1887

Abstract

Multiply antibiotic-resistant infections are a global public health concern and accurate tracking of the spread of specific lineages is needed. Variation in the composition and structure of capsular polysaccharide (CPS), a critical determinant of virulence and phage susceptibility, makes it an attractive epidemiological marker. The outer core (OC) of lipooligosaccharide also exhibits variation. To take better advantage of the untapped information available in whole genome sequences, we have created a curated reference database of 92 publicly available gene clusters at the locus encoding proteins responsible for biosynthesis and export of CPS (K locus), and a second database for 12 gene clusters at the locus for outer core biosynthesis (OC locus). Each entry has been assigned a unique KL or OCL number, and is fully annotated using a simple, transparent and standardized nomenclature. These databases are compatible with , a tool for typing of bacterial surface polysaccharide loci, and their utility was validated using (a) >630 assembled draft genomes for which the KL and OCL regions had been previously typed manually, and (b) 3386 genome assemblies downloaded from NCBI. Among the previously typed genomes, was able to confidently assign KL and OCL types with 100 % accuracy. Among the genomes retrieved from NCBI, detected known KL and OCL in 87 and 90 % of genomes, respectively, indicating that the majority of common KL and OCL types are captured within the databases; 13 of the 92 KL in the database were not detected in any publicly available whole genome assembly. The failure to assign a KL or OCL type may indicate incomplete or poor-quality genomes. However, further novel variants may remain to be documented. Combining outputs with multilocus sequence typing (Institut Pasteur scheme) revealed multiple KL and OCL types in collections of a single sequence type (ST) representing each of the two predominant globally distributed clones, ST1 of GC1 and ST2 of GC2, and in collections of other clones comprising >20 isolates each (ST10, ST25, and ST140), indicating extensive within-clone replacement of these loci. The databases are available at https://github.com/katholt/Kaptive and will be updated as further locus types become available.

Funding
This study was supported by the:
  • Australian Research Council (Award DE180101563)
    • Principle Award Recipient: Johanna J Kenyon
  • 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.0.000339
2020-03-02
2024-03-19
Loading full text...

Full text loading...

/deliver/fulltext/mgen/6/3/mgen000339.html?itemId=/content/journal/mgen/10.1099/mgen.0.000339&mimeType=html&fmt=ahah

References

  1. World Health Organisation (WHO) 2017; Global priority list of antibiotic-resistant bacteria to guide research, discovery, and development of new antibiotics. https://www.who.int/medicines/publications/WHO-PPL-Short_Summary_25Feb-ET_NM_WHO.pdf
  2. 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]
    [Google Scholar]
  3. 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]
    [Google Scholar]
  4. Sahl JW, Del Franco M, Pournaras S, Colman RE, Karah N et al. Phylogenetic and genomic diversity in isolates from the globally distributed Acinetobacter baumannii ST25 lineage. Sci Rep 2015; 5:15188 [View Article]
    [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]
    [Google Scholar]
  6. Hamidian M, Nigro SJ. Emergence, molecular mechanisms and global spread of carbapenem-resistant Acinetobacter baumannii . Microb Genom 2019; 5: [View Article]
    [Google Scholar]
  7. Orskov I, Orskov F, Jann B, Jann K. Serology, chemistry, and genetics of O and K antigens of Escherichia coli . Bacteriol Rev 1977; 41:667–710 [View Article]
    [Google Scholar]
  8. Ørskov I, Ørskov F. Serotyping of Klebsiella . Method. Microbiol 1984; 14:143–164
    [Google Scholar]
  9. Liu B, Knirel YA, Feng L, Perepelov AV, Senchenkova S et al. Structure and genetics of Shigella O antigens. FEMS Microbiol Rev 2008; 32:627–653 [View Article]
    [Google Scholar]
  10. Liu B, Knirel YA, Feng L, Perepelov A, Senchenkova S et al. Structural diversity in Salmonella O antigens and its genetic basis. FEMS Microbiol Rev 2014; 38:56–89 [View Article]
    [Google Scholar]
  11. Kenyon JJ, Cunneen MM, Reeves PR. Genetics and evolution of Yersinia pseudotuberculosis O-specific polysaccharides: a novel pattern of O-antigen diversity. FEMS Microbiol Rev 2017; 41:200–217 [View Article]
    [Google Scholar]
  12. Stenutz R, Weintraub A, Widmalm G. The structures of Escherichia coli O-polysaccharide antigens. FEMS Microbiol Rev 2006; 30:382–403 [View Article]
    [Google Scholar]
  13. Traub WH. Acinetobacter baumannii serotyping for delineation of outbreaks of nosocomial cross-infection. J Clin Microbiol 1989; 27:2713–2716 [View Article]
    [Google Scholar]
  14. Pantophlet R. Lipopolysaccharides of Acinetobacter . In Gerischer U. editor Acinetobacter Molecular Microbiology Norfolk, UK: Horizon Scientific Press; 2008
    [Google Scholar]
  15. Traub WH, Bauer D. Surveillance of nosocomial cross-infections due to three Acinetobacter genospecies (Acinetobacter baumannii, genospecies 3 and genospecies 13) during a 10-year observation period: serotyping, macrorestriction analysis of genomic DNA and antibiotic susceptibilities. Chemotherapy 2000; 46:282–292 [View Article]
    [Google Scholar]
  16. Kenyon JJ, Hall RM. Variation in the complex carbohydrate biosynthesis loci of Acinetobacter baumannii genomes. PLoS One 2013; 8:e62160 [View Article]
    [Google Scholar]
  17. Russo TA, Luke NR, Beanan JM, Olson R, Sauberan SL et al. The K1 capsular polysaccharide of Acinetobacter baumannii strain 307-0294 is a major virulence factor. Infect Immun 2010; 78:3993–4000 [View Article]
    [Google Scholar]
  18. Fregolino E, Gargiulo V, Lanzetta R, Parrilli M, Holst O et al. Identification and structural determination of the capsular polysaccharides from two Acinetobacter baumannii clinical isolates, MG1 and SMAL. Carbohydr Res 2011; 346:973–977 [View Article]
    [Google Scholar]
  19. Oliveira H, Costa AR, Ferreira A, Konstantinides N, Santos SB et al. Functional analysis and antivirulence properties of a new depolymerase from a Myovirus that infects Acinetobacter baumannii capsule K45. J Virol 2019; 93:e01163–18 [View Article]
    [Google Scholar]
  20. Oliveira H, Costa AR, Konstantinides N, Ferreira A, Akturk E et al. Ability of phages to infect Acinetobacter calcoaceticus-Acinetobacter baumannii complex species through acquisition of different pectate lyase depolymerase domains. Environ Microbiol 2017; 19:5060–5077 [View Article]
    [Google Scholar]
  21. Russo TA, Beanan JM, Olson R, MacDonald U, Cox AD et al. The K1 capsular polysaccharide from Acinetobacter baumannii is a potential therapeutic target via passive immunization. Infect Immun 2013; 81:915–922 [View Article]
    [Google Scholar]
  22. Yang F-L, Lou T-C, Kuo S-C, Wu W-L, Chern J et al. A medically relevant capsular polysaccharide in Acinetobacter baumannii is a potential vaccine candidate. Vaccine 2017; 35:1440–1447 [View Article]
    [Google Scholar]
  23. Hu D, Liu B, Dijkshoorn L, Wang L, Reeves PR. Diversity in the major polysaccharide antigen of Acinetobacter baumannii assessed by DNA sequencing, and development of a molecular serotyping scheme. PLoS One 2013; 8:e70329 [View Article]
    [Google Scholar]
  24. Kenyon JJ, Senchenkova SYN, Shashkov AS, Shneider MM, Popova AV et al. K17 capsular polysaccharide produced by Acinetobacter baumannii isolate G7 contains an amide of 2-acetamido-2-deoxy-d-galacturonic acid with D-alanine. Int J Biol Macromol 2020; 144:857-862 [View Article]
    [Google Scholar]
  25. Kenyon JJ, Kasimova AA, Shashkov AS, Hall RM, Knirel YA. Acinetobacter baumannii isolate BAL_212 from Vietnam produces the K57 capsular polysaccharide containing a rarely occurring amino sugar N-acetylviosamine. Microbiology 2018; 164:217–220 [View Article]
    [Google Scholar]
  26. 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]
    [Google Scholar]
  27. Kenyon JJ, Shashkov AS, Senchenkova Sof'ya N, Shneider MM, Liu B et al. Acinetobacter baumannii K11 and K83 capsular polysaccharides have the same 6-deoxy-l-talose-containing pentasaccharide K units but different linkages between the K units. Int J Biol Macromol 2017; 103:648–655 [View Article]
    [Google Scholar]
  28. Kenyon JJ, Kasimova AA, Shneider MM, Shashkov AS, Arbatsky NP et al. The KL24 gene cluster and a genomic island encoding a Wzy polymerase contribute genes needed for synthesis of the K24 capsular polysaccharide by the multiply antibiotic resistant Acinetobacter baumannii isolate RCH51. Microbiol 2017; 163:355–363 [View Article]
    [Google Scholar]
  29. Kenyon JJ, Kasimova AA, Notaro A, Arbatsky NP, Speciale I et al. Acinetobacter baumannii K13 and K73 capsular polysaccharides differ only in K-unit side branches of novel non-2-ulosonic acids: di-N-acetylated forms of either acinetaminic acid or 8-epiacinetaminic acid. Carbohydr Res 2017; 452:149–155 [View Article]
    [Google Scholar]
  30. Kenyon JJ, Marzaioli AM, Hall RM, De Castro C. Structure of the K2 capsule associated with the KL2 gene cluster of Acinetobacter baumannii . Glycobiology 2014; 24:554–563 [View Article]
    [Google Scholar]
  31. Arbatsky NP, Kasimova AA, Shashkov AS, Shneider MM, Popova AV et al. Structure of the K128 capsular polysaccharide produced by Acinetobacter baumannii KZ-1093 from Kazakhstan. Carbohydr Res 2019; 485:107814 [View Article]
    [Google Scholar]
  32. Arbatsky NP, Shneider MM, Dmitrenok AS, Popova AV, Shagin DA et al. Structure and gene cluster of the K125 capsular polysaccharide from Acinetobacter baumannii MAR13-1452. Int J Biol Macromol 2018; 117:1195–1199 [View Article]
    [Google Scholar]
  33. Kasimova AA, Shneider MM, Arbatsky NP, Popova AV, Shashkov AS et al. Structure and gene cluster of the K93 capsular polysaccharide of Acinetobacter baumannii B11911 containing 5-N-Acetyl-7-N-[(R)-3-hydroxybutanoyl]pseudaminic acid. Biochemistry Moscow 2017; 82:483–489 [View Article]
    [Google Scholar]
  34. Senchenkova SN, Shashkov AS, Popova AV, Shneider MM, Arbatsky NP et al. Structure elucidation of the capsular polysaccharide of Acinetobacter baumannii AB5075 having the KL25 capsule biosynthesis locus. Carbohydr Res 2015; 408:8–11 [View Article]
    [Google Scholar]
  35. Shashkov AS, Kenyon JJ, Senchenkova SN, Shneider MM, Popova AV et al. Acinetobacter baumannii K27 and K44 capsular polysaccharides have the same K unit but different structures due to the presence of distinct wzy genes in otherwise closely related K gene clusters. Glycobiology 2016; 26:501–508 [View Article]
    [Google Scholar]
  36. Kenyon JJ, Hall RM, De Castro C. Structural determination of the K14 capsular polysaccharide from an ST25 Acinetobacter baumannii isolate, D46. Carbohydr Res 2015; 417:52–56 [View Article]
    [Google Scholar]
  37. Lees-Miller RG, Iwashkiw JA, Scott NE, Seper A, Vinogradov E et al. A common pathway for O-linked protein-glycosylation and synthesis of capsule in Acinetobacter baumannii . Mol Microbiol 2013; 89:816–830 [View Article]
    [Google Scholar]
  38. 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]
    [Google Scholar]
  39. Kenyon JJ, Nigro SJ, Hall RM. Variation in the OC locus of Acinetobacter baumannii genomes predicts extensive structural diversity in the lipooligosaccharide. PLoS One 2014; 9:e107833 [View Article]
    [Google Scholar]
  40. Meumann EM, Anstey NM, Currie BJ, Piera KA, Kenyon JJ et al. Genomic epidemiology of severe community-onset Acinetobacter baumannii infection. Microb Genom 2019; 5: 26 02 2019 [View Article]
    [Google Scholar]
  41. Schultz MB, Pham Thanh D, Tran Do Hoan N, Wick RR, Ingle DJ et al. Repeated local emergence of carbapenem-resistant Acinetobacter baumannii in a single hospital ward. Microb Genom 2016; 2:e000050 [View Article]
    [Google Scholar]
  42. Wright MS, Haft DH, Harkins DM, Perez F, Hujer KM et al. New insights into dissemination and variation of the health care-associated pathogen Acinetobacter baumannii from genomic analysis. mBio 2014; 5:e00963–13 [View Article]
    [Google Scholar]
  43. 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]
    [Google Scholar]
  44. Wyres KL, Wick RR, Gorrie C, Jenney A, Follador R et al. Identification of Klebsiella capsule synthesis loci from whole genome data. Microb Genom 2016; 2:e000102 [View Article]
    [Google Scholar]
  45. Wick RR, Heinz E, Holt KE, Wyres KL. Kaptive Web: User-friendly capsule and lipopolysaccharide Serotype prediction for Klebsiella genomes. J Clin Microbiol 2018; 56:e00197–18 [View Article]
    [Google Scholar]
  46. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012; 19:455–477 [View Article]
    [Google Scholar]
  47. 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]
    [Google Scholar]
  48. Kenyon JJ, Marzaioli AM, De Castro C, Hall RM. 5,7-di-N-acetyl-acinetaminic acid: a novel non-2-ulosonic acid found in the capsule of an Acinetobacter baumannii isolate. Glycobiology 2015; 25:644–654 [View Article]
    [Google Scholar]
  49. Arbatsky NP, Kenyon JJ, Shashkov AS, Shneider MM, Popova AV et al. The K5 capsular polysaccharide of the bacterium Acinetobacter baumannii SDF with the same K unit containing Leg5Ac7Ac as the K7 capsular polysaccharide but a different linkage between the K units. Russ Chem Bull 2019; 68:163–167 [View Article]
    [Google Scholar]
  50. Shashkov AS, Kenyon JJ, Arbatsky NP, Shneider MM, Popova AV et al. Structures of three different neutral polysaccharides of Acinetobacter baumannii, NIPH190, NIPH201, and NIPH615, assigned to K30, K45, and K48 capsule types, respectively, based on capsule biosynthesis gene clusters. Carbohydr Res 2015; 417:81–88 [View Article]
    [Google Scholar]
  51. Kenyon JJ, Shneider MM, Senchenkova SN, Shashkov AS, Siniagina MN et al. K19 capsular polysaccharide of Acinetobacter baumannii is produced via a Wzy polymerase encoded in a small genomic island rather than the KL19 capsule gene cluster. Microbiology 2016; 162:1479–1489 [View Article]
    [Google Scholar]
  52. Shashkov AS, Kenyon JJ, Arbatsky NP, Shneider MM, Popova AV et al. Related structures of neutral capsular polysaccharides of Acinetobacter baumannii isolates that carry related capsule gene clusters KL43, KL47, and KL88. Carbohydr Res 2016; 435:173–179 [View Article]
    [Google Scholar]
  53. Shashkov AS, Cahill SM, Arbatsky NP, Westacott AC, Kasimova AA et al. Acinetobacter baumannii K116 capsular polysaccharide structure is a hybrid of the K14 and revised K37 structures. Carbohydr Res 2019; 484:107774 [View Article]
    [Google Scholar]
  54. Kenyon JJ, Arbatsky NP, Shneider MM, Popova AV, Dmitrenok AS et al. The K46 and K5 capsular polysaccharides produced by Acinetobacter baumannii NIPH 329 and SDF have related structures and the side-chain non-ulosonic acids are 4-O-acetylated by phage-encoded O-acetyltransferases. PLoS One 2019; 14:e0218461 [View Article]
    [Google Scholar]
  55. Arbatsky NP, Shneider MM, Kenyon JJ, Shashkov AS, Popova AV et al. Structure of the neutral capsular polysaccharide of Acinetobacter baumannii NIPH146 that carries the KL37 capsule gene cluster. Carbohydr Res 2015; 413:12–15 [View Article]
    [Google Scholar]
  56. Kenyon JJ, Notaro A, Hsu LY, De Castro C, Hall RM. 5,7-Di-N-acetyl-8-epiacinetaminic acid: A new non-2-ulosonic acid found in the K73 capsule produced by an Acinetobacter baumannii isolate from Singapore. Sci Rep 2017; 7:11357 [View Article]
    [Google Scholar]
  57. 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]
  58. 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]
    [Google Scholar]
  59. Wick RR, Schultz MB, Zobel J, Holt KE. Bandage: interactive visualization of de novo genome assemblies. Bioinformatics 2015; 31:3350–3352 [View Article]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/mgen/10.1099/mgen.0.000339
Loading
/content/journal/mgen/10.1099/mgen.0.000339
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Supplementary material 2

EXCEL
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