1887

Abstract

asymptomatically colonises 30 % of humans but can also cause a range of diseases, which can be fatal. In 2017 . was associated with 20 000 deaths in the USA alone. Dividing isolates into smaller sub-groups can reveal the emergence of distinct sub-populations with varying potential to cause infections. Despite multiple molecular typing methods categorising such sub-groups, they do not take full advantage of genome sequences when describing the fundamental population structure of the species. In this study, we developed Lineage Typing (SaLTy), which rapidly divides the species into 61 phylogenetically congruent lineages. Alleles of three core genes were identified that uniquely define the 61 lineages and were used for SaLTy typing. SaLTy was validated on 5000 genomes and 99.12 % (4956/5000) of isolates were assigned the correct lineage. We compared SaLTy lineages to previously calculated clonal complexes (CCs) from BIGSdb (=21 173). SALTy improves on CCs by grouping isolates congruently with phylogenetic structure. SaLTy lineages were further used to describe the carriage of Staphylococcal chromosomal cassette containing (SCC) which is carried by methicillin-resistant (MRSA). Most lineages had isolates lacking SCC and the four largest lineages varied in SCC over time. Classifying isolates into SaLTy lineages, which were further SCC typed, allowed SaLTy to describe high-level MRSA epidemiology. We provide SaLTy as a simple typing method that defines phylogenetic lineages (https://github.com/LanLab/SaLTy). SaLTy is highly accurate and can quickly analyse large amounts of genome data. SaLTy will aid the characterisation of populations and ongoing surveillance of sub-groups that threaten human health.

Funding
This study was supported by the:
  • National Health and Medical Research Council (Award 2021/GNT2011806)
    • Principle Award Recipient: RuitingLan
  • 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.0.001250
2024-05-13
2024-05-26
Loading full text...

Full text loading...

/deliver/fulltext/mgen/10/5/mgen001250.html?itemId=/content/journal/mgen/10.1099/mgen.0.001250&mimeType=html&fmt=ahah

References

  1. Wertheim HFL, Melles DC, Vos MC, van Leeuwen W, van Belkum A et al. The role of nasal carriage in Staphylococcus aureus infections. Lancet Infect Dis 2005; 5:751–762 [View Article] [PubMed]
    [Google Scholar]
  2. Tong SYC, Davis JS, Eichenberger E, Holland TL, Fowler VG. Staphylococcus aureus infections: epidemiology, pathophysiology, clinical manifestations, and management. Clin Microbiol Rev 2015; 28:603–661 [View Article] [PubMed]
    [Google Scholar]
  3. Chambers HF, Deleo FR. Waves of resistance: Staphylococcus aureus in the antibiotic era. Nat Rev Microbiol 2009; 7:629–641 [View Article] [PubMed]
    [Google Scholar]
  4. Robinson DA, Enright MC. Evolutionary models of the emergence of methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 2003; 47:3926–3934 [View Article] [PubMed]
    [Google Scholar]
  5. McGuinness WA, Malachowa N, DeLeo FR. Vancomycin resistance in Staphylococcus aureus. Yale J Biol Med 2017; 90:269–281
    [Google Scholar]
  6. Cong Y, Yang S, Rao X. Vancomycin resistant Staphylococcus aureus infections: a review of case updating and clinical features. J Adv Res 2020; 21:169–176 [View Article] [PubMed]
    [Google Scholar]
  7. David MZ, Daum RS. Community-associated methicillin-resistant Staphylococcus aureus: epidemiology and clinical consequences of an emerging epidemic. Clin Microbiol Rev 2010; 23:616–687 [View Article] [PubMed]
    [Google Scholar]
  8. Maree CL, Daum RS, Boyle-Vavra S, Matayoshi K, Miller LG. Community-associated methicillin-resistant Staphylococcus aureus isolates causing healthcare-associated infections. Emerg Infect Dis 2007; 13:236–242 [View Article] [PubMed]
    [Google Scholar]
  9. Naimi TS, LeDell KH, Como-Sabetti K, Borchardt SM, Boxrud DJ et al. Comparison of community- and health care-associated methicillin-resistant Staphylococcus aureus infection. JAMA 2003; 290:2976–2984 [View Article] [PubMed]
    [Google Scholar]
  10. Seybold U, Kourbatova EV, Johnson JG, Halvosa SJ, Wang YF et al. Emergence of community-associated methicillin-resistant Staphylococcus aureus USA300 genotype as a major cause of health care-associated blood stream infections. Clin Infect Dis 2006; 42:647–656 [View Article] [PubMed]
    [Google Scholar]
  11. Deurenberg RH, Vink C, Kalenic S, Friedrich AW, Bruggeman CA et al. The molecular evolution of methicillin-resistant Staphylococcus aureus. Clin Microbiol Infect 2007; 13:222–235 [View Article] [PubMed]
    [Google Scholar]
  12. Enright MC, Day NP, Davies CE, Peacock SJ, Spratt BG. Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus. J Clin Microbiol 2000; 38:1008–1015 [View Article] [PubMed]
    [Google Scholar]
  13. Strandén A, Frei R, Widmer AF. Molecular typing of methicillin-resistant Staphylococcus aureus: can PCR replace pulsed-field gel electrophoresis?. J Clin Microbiol 2003; 41:3181–3186 [View Article] [PubMed]
    [Google Scholar]
  14. McDougal LK, Steward CD, Killgore GE, Chaitram JM, McAllister SK et al. Pulsed-field gel electrophoresis typing of oxacillin-resistant Staphylococcus aureus isolates from the United States: establishing a national database. J Clin Microbiol 2003; 41:5113–5120 [View Article] [PubMed]
    [Google Scholar]
  15. Murchan S, Kaufmann ME, Deplano A, de Ryck R, Struelens M et al. Harmonization of pulsed-field gel electrophoresis protocols for epidemiological typing of strains of methicillin-resistant Staphylococcus aureus: a single approach developed by consensus in 10 European laboratories and its application for tracing the spread of related strains. J Clin Microbiol 2003; 41:1574–1585 [View Article] [PubMed]
    [Google Scholar]
  16. Bannerman TL, Hancock GA, Tenover FC, Miller JM. Pulsed-field gel electrophoresis as a replacement for bacteriophage typing of Staphylococcus aureus. J Clin Microbiol 1995; 33:551–555 [View Article] [PubMed]
    [Google Scholar]
  17. Simor AE, Ofner-Agostini M, Bryce E, Green K, McGeer A et al. The evolution of Methicillin-resistant Staphylococcus aureus in Canadian hospitals: 5 years of national surveillance. Can Med Assoc J 2001; 165:21–26
    [Google Scholar]
  18. Enright MC, Robinson DA, Randle G, Feil EJ, Grundmann H et al. The evolutionary history of methicillin-resistant Staphylococcus aureus (MRSA). Proc Natl Acad Sci U S A 2002; 99:7687–7692 [View Article] [PubMed]
    [Google Scholar]
  19. DeLeo FR, Otto M, Kreiswirth BN, Chambers HF. Community-associated meticillin-resistant Staphylococcus aureus. Lancet 2010; 375:1557–1568 [View Article] [PubMed]
    [Google Scholar]
  20. Feil EJ, Li BC, Aanensen DM, Hanage WP, Spratt BG. eBURST: inferring patterns of evolutionary descent among clusters of related bacterial genotypes from multilocus sequence typing data. J Bacteriol 2004; 186:1518–1530 [View Article] [PubMed]
    [Google Scholar]
  21. Bowers JR, Driebe EM, Albrecht V, McDougal LK, Granade M et al. Improved subtyping of Staphylococcus aureus clonal complex 8 strains based on whole-genome phylogenetic analysis. mSphere 2018; 3:e00464-17 [View Article] [PubMed]
    [Google Scholar]
  22. Feil EJ, Cooper JE, Grundmann H, Robinson DA, Enright MC et al. How clonal is Staphylococcus aureus?. J Bacteriol 2003; 185:3307–3316 [View Article] [PubMed]
    [Google Scholar]
  23. Havaei SA, Vidovic S, Tahmineh N, Mohammad K, Mohsen K et al. Epidemic methicillin-susceptible Staphylococcus aureus lineages are the main cause of infections at an Iranian university hospital. J Clin Microbiol 2011; 49:3990–3993 [View Article] [PubMed]
    [Google Scholar]
  24. Leinonen R, Sugawara H, Shumway M. International nucleotide sequence database C. the sequence read archive. Nucleic Acids Res 2011; 39:D19–D21 [View Article]
    [Google Scholar]
  25. Ridom GmbH cgMLST.org nomenclature server; 2022 https://cgmlst.org/ncs
  26. Frentrup M, Zhou Z, Steglich M, Meier-Kolthoff JP, Göker M et al. A publicly accessible database for Clostridioides difficile genome sequences supports tracing of transmission chains and epidemics. Microb Genom 2020; 6:mgen000410 [View Article] [PubMed]
    [Google Scholar]
  27. Achtman M, Zhou Z, Charlesworth J, Baxter L. EnteroBase: hierarchical clustering of 100 000s of bacterial genomes into species/subspecies and populations. Philos Trans R Soc Lond B Biol Sci20210240 2022; 377 [View Article] [PubMed]
    [Google Scholar]
  28. Leopold SR, Goering RV, Witten A, Harmsen D, Mellmann A. Bacterial whole-genome sequencing revisited: portable, scalable, and standardized analysis for typing and detection of virulence and antibiotic resistance genes. J Clin Microbiol 2014; 52:2365–2370 [View Article] [PubMed]
    [Google Scholar]
  29. Slott Jensen ML, Nielsine Skov M, Pries Kristiansen H, Toft A, Lundgaard H et al. Core genome multi-locus sequence typing as an essential tool in a high-cost livestock-associated meticillin-resistant Staphylococcus aureus CC398 hospital outbreak. J Hosp Infect 2020; 104:574–581 [View Article] [PubMed]
    [Google Scholar]
  30. Chen Y, Sun L, Wu D, Wang H, Ji S et al. Using core-genome multilocus sequence typing to monitor the changing epidemiology of methicillin-resistant Staphylococcus aureus in a teaching hospital. Clin Infect Dis 2018; 67:S241–S248 [View Article] [PubMed]
    [Google Scholar]
  31. Wildeman P, Tevell S, Eriksson C, Lagos AC, Söderquist B et al. Genomic characterization and outcome of prosthetic joint infections caused by Staphylococcus aureus. Sci Rep 2020; 10:5938 [View Article] [PubMed]
    [Google Scholar]
  32. Lagos AC, Sundqvist M, Dyrkell F, Stegger M, Söderquist B et al. Evaluation of within-host evolution of methicillin-resistant Staphylococcus aureus (MRSA) by comparing cgMLST and SNP analysis approaches. Sci Rep 2022; 12:10541 [View Article] [PubMed]
    [Google Scholar]
  33. Zhou Z, Charlesworth J, Achtman M. HierCC: a multi-level clustering scheme for population assignments based on core genome MLST. Bioinformatics 2021; 37:3645–3646 [View Article] [PubMed]
    [Google Scholar]
  34. Lees JA, Harris SR, Tonkin-Hill G, Gladstone RA, Lo SW et al. Fast and flexible bacterial genomic epidemiology with PopPUNK. Genome Res 2019; 29:304–316 [View Article] [PubMed]
    [Google Scholar]
  35. Hennart M, Guglielmini J, Bridel S, Maiden MCJ, Jolley KA et al. A dual barcoding approach to bacterial strain nomenclature: genomic taxonomy of Klebsiella pneumoniae strains. Mol Biol Evol 2022; 39:msac135 [View Article] [PubMed]
    [Google Scholar]
  36. Blin K. NCBI genome downloading scripts, GitHub repository; 2020 https://github.com/kblin/ncbi-genome-download
  37. Wood DE, Salzberg SL. Kraken: ultrafast metagenomic sequence classification using exact alignments. Genome Biol 2014; 15:R46 [View Article] [PubMed]
    [Google Scholar]
  38. Payne M, Kaur S, Wang Q, Hennessy D, Luo L et al. Multilevel genome typing: genomics-guided scalable resolution typing of microbial pathogens. Euro Surveill 2020; 25:1900519 [View Article] [PubMed]
    [Google Scholar]
  39. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014; 30:2114–2120 [View Article] [PubMed]
    [Google Scholar]
  40. 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] [PubMed]
    [Google Scholar]
  41. Gurevich A, Saveliev V, Vyahhi N, Tesler G. QUAST: quality assessment tool for genome assemblies. Bioinformatics 2013; 29:1072–1075 [View Article] [PubMed]
    [Google Scholar]
  42. Jolley KA, Maiden MCJ. BIGSdb: scalable analysis of bacterial genome variation at the population level. BMC Bioinform 2010; 11:595 [View Article] [PubMed]
    [Google Scholar]
  43. Simonsen M, Mailund T, Pedersen CNS. eds Inference of Large Phylogenies Using Neighbour-Joining Berlin, Heidelberg: Springer; 2011 [View Article]
    [Google Scholar]
  44. Zhou Z, Alikhan N-F, Sergeant MJ, Luhmann N, Vaz C et al. GrapeTree: visualization of core genomic relationships among 100,000 bacterial pathogens. Genome Res 2018; 28:1395–1404 [View Article] [PubMed]
    [Google Scholar]
  45. Hart EB. K. Prism: download data from the Oregon prism project; 2015 http://github.com/ropensci/prism
  46. Clausen P, Aarestrup FM, Lund O. Rapid and precise alignment of raw reads against redundant databases with KMA. BMC Bioinform 2018; 19:307 [View Article] [PubMed]
    [Google Scholar]
  47. Deadorf A. Tableau (version. 9.1). J Med Libr Assoc 2016; 104:182–183 [View Article]
    [Google Scholar]
  48. Seemann T. snippy: fast bacterial variant calling from NGS reads. 3.1 ed. https://github.com/tseemann/snippy GitHub; 2015
  49. Gill SR, Fouts DE, Archer GL, Mongodin EF, Deboy RT et al. Insights on evolution of virulence and resistance from the complete genome analysis of an early methicillin-resistant Staphylococcus aureus strain and a biofilm-producing methicillin-resistant Staphylococcus epidermidis strain. J Bacteriol 2005; 187:2426–2438 [View Article] [PubMed]
    [Google Scholar]
  50. Hu D, Liu B, Wang L, Reeves PR. Living trees: high-quality reproducible and reusable construction of bacterial phylogenetic trees. Mol Biol Evol 2020; 37:563–575 [View Article] [PubMed]
    [Google Scholar]
  51. Letunic I, Bork P. Interactive tree of life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res 2021; 49:W293–W296 [View Article] [PubMed]
    [Google Scholar]
  52. Petit RA, Read TD. Staphylococcus aureus viewed from the perspective of 40,000+ genomes. PeerJ 2018; 6:e5261 [View Article] [PubMed]
    [Google Scholar]
  53. Jolley KA, Bray JE, Maiden MCJ. Open-access bacterial population genomics: BIGSdb software, the PubMLST.org website and their applications. Wellcome Open Res 2018; 3:124 [View Article] [PubMed]
    [Google Scholar]
  54. Price J, Gordon NC, Crook D, Llewelyn M, Paul J. The usefulness of whole genome sequencing in the management of Staphylococcus aureus infections. Clin Microbiol Infect 2013; 19:784–789 [View Article] [PubMed]
    [Google Scholar]
  55. Aanensen DM, Feil EJ, Holden MTG, Dordel J, Yeats CA et al. Whole-genome sequencing for routine pathogen surveillance in public health: a population snapshot of invasive Staphylococcus aureus in Europe. mBio 2016; 7:e00444-16 [View Article] [PubMed]
    [Google Scholar]
  56. Schoch CL, Ciufo S, Domrachev M, Hotton CL, Kannan S et al. NCBI taxonomy: a comprehensive update on curation, resources and tools. Database 2020; 2020:baaa062 [View Article] [PubMed]
    [Google Scholar]
  57. King MD, Humphrey BJ, Wang YF, Kourbatova EV, Ray SM et al. Emergence of community-acquired methicillin-resistant Staphylococcus aureus USA 300 clone as the predominant cause of skin and soft-tissue infections. Ann Intern Med 2006; 144:309–317 [View Article] [PubMed]
    [Google Scholar]
  58. Richardson EJ, Bacigalupe R, Harrison EM, Weinert LA, Lycett S et al. Gene exchange drives the ecological success of a multi-host bacterial pathogen. Nat Ecol Evol 2018; 2:1468–1478 [View Article] [PubMed]
    [Google Scholar]
  59. Planet PJ, Narechania A, Chen L, Mathema B, Boundy S et al. Architecture of a species: phylogenomics of Staphylococcus aureus. Trends Microbiol 2017; 25:153–166 [View Article] [PubMed]
    [Google Scholar]
  60. Dallman T, Ashton P, Schafer U, Jironkin A, Painset A et al. SnapperDB: a database solution for routine sequencing analysis of bacterial isolates. Bioinformatics 2018; 34:3028–3029 [View Article] [PubMed]
    [Google Scholar]
  61. Turner NA, Sharma-Kuinkel BK, Maskarinec SA, Eichenberger EM, Shah PP et al. Methicillin-resistant Staphylococcus aureus: an overview of basic and clinical research. Nat Rev Microbiol 2019; 17:203–218 [View Article] [PubMed]
    [Google Scholar]
  62. Lakhundi S, aureus ZKM-RS. Molecular characterization, evolution, and epidemiology. Clin Microbiol Rev 2018; 31: [View Article]
    [Google Scholar]
  63. Stapleton PD, Taylor PW. Methicillin resistance in Staphylococcus aureus: mechanisms and modulation. Sci Prog 2002; 85:57–72 [View Article] [PubMed]
    [Google Scholar]
  64. Peacock SJ, Paterson GK. Mechanisms of methicillin resistance in Staphylococcus aureus. Annu Rev Biochem 2015; 84:577–601 [View Article] [PubMed]
    [Google Scholar]
  65. Deurenberg RH, Stobberingh EE. The evolution of Staphylococcus aureus. Infect Genet Evol 2008; 8:747–763 [View Article] [PubMed]
    [Google Scholar]
  66. Shopsin B, Kreiswirth BN. Molecular epidemiology of methicillin-resistant Staphylococcus aureus. Emerg Infect Dis 2001; 7:323–326 [View Article] [PubMed]
    [Google Scholar]
  67. Harmsen D, Claus H, Witte W, Rothgänger J, Claus H et al. Typing of methicillin-resistant Staphylococcus aureus in a university hospital setting by using novel software for spa repeat determination and database management. J Clin Microbiol 2003; 41:5442–5448 [View Article] [PubMed]
    [Google Scholar]
  68. Hanssen A-M, Ericson Sollid JU. Sccmec in Staphylococci: genes on the move. FEMS Immunol Med Microbiol 2006; 46:8–20 [View Article]
    [Google Scholar]
  69. Lowy FD. Antimicrobial resistance: the example of Staphylococcus aureus. J Clin Invest 2003; 111:1265–1273 [View Article] [PubMed]
    [Google Scholar]
  70. Strommenger B, Bartels MD, Kurt K, Layer F, Rohde SM et al. Evolution of methicillin-resistant Staphylococcus aureus towards increasing resistance. J Antimicrob Chemother 2014; 69:616–622 [View Article] [PubMed]
    [Google Scholar]
  71. Khatib R, Johnson L, Riederer K. Resurgence of methicillin susceptible (MSSA) Staphylococcus aureus (SA) in bacteremia. Open Forum Infect Dis 2017; 4:S562 [View Article]
    [Google Scholar]
  72. Kaplan SL, Hulten KG, Gonzalez BE, Hammerman WA, Lamberth L et al. Three-year surveillance of community-acquired Staphylococcus aureus infections in children. Clin Infect Dis 2005; 40:1785–1791 [View Article] [PubMed]
    [Google Scholar]
  73. Hota B, Ellenbogen C, Hayden MK, Aroutcheva A, Rice TW et al. Community-associated methicillin-resistant Staphylococcus aureus skin and soft tissue infections at a public hospital: do public housing and incarceration amplify transmission?. Arch Intern Med 2007; 167:1026–1033 [View Article] [PubMed]
    [Google Scholar]
  74. Jian Y, Zhao L, Zhao N, Lv H-Y, Liu Y et al. Increasing prevalence of hypervirulent ST5 methicillin susceptible Staphylococcus aureus subtype poses a serious clinical threat. Emerg Microbes Infect 2021; 10:109–122 [View Article] [PubMed]
    [Google Scholar]
  75. Maiden MCJ, Jansen van Rensburg MJ, Bray JE, Earle SG, Ford SA et al. MLST revisited: the gene-by-gene approach to bacterial genomics. Nat Rev Microbiol 2013; 11:728–736 [View Article] [PubMed]
    [Google Scholar]
  76. Kirchberger PC, Orata FD, Nasreen T, Kauffman KM, Tarr CL et al. Culture-independent tracking of vibrio cholerae lineages reveals complex spatiotemporal dynamics in a natural population. Environ Microbiol 2020; 22:4244–4256 [View Article] [PubMed]
    [Google Scholar]
  77. Johnson EJ, Zemanick ET, Accurso FJ, Wagner BD, Robertson CE et al. Molecular identification of Staphylococcus aureus in airway samples from children with cystic fibrosis. PLoS One 2016; 11:e0147643 [View Article] [PubMed]
    [Google Scholar]
  78. Hookey JV, Richardson JF, Cookson BD. Molecular typing of Staphylococcus aureus based on PCR restriction fragment length polymorphism and DNA sequence analysis of the coagulase gene. J Clin Microbiol 1998; 36:1083–1089 [View Article] [PubMed]
    [Google Scholar]
  79. Nguyen L-T, Schmidt HA, von Haeseler A, Minh BQ. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 2015; 32:268–274 [View Article] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/mgen/10.1099/mgen.0.001250
Loading
/content/journal/mgen/10.1099/mgen.0.001250
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
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