 29th Informational Supplement Wayne, PA: Clinical and Laboratory Standards Institute; 2019
     [Google Scholar]
  18. Wick RR, Judd LM, Gorrie CL, Holt KE. Completing bacterial genome assemblies with multiplex MinION sequencing. Microb Genom 2017; 3:e000132 [View Article] [PubMed]
     [Google Scholar]
  19. Wick RR, Judd LM, Gorrie CL, Holt KE. Unicycler: Resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput Biol 2017; 13:e1005595 [View Article] [PubMed]
     [Google Scholar]
  20. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article]
     [Google Scholar]
  21. Diancourt L, Passet V, Nemec A, Dijkshoorn L, Brisse S. The population structure of Acinetobacter baumannii: Expanding multiresistant clones from an ancestral susceptible genetic pool. PLOS ONE 2010; 5:e10034 [View Article] [PubMed]
     [Google Scholar]
  22. Bartual SG, Seifert H, Hippler C, Luzon MAD, Wisplinghoff H et al. Development of a Multilocus Sequence Typing scheme for characterization of clinical isolates of Acinetobacter baumannii. J Clin Microbiol 2005; 43:4382–4390 [View Article] [PubMed]
     [Google Scholar]
  23. 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]
  24. 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]
  25. 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 [View Article] [PubMed]
     [Google Scholar]
  26. Kozlov AM, Darriba D, Flouri T, Morel B, Stamatakis A et al. RAxML-NG: a fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference. Bioinformatics 2019; 35:4453–4455 [View Article]
     [Google Scholar]
  27. Tonkin-Hill G, Lees JA, Bentley SD, Frost SDW, Corander J. Fast hierarchical Bayesian analysis of population structure. Nucleic Acids Res 2019; 47:5539–5549 [View Article] [PubMed]
     [Google Scholar]
  28. Wickham H. Elegant graphics for data analysis. Media 2009; 35:10
     [Google Scholar]
  29. Yu G, Smith DK, Zhu H, Guan Y, Lam TT et al. ggtree : an r package for visualization and annotation of phylogenetic trees with their covariates and other associated data. Methods Ecol Evol 2016; 8:28–36 [View Article]
     [Google Scholar]
  30. Turton JF, Woodford N, Glover J, Yarde S, Kaufmann ME et al. Identification of Acinetobacter baumannii by detection of the blaOXA-51-like carbapenemase gene intrinsic to this species. J Clin Microbiol 2006; 44:2974–2976 [View Article] [PubMed]
     [Google Scholar]
  31. Vila J, Ruiz J, Goñi P, Jimenez de Anta T. Quinolone-resistance mutations in the topoisomerase IV parC gene of Acinetobacter baumannii. J Antimicrob Chemother 1997; 39:757–762 [View Article] [PubMed]
     [Google Scholar]
  32. Vila J, Ruiz J, Goñi P, Marcos A, Jimenez de Anta T. Mutation in the gyrA gene of quinolone-resistant clinical isolates of Acinetobacter baumannii. Antimicrob Agents Chemother 1995; 39:1201–1203 [View Article] [PubMed]
     [Google Scholar]
  33. Hamidian M, Holt KE, Pickard D, Hall RM. A small Acinetobacter plasmid carrying the tet39 tetracycline resistance determinant. J Antimicrob Chemother 2016; 71:269–271 [View Article] [PubMed]
     [Google Scholar]
  34. 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:e00780-17 [View Article] [PubMed]
     [Google Scholar]
  35. D’Andrea MM, Giani T, D’Arezzo S, Capone A, Petrosillo N et al. Characterization of pABVA01, a plasmid encoding the OXA-24 carbapenemase from Italian isolates of Acinetobacter baumannii. Antimicrob Agents Chemother 2009; 53:3528–3533 [View Article] [PubMed]
     [Google Scholar]
  36. 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]
  37. Merino M, Acosta J, Poza M, Sanz F, Beceiro A et al. OXA-24 carbapenemase gene flanked by XerC/XerD-like recombination sites in different plasmids from different Acinetobacter species isolated during a nosocomial outbreak. Antimicrob Agents Chemother 2010; 54:2724–2727 [View Article] [PubMed]
     [Google Scholar]
  38. Hamidian M, Hall RM. Dissemination of novel Tn7 family transposons carrying genes for synthesis and uptake of fimsbactin siderophores among Acinetobacter baumannii isolates. Microb Genom 2021; 7:000548 [View Article]
     [Google Scholar]
  39. Karah N, Wai SN, Uhlin BE. CRISPR-based subtyping to track the evolutionary history of a global clone of Acinetobacter baumannii. Infect Genet Evol 2021; 90:104774 [View Article] [PubMed]
     [Google Scholar]
  40. 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]
  41. Hujer KM, Hujer AM, Hulten EA, Bajaksouzian S, Adams JM et al. Analysis of antibiotic resistance genes in multidrug-resistant Acinetobacter sp. isolates from military and civilian patients treated at the Walter Reed Army Medical Center. Antimicrob Agents Chemother 2006; 50:4114–4123 [View Article]
     [Google Scholar]
  42. 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:e00356-19 [View Article] [PubMed]
     [Google Scholar]
  43. 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]
  44. Héritier C, Poirel L, Nordmann P. Cephalosporinase over-expression resulting from insertion of ISAba1 in Acinetobacter baumannii. Clin Microbiol Infect 2006; 12:123–130 [View Article] [PubMed]
     [Google Scholar]
  45. 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]
  46. Hamidian M, Kenyon JJ, Holt KE, Pickard D, Hall RM. A conjugative plasmid carrying the carbapenem resistance gene blaOXA-23 in AbaR4 in an extensively resistant GC1 Acinetobacter baumannii isolate. J Antimicrob Chemother 2014; 69:2625–2628 [View Article] [PubMed]
     [Google Scholar]
  47. 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]
  48. Loraine J, Heinz E, Soontarach R, Blackwell GA, Stabler RA et al. Genomic and phenotypic analyses of Acinetobacter baumannii isolates from three tertiary care hospitals in Thailand. Front Microbiol 2020; 11:548 [View Article] [PubMed]
     [Google Scholar]
  49. Palmieri M, D’Andrea MM, Pelegrin AC, Perrot N, Mirande C et al. Abundance of colistin-resistant, OXA-23- and ArmA-producing Acinetobacter baumannii belonging to International Clone 2 in Greece. Front Microbiol 2020; 11:668 [View Article] [PubMed]
     [Google Scholar]
  50. Hamidian M, Holt KE, Pickard D, Dougan G, Hall RM. A GC1 Acinetobacter baumannii isolate carrying AbaR3 and the aminoglycoside resistance transposon TnaphA6 in a conjugative plasmid. J Antimicrob Chemother 2014; 69:955–958 [View Article] [PubMed]
     [Google Scholar]
  51. Nigro SJ, Post V, Hall RM. Aminoglycoside resistance in multiply antibiotic-resistant Acinetobacter baumannii belonging to global clone 2 from Australian hospitals. J Antimicrob Chemother 2011; 66:1504–1509 [View Article] [PubMed]
     [Google Scholar]
  52. da Silva KE, Maciel WG, Croda J, Cayô R, Ramos AC et al. A high mortality rate associated with multidrug-resistant Acinetobacter baumannii ST79 and ST25 carrying OXA-23 in a Brazilian intensive care unit. PLOS ONE 2018; 13:e0209367 [View Article] [PubMed]
     [Google Scholar]
  53. Camargo CH, Cunha MPV, de Barcellos TAF, Bueno MS, Bertani A 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]
  54. Álvarez VE, Quiroga MP, Galán AV, Vilacoba E, Quiroga C et al. Crucial role of the accessory genome in the evolutionary trajectory of Acinetobacter baumannii global clone 1. Front Microbiol 2020; 11:342 [View Article] [PubMed]
     [Google Scholar]
  55. Kenyon JJ, Holt KE, Pickard D, Dougan G, Hall RM. Insertions in the OCL1 locus of Acinetobacter baumannii lead to shortened lipooligosaccharides. Res Microbiol 2014; 165:472–475 [View Article] [PubMed]
     [Google Scholar]
  56. Hamidian M, Ambrose SJ, Blackwell GA, Nigro SJ, Hall RM. An outbreak of multiply antibiotic-resistant ST49:ST128:KL11:OCL8 Acinetobacter baumannii isolates at a Sydney hospital. J Antimicrob Chemother 2021; 76:893–900 [View Article] [PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/mgen/10.1099/mgen.0.000705
Loading
Phylogenomics of two ST1 antibiotic-susceptible non-clinical Acinetobacter baumannii strains reveals multiple lineages and complex evolutionary history in global clone 1
M Gen 7, 000705 (2021); https://doi.org/10.1099/mgen.0.000705
/content/journal/mgen/10.1099/mgen.0.000705
/content/journal/mgen/10.1099/mgen.0.000705
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited Most Cited RSS feed

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