Skip to content
1887

Microbial Genomics logo Microbial Genomics

Volume 9, Issue 12

Genomic characterization of a unique Panton–Valentine leucocidin-positive community-associated methicillin-resistant lineage increasingly impacting on Australian indigenous communities Open Access

A Correction to this article was published on 31 January 2024

Abstract

In 2010 a single isolate of a trimethoprim-resistant multilocus sequence type 5, Panton–Valentine leucocidin-positive, community-associated methicillin-resistant (PVL-positive ST5 CA-MRSA), colloquially named WA121, was identified in northern Western Australia (WA). WA121 now accounts for ~14 % of all WA MRSA infections. To gain an understanding of the genetic composition and phylogenomic structure of WA121 isolates we sequenced the genomes of 155 WA121 isolates collected 2010–2021 and present a detailed genomic description. WA121 was revealed to be a single clonally expanding lineage clearly distinct from sequenced ST5 strains reported outside Australia. WA121 strains were typified by the presence of the distinct PVL phage φSa2wa-st5, the recently described methicillin resistance element SCCIVo carrying the trimethoprim resistance () transposon Tn, the novel β-lactamase transposon Tn and the epidermal cell differentiation inhibitor (EDIN-A) plasmid p2010-15611-2. We present evidence that SCCIVo together with Tn has horizontally transferred to and evidence of intragenomic movement of both Tn and Tn. We experimentally demonstrate that p2010-15611-2 is capable of horizontal transfer by conjugative mobilization from one of several WA121 isolates also harbouring a pWBG749-like conjugative plasmid. In summary, WA121 is a distinct and clonally expanding Australian PVL-positive CA-MRSA lineage that is increasingly responsible for infections in indigenous communities in northern and western Australia. WA121 harbours a unique complement of mobile genetic elements and is capable of transferring antimicrobial resistance and virulence determinants to other staphylococci.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): conjugative mobilization , dfrG SXT , Panton–Valentine leucocidin , PVL-positive , ST5 CA-MRSA and Tn4791 Tn916 Tn7702 Tn553
Funding
This study was supported by the:
  • Australian Research Council (Award FT170100235)
    • Principle Award Recipient: JoshuaPeter Ramsay
© 2023 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.

Erratum

An erratum has been published for this content:
Corrigendum: Genomic characterisation of a unique Panton-Valentine leucocidin-positive community-associated methicillin-resistant Staphylococcus aureus lineage increasingly impacting Australian indigenous communities
Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.001172
2023-12-20
2025-03-24
Loading full text...

Full text loading...

/deliver/fulltext/mgen/9/12/mgen001172.html?itemId=/content/journal/mgen/10.1099/mgen.0.001172&mimeType=html&fmt=ahah

References

  1. Lakhundi S, Zhang K. Methicillin-resistant Staphylococcus aureus: molecular characterization, evolution, and epidemiology. Clin Microbiol Rev 2018; 31:e00020-18 [View Article] [PubMed]
     [Google Scholar]
  2. Coombs GW, Goering RV, Chua KYL, Monecke S, Howden BP et al. The molecular epidemiology of the highly virulent ST93 Australian community Staphylococcus aureus strain. PLoS One 2012; 7:e43037 [View Article] [PubMed]
     [Google Scholar]
  3. Udo EE, Pearman JW, Grubb WB. Genetic analysis of community isolates of methicillin-resistant Staphylococcus aureus in Western Australia. J Hosp Infect 1993; 25:97–108 [View Article] [PubMed]
     [Google Scholar]
  4. Tong SYC, Bishop EJ, Lilliebridge RA, Cheng AC, Spasova-Penkova Z et al. Community-associated strains of methicillin-resistant Staphylococcus aureus and methicillin-susceptible S. aureus in indigenous Northern Australia: epidemiology and outcomes. J Infect Dis 2009; 199:1461–1470 [View Article] [PubMed]
     [Google Scholar]
  5. Munckhof WJ, Schooneveldt J, Coombs GW, Hoare J, Nimmo GR. Emergence of community-acquired methicillin-resistant Staphylococcus aureus (MRSA) infection in Queensland, Australia. Int J Infect Dis 2003; 7:259–264 [View Article] [PubMed]
     [Google Scholar]
  6. Coombs GW, Daley DA, Mowlaboccus S, Lee YT, Pang S et al. Australian Group on Antimicrobial Resistance (AGAR) Australian Staphylococcus aureus sepsis outcome programme (ASSOP) annual report 2018. Commun Dis Intell 2020; 44: [View Article] [PubMed]
     [Google Scholar]
  7. van Hal SJ, Steinig EJ, Andersson P, Holden MTG, Harris SR et al. Global scale dissemination of ST93: a divergent Staphylococcus aureus epidemic lineage that has recently emerged from remote Northern Australia. Front Microbiol 2018; 9:1453 [View Article]
     [Google Scholar]
  8. Tong SYC, Varrone L, Chatfield MD, Beaman M, Giffard PM. Progressive increase in community-associated methicillin-resistant Staphylococcus aureus in Indigenous populations in northern Australia from 1993 to 2012. Epidemiol Infect 2015; 143:1519–1523 [View Article] [PubMed]
     [Google Scholar]
  9. Peleg AY, Munckhof WJ. Fatal necrotising pneumonia due to community-acquired methicillin-resistant Staphylococcus aureus (MRSA). Med J Aust 2004; 181:228–229 [View Article] [PubMed]
     [Google Scholar]
  10. Coombs GW, Monecke S, Pearson JC, Tan H, Chew Y-K et al. Evolution and diversity of community-associated methicillin-resistant Staphylococcus aureus in a geographical region. BMC Microbiol 2011; 11:215 [View Article] [PubMed]
     [Google Scholar]
  11. Coombs GW, Mowlaboccus S, Daley D, Lee T, Pearson J et al. Sulfamethoxazole/trimethoprim resistance overcall by VITEK® 2 and BD Phoenix. J Antimicrob Chemother 2019; 74:3639–3641 [View Article] [PubMed]
     [Google Scholar]
  12. McGuinness SL, Holt DC, Harris TM, Wright C, Baird R et al. Clinical and molecular epidemiology of an emerging panton-valentine leukocidin-positive ST5 methicillin-resistant Staphylococcus aureus clone in Northern Australia. mSphere 2021; 6:e00651-20 [View Article] [PubMed]
     [Google Scholar]
  13. Coombs GW, Pearson J, Robinson O. Western Australian Methcillin-Resistant Staphylococcus aureus (MRSA) Epidemiology and Typing Report, July 1 2021 to June 30 2022; 2022
  14. Harris TM, Bowen AC, Holt DC, Sarovich DS, Stevens K et al. Investigation of trimethoprim/sulfamethoxazole resistance in an emerging sequence type 5 methicillin-resistant Staphylococcus aureus clone reveals discrepant resistance reporting. Clin Microbiol Infect 2018; 24:1027–1029 [View Article] [PubMed]
     [Google Scholar]
  15. Coombs GPJ, Robinson O. Western Australian Methcillin-Resistant Staphylococcus aureus (MRSA) Epidemiology and Typing Report, July 1 2020 to June 30 2021; 2021
  16. Karakatsanis NM, Colombi E, Mowlaboccus S, Pearson JC, Coombs GW et al. Complete genome sequences of three of the earliest community-associated methicillin-resistant Staphylococcus aureus strains isolated in remote Western Australia. Microbiol Resour Announc 2021; 10:e0079721 [View Article] [PubMed]
     [Google Scholar]
  17. Li H, Durbin R. Fast and accurate short read alignment with burrows-wheeler transform. Bioinformatics 2009; 25:1754–1760 [View Article] [PubMed]
     [Google Scholar]
  18. Okonechnikov K, Conesa A, García-Alcalde F. Qualimap 2: advanced multi-sample quality control for high-throughput sequencing data. Bioinformatics 2016; 32:292–294 [View Article] [PubMed]
     [Google Scholar]
  19. 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]
  20. 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]
  21. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article] [PubMed]
     [Google Scholar]
  22. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M et al. Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 2012; 28:1647–1649 [View Article] [PubMed]
     [Google Scholar]
  23. Zankari E, Hasman H, Cosentino S, Vestergaard M, Rasmussen S et al. Identification of acquired antimicrobial resistance genes. J Antimicrob Chemother 2012; 67:2640–2644 [View Article] [PubMed]
     [Google Scholar]
  24. Katz LS, Griswold T, Williams-Newkirk AJ, Wagner D, Petkau A et al. A comparative analysis of the Lyve-SET phylogenomics pipeline for genomic epidemiology of foodborne pathogens. Front Microbiol 2017; 8:375 [View Article] [PubMed]
     [Google Scholar]
  25. Zhou Y, Liang Y, Lynch KH, Dennis JJ, Wishart DS. PHAST: a fast phage search tool. Nucleic Acids Res 2011; 39:W347–52 [View Article] [PubMed]
     [Google Scholar]
  26. Kislyuk AO, Katz LS, Agrawal S, Hagen MS, Conley AB et al. A computational genomics pipeline for prokaryotic sequencing projects. Bioinformatics 2010; 26:1819–1826 [View Article] [PubMed]
     [Google Scholar]
  27. Ponstingl H, Ning Z. S. A new mapper for DNA sequencing reads. F1000Posters 2010; 1:313
     [Google Scholar]
  28. Koboldt DC, Zhang Q, Larson DE, Shen D, McLellan MD et al. VarScan 2: somatic mutation and copy number alteration discovery in cancer by exome sequencing. Genome Res 2012; 22:568–576 [View Article] [PubMed]
     [Google Scholar]
  29. Danecek P, Bonfield JK, Liddle J, Marshall J, Ohan V et al. Twelve years of SAMtools and BCFtools. Gigascience 2021; 10:giab008 [View Article] [PubMed]
     [Google Scholar]
  30. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014; 30:1312–1313 [View Article] [PubMed]
     [Google Scholar]
  31. Argimón S, Abudahab K, Goater RJE, Fedosejev A, Bhai J et al. Microreact: visualizing and sharing data for genomic epidemiology and phylogeography. Microb Genom 2016; 2:e000093 [View Article] [PubMed]
     [Google Scholar]
  32. Bouckaert R, Vaughan TG, Barido-Sottani J, Duchêne S, Fourment M et al. BEAST 2.5: An advanced software platform for Bayesian evolutionary analysis. PLoS Comput Biol 2019; 15:e1006650 [View Article] [PubMed]
     [Google Scholar]
  33. Suchard MA, Rambaut A. Many-core algorithms for statistical phylogenetics. Bioinformatics 2009; 25:1370–1376 [View Article] [PubMed]
     [Google Scholar]
  34. O’Brien FG, Yui Eto K, Murphy RJT, Fairhurst HM, Coombs GW et al. Origin-of-transfer sequences facilitate mobilisation of non-conjugative antimicrobial-resistance plasmids in Staphylococcus aureus. Nucleic Acids Res 2015; 43:7971–7983 [View Article] [PubMed]
     [Google Scholar]
  35. Challagundla L, Reyes J, Rafiqullah I, Sordelli DO, Echaniz-Aviles G et al. Phylogenomic classification and the evolution of clonal complex 5 methicillin-resistant Staphylococcus aureus in the Western hemisphere. Front Microbiol 2018; 9:1901 [View Article] [PubMed]
     [Google Scholar]
  36. O’Brien FG, Coombs GW, Pearman JW, Gracey M, Moss F et al. Population dynamics of methicillin-susceptible and -resistant Staphylococcus aureus in remote communities. J Antimicrob Chemother 2009; 64:684–693 [View Article] [PubMed]
     [Google Scholar]
  37. Aloba BK, Kinnevey PM, Monecke S, Brennan GI, O’Connell B et al. An emerging panton-Valentine leukocidin-positive CC5-meticillin-resistant Staphylococcus aureus-IVc clone recovered from hospital and community settings over a 17-year period from 12 countries investigated by whole-genome sequencing. J Hosp Infect 2023; 132:8–19 [View Article] [PubMed]
     [Google Scholar]
  38. Wang H, Wu D, Di L, Zhu F, Wang Z et al. Genetic characteristics of multiple copies of Tn1546-like elements in ermB-positive methicillin-resistant Staphylococcus aureus from Mainland China. Front Microbiol 2022; 13:814062 [View Article]
     [Google Scholar]
  39. Nurjadi D, Zizmann E, Chanthalangsy Q, Heeg K, Boutin S. Integrative analysis of whole genome sequencing and phenotypic resistance toward prediction of trimethoprim-sulfamethoxazole resistance in Staphylococcus aureus. Front Microbiol 2020; 11:607842 [View Article] [PubMed]
     [Google Scholar]
  40. Bertsch D, Uruty A, Anderegg J, Lacroix C, Perreten V et al. Tn6198, a novel transposon containing the trimethoprim resistance gene dfrG embedded into a Tn916 element in Listeria monocytogenes. J Antimicrob Chemother 2013; 68:986–991 [View Article] [PubMed]
     [Google Scholar]
  41. Sugai M, Enomoto T, Hashimoto K, Matsumoto K, Matsuo Y et al. A novel epidermal cell differentiation inhibitor (EDIN): purification and characterization from Staphylococcus aureus. Biochem Biophys Res Commun 1990; 173:92–98 [View Article] [PubMed]
     [Google Scholar]
  42. Inoue S, Sugai M, Murooka Y, Paik SY, Hong YM et al. Molecular cloning and sequencing of the epidermal cell differentiation inhibitor gene from Staphylococcus aureus. Biochem Biophys Res Commun 1991; 174:459–464 [View Article] [PubMed]
     [Google Scholar]
  43. Czech A, Yamaguchi T, Bader L, Linder S, Kaminski K et al. Prevalence of Rho-inactivating epidermal cell differentiation inhibitor toxins in clinical Staphylococcus aureus isolates. J Infect Dis 2001; 184:785–788 [View Article] [PubMed]
     [Google Scholar]
  44. Coombs GW, Baines SL, Howden BP, Swenson KM, O’Brien FG. Diversity of bacteriophages encoding Panton-Valentine leukocidin in temporally and geographically related Staphylococcus aureus. PLoS One 2020; 15:e0228676 [View Article] [PubMed]
     [Google Scholar]
  45. Gutiérrez D, Adriaenssens EM, Martínez B, Rodríguez A, Lavigne R et al. Three proposed new bacteriophage genera of staphylococcal phages: “3alikevirus”, “77likevirus” and “Phietalikevirus.”. Arch Virol 2014; 159:389–398 [View Article] [PubMed]
     [Google Scholar]
  46. Utter B, Deutsch DR, Schuch R, Winer BY, Verratti K et al. Beyond the chromosome: the prevalence of unique extra-chromosomal bacteriophages with integrated virulence genes in pathogenic Staphylococcus aureus. PLoS One 2014; 9:e100502 [View Article] [PubMed]
     [Google Scholar]
  47. Krüger H, Ji X, Wang Y, Feßler AT, Wang Y et al. Identification of Tn553, a novel Tn554-related transposon that carries a complete blaZ-blaR1-blaI β-lactamase operon in Staphylococcus aureus. J Antimicrob Chemother 2021; 76:2733–2735 [View Article] [PubMed]
     [Google Scholar]
  48. Permina EA, Mironov AA, Gelfand MS. Damage-repair error-prone polymerases of eubacteria: association with mobile genome elements. Gene 2002; 293:133–140 [View Article] [PubMed]
     [Google Scholar]
  49. Murphy E. Properties of the site-specific transposable element Tn554. In Novick RP. eds Molecular Biology of the Staphylococci New York, N.Y: VCH Publishers; 1990 pp 123–135
     [Google Scholar]
  50. Murphy E, Huwyler L, de Freire Bastos M do C. Transposon Tn554: complete nucleotide sequence and isolation of transposition-defective and antibiotic-sensitive mutants. EMBO J 1985; 4:3357–3365 [View Article] [PubMed]
     [Google Scholar]
  51. Murphy E. Transposable elements in Gram-positive bacteria. In Berg D, Howe M. eds Mobile DNA ASM Press; 1989 pp 269–288
     [Google Scholar]
  52. Shearer JES, Wireman J, Hostetler J, Forberger H, Borman J et al. Major families of multiresistant plasmids from geographically and epidemiologically diverse staphylococci. G3 (Bethesda) 2011; 1:581–591 [View Article] [PubMed]
     [Google Scholar]
  53. Ramsay JP, Kwong SM, Murphy RJT, Yui Eto K, Price KJ et al. An updated view of plasmid conjugation and mobilization in Staphylococcus. Mob Genet Elements 2016; 6:e1208317 [View Article] [PubMed]
     [Google Scholar]
  54. Berg T, Firth N, Apisiridej S, Hettiaratchi A, Leelaporn A et al. Complete nucleotide sequence of pSK41: evolution of staphylococcal conjugative multiresistance plasmids. J Bacteriol 1998; 180:4350–4359 [View Article] [PubMed]
     [Google Scholar]
  55. Bloomfield LE, Coombs GW, Tempone S, Armstrong PK. Marked increase in community-associated methicillin-resistant Staphylococcus aureus infections, Western Australia, 2004-2018. Epidemiol Infect 2020; 148:e153 [View Article] [PubMed]
     [Google Scholar]
  56. Sullivan MJ, Petty NK, Beatson SA. Easyfig: a genome comparison visualizer. Bioinformatics 2011; 27:1009–1010 [View Article] [PubMed]
     [Google Scholar]
/content/journal/mgen/10.1099/mgen.0.001172
Loading
Genomic characterization of a unique Panton–Valentine leucocidin-positive community-associated methicillin-resistant Staphylococcus aureus lineage increasingly impacting on Australian indigenous communities
M Gen 9, 001172 (2023); https://doi.org/10.1099/mgen.0.001172
/content/journal/mgen/10.1099/mgen.0.001172
/content/journal/mgen/10.1099/mgen.0.001172
Loading

Data & Media loading...

Supplements

Supplementary material 1

EXCEL

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