1887

Microbial Genomics logo

Volume 10, Issue 1

Insights gained from sequencing Australian non-invasive and invasive isolates Open Access

Abstract

Epidemiological data have indicated that invasive infections caused by the Gram-positive cocci (group A streptococcus, GAS) have increased in many Australian states over the past two decades. In July 2022, invasive GAS (iGAS) infections became nationally notifiable in Australia via public-health agencies. Surveillance for infections has been sporadic within the state of New South Wales (NSW). This has led to a lack of genetic data on GAS strains in circulation, particularly for non-invasive infections, which are the leading cause of GAS’s burden on the Australian healthcare system. To address this gap, we used whole-genome sequencing to analyse the genomes of 318 . isolates collected within two geographical regions of NSW. Invasive isolates were collected in 2007–2017, whilst non-invasive isolates were collected in 2019–2021. We found that at least 66 different -types were associated with clinical disease within NSW. There was no evidence of any Australian-specific clones in circulation. The M1 variant of the global pandemic clone (M1) has been detected in our isolates from 2013 onwards. We detected antimicrobial-resistance genes (mainly , or genes) in less than 10 % of our 318 isolates, which were more commonly associated with non-invasive infections. Superantigen virulence gene carriage was reasonably proportionate between non-invasive and invasive infection isolates. Our study adds rich data on the genetic makeup of historical infections within Australia. Ongoing surveillance of invasive and non-invasive GAS infections within NSW by whole-genome sequencing is warranted to inform on outbreaks, antimicrobial resistance and vaccine coverage.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): group A streptococcus
© 2024 Crown Copyright
  • 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.0.001152
2024-01-10
2024-12-06
Loading full text...

Full text loading...

/deliver/fulltext/mgen/10/1/mgen001152.html?itemId=/content/journal/mgen/10.1099/mgen.0.001152&mimeType=html&fmt=ahah

References

  1. Walker MJ, Barnett TC, McArthur JD, Cole JN, Gillen CM et al. Disease manifestations and pathogenic mechanisms of group A Streptococcus. Clin Microbiol Rev 2014; 27:264–301 [View Article] [PubMed]
     [Google Scholar]
  2. Dombek PE, Cue D, Sedgewick J, Lam H, Ruschkowski S et al. High-frequency intracellular invasion of epithelial cells by serotype M1 group A streptococci: M1 protein-mediated invasion and cytoskeletal rearrangements. Mol Microbiol 1999; 31:859–870 [View Article] [PubMed]
     [Google Scholar]
  3. Purushothaman SS, Wang B, Cleary PP. M1 protein triggers a phosphoinositide cascade for group A Streptococcus invasion of epithelial cells. Infect Immun 2003; 71:5823–5830 [View Article] [PubMed]
     [Google Scholar]
  4. Cole JN, Barnett TC, Nizet V, Walker MJ. Molecular insight into invasive group A streptococcal disease. Nat Rev Microbiol 2011; 9:724–736 [View Article] [PubMed]
     [Google Scholar]
  5. Brouwer S, Rivera-Hernandez T, Curren BF, Harbison-Price N, De Oliveira DMP et al. Pathogenesis, epidemiology and control of Group A Streptococcus infection. Nat Rev Microbiol 2023; 21:431–447 [View Article] [PubMed]
     [Google Scholar]
  6. Factor SH, Levine OS, Schwartz B, Harrison LH, Farley MM et al. Invasive group A streptococcal disease: risk factors for adults. Emerg Infect Dis 2003; 9:970–977 [View Article] [PubMed]
     [Google Scholar]
  7. Wright CM, Langworthy K, Manning L. The Australian burden of invasive group A streptococcal disease: a narrative review. Intern Med J 2021; 51:835–844 [View Article] [PubMed]
     [Google Scholar]
  8. Gray L-A, D’Antoine HA, Tong SYC, McKinnon M, Bessarab D et al. Genome-wide analysis of genetic risk factors for rheumatic heart disease in aboriginal Australians provides support for pathogenic molecular mimicry. J Infect Dis 2017; 216:1460–1470 [View Article] [PubMed]
     [Google Scholar]
  9. Coffey PM, Ralph AP, Krause VL. The role of social determinants of health in the risk and prevention of group A streptococcal infection, acute rheumatic fever and rheumatic heart disease: a systematic review. PLoS Negl Trop Dis 2018; 12:e0006577 [View Article] [PubMed]
     [Google Scholar]
  10. Carapetis JR, Steer AC, Mulholland EK, Weber M. The global burden of group A streptococcal diseases. Lancet Infect Dis 2005; 5:685–694 [View Article] [PubMed]
     [Google Scholar]
  11. Wright CM, Moorin R, Pearson G, Dyer JR, Carapetis JR et al. Increasing incidence of invasive group A streptococcal disease in Western Australia, particularly among indigenous people. Med J Aust 2021; 215:36–41 [View Article] [PubMed]
     [Google Scholar]
  12. Thomson TN, Campbell PT, Gibney KB. The epidemiology of invasive group A streptococcal disease in Victoria, 2007–2017: an analysis of linked datasets. Aust NZ J Public Health 2022; 46:878–883 [View Article] [PubMed]
     [Google Scholar]
  13. Cannon JW, Jack S, Wu Y, Zhang J, Baker MG et al. An economic case for a vaccine to prevent group A streptococcus skin infections. Vaccine 2018; 36:6968–6978 [View Article] [PubMed]
     [Google Scholar]
  14. Williamson KM, Varadhan H, Taylor K, Crooks K, Brett K. Epidemiology of group A streptococcal bacteraemia in Hunter New England Local Health district, 2008 to 2019. Commun Dis Intell 2008; 47:cdi.2023.47.49 [View Article]
     [Google Scholar]
  15. Australian Government Group A Streptococcal Disease – Invasive (iGAS) Canberra: Australian Government, Department of Health and Aged Care; 2022
     [Google Scholar]
  16. NSW Government, NSW Health, Invasive Group A Streptococcus control guideline; 2022 https://www.health.nsw.gov.au/Infectious/controlguideline/Pages/invasive-group-astrep.aspx
  17. Sivagnanam S, Zhou F, Lee AS, OʼSullivan MVN. Epidemiology of invasive group A Streptococcus infections in Sydney, Australia. Pathology 2015; 47:365–371 [View Article] [PubMed]
     [Google Scholar]
  18. Li Y, Rivers J, Mathis S, Li Z, Velusamy S et al. Genomic surveillance of Streptococcus pyogenes strains causing invasive disease, United States, 2016–2017. Front Microbiol 2020; 11:1547 [View Article] [PubMed]
     [Google Scholar]
  19. Lynskey NN. Emergence of dominant toxigenic M1T1 Streptococcus pyogenes clone during increased scarlet fever activity in England: a population-based molecular epidemiological study. Lancet Infect Dis 2019; 19:1209–1218 [View Article]
     [Google Scholar]
  20. NSW Government, Department of Communities and Justice, District Profiles, ABS 2016 Census Data; 2020 https://www.facs.nsw.gov.au/resources/statistics/dcj-districts
  21. Andrews S. FastQC: a quality control tool for high throughput sequence data; 2010 http://www.bioinformatics.babraham.ac.uk/projects/fastqc
  22. Wood DE, Lu J, Langmead B. Improved metagenomic analysis with Kraken 2. Genome Biol 2019; 20:257 [View Article] [PubMed]
     [Google Scholar]
  23. Souvorov A, Agarwala R, Lipman DJ. SKESA: strategic k-mer extension for scrupulous assemblies. Genome Biol 2018; 19:153 [View Article] [PubMed]
     [Google Scholar]
  24. Davies MR, McIntyre L, Mutreja A, Lacey JA, Lees JA et al. Atlas of group A streptococcal vaccine candidates compiled using large-scale comparative genomics. Nat Genet 2019; 51:1035–1043 [View Article] [PubMed]
     [Google Scholar]
  25. Chen S, Zhou Y, Chen Y, Gu J. fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 2018; 34:i884–i890 [View Article] [PubMed]
     [Google Scholar]
  26. 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]
  27. Seeman T. MLST; 2022 https://github.com/tseemann/mlst
  28. Seemann T. Abricate; 2020 https://github.com/tseemann/abricate
  29. Chen L, Zheng D, Liu B, Yang J, Jin Q. VFDB 2016: hierarchical and refined dataset for big data analysis – 10 years on. Nucleic Acids Res 2016; 44:D694–D697 [View Article] [PubMed]
     [Google Scholar]
  30. Feldgarden M, Brover V, Haft DH, Prasad AB, Slotta DJ et al. Validating the AMRFinder tool and resistance gene database by using antimicrobial resistance genotype-phenotype correlations in a collection of isolates. Antimicrob Agents Chemother 2019; 63:e00483-19 [View Article] [PubMed]
     [Google Scholar]
  31. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J et al. BLAST+: architecture and applications. BMC Bioinformatics 2009; 10:421 [View Article] [PubMed]
     [Google Scholar]
  32. Frost HR, Davies MR, Delforge V, Lakhloufi D, Sanderson-Smith M et al. Analysis of global collection of group A Streptococcus genomes reveals that the majority encode a trio of M and M-Like proteins. mSphere 2020; 5:e00806-19 [View Article] [PubMed]
     [Google Scholar]
  33. Sanderson-Smith M, De Oliveira DMP, Guglielmini J, McMillan DJ, Vu T et al. A systematic and functional classification of Streptococcus pyogenes that serves as a new tool for molecular typing and vaccine development. J Infect Dis 2014; 210:1325–1338 [View Article] [PubMed]
     [Google Scholar]
  34. Salvà-Serra F, Jaén-Luchoro D, Jakobsson HE, Gonzales-Siles L, Karlsson R et al. Complete genome sequences of Streptococcus pyogenes type strain reveal 100%-match between PacBio-solo and Illumina-Oxford Nanopore hybrid assemblies. Sci Rep 2020; 10:11656 [View Article] [PubMed]
     [Google Scholar]
  35. Li H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXiv 20131303.3997
     [Google Scholar]
  36. Garrison E, Marth G. Haplotype-based variant detection from short-read sequencing. arXiv 20121207.3907
     [Google Scholar]
  37. 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]
  38. 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 2014; 43:e15 [View Article] [PubMed]
     [Google Scholar]
  39. Minh BQ, Schmidt HA, Chernomor O, Schrempf D, Woodhams MD et al. IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol Biol Evol 2020; 37:1530–1534 [View Article] [PubMed]
     [Google Scholar]
  40. Letunic I, Bork P. Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res 2016; 44:W242–W245 [View Article] [PubMed]
     [Google Scholar]
  41. Oliver J, Wilmot M, Strachan J, St George S, Lane CR et al. Recent trends in invasive group A Streptococcus disease in Victoria. Commun Dis Intell 2018; 43:cdi.2019.43.8 [View Article]
     [Google Scholar]
  42. Gherardi G, Vitali LA, Creti R. Prevalent emm types among invasive GAS in Europe and North America since year 2000. Front Public Health 2018; 6:59 [View Article] [PubMed]
     [Google Scholar]
  43. Ekelund K, Darenberg J, Norrby-Teglund A, Hoffmann S, Bang D et al. Variations in emm type among group A streptococcal isolates causing invasive or noninvasive infections in a nationwide study. J Clin Microbiol 2005; 43:3101–3109 [View Article] [PubMed]
     [Google Scholar]
  44. Shea PR. Group A Streptococcus emm gene types in pharyngeal isolates. Emerg Infect Dis 2002; 17:2010–2017 [View Article]
     [Google Scholar]
  45. Li Y, Dominguez S, Nanduri SA, Rivers J, Mathis S et al. Genomic characterization of group A streptococci causing pharyngitis and invasive disease in Colorado, USA, June 2016– April 2017. J Infect Dis 2022; 225:1841–1851 [View Article] [PubMed]
     [Google Scholar]
  46. Shulman ST, Tanz RR, Kabat W, Kabat K, Cederlund E et al. Group A streptococcal pharyngitis serotype surveillance in North America, 2000–2002. Clin Infect Dis 2004; 39:325–332 [View Article] [PubMed]
     [Google Scholar]
  47. Hoe NP, Vuopio-Varkila J, Vaara M, Grigsby D, De Lorenzo D et al. Distribution of streptococcal inhibitor of complement variants in pharyngitis and invasive isolates in an epidemic of serotype M1 group A Streptococcus infection. J Infect Dis 2001; 183:633–639 [View Article] [PubMed]
     [Google Scholar]
  48. Bergin SM, Periaswamy B, Barkham T, Chua HC, Mok YM et al. An outbreak of Streptococcus pyogenes in a mental health facility: advantage of well-timed whole-genome sequencing over emm typing. Infect Control Hosp Epidemiol 2018; 39:852–860 [View Article] [PubMed]
     [Google Scholar]
  49. Turner CE, Bedford L, Brown NM, Judge K, Török ME et al. Community outbreaks of group A Streptococcus revealed by genome sequencing. Sci Rep 2017; 7:8554 [View Article] [PubMed]
     [Google Scholar]
  50. Plainvert C, Longo M, Seringe E, Saintpierre B, Sauvage E et al. A clone of the emergent Streptococcus pyogenes emm89 clade responsible for a large outbreak in a post-surgery oncology unit in France. Med Microbiol Immunol 2018; 207:287–296 [View Article] [PubMed]
     [Google Scholar]
  51. Shea PR, Beres SB, Flores AR, Ewbank AL, Gonzalez-Lugo JH et al. Distinct signatures of diversifying selection revealed by genome analysis of respiratory tract and invasive bacterial populations. Proc Natl Acad Sci USA 2011; 108:5039–5044 [View Article] [PubMed]
     [Google Scholar]
  52. Alamarat ZI, Sanson MA, McNeil JC, Baker CJ, Flores AR. Use of whole-genome sequencing to detect transmission of group A Streptococcus in Houston, TX. Access Microbiol 2022; 4:acmi000351 [View Article] [PubMed]
     [Google Scholar]
  53. Turner CE, Dryden M, Holden MTG, Davies FJ, Lawrenson RA et al. Molecular analysis of an outbreak of lethal postpartum sepsis caused by Streptococcus pyogenes. J Clin Microbiol 2013; 51:2089–2095 [View Article] [PubMed]
     [Google Scholar]
  54. Cockerill FR, MacDonald KL, Thompson RL, Roberson F, Kohner PC et al. An outbreak of invasive group A streptococcal disease associated with high carriage rates of the invasive clone among school-aged children. JAMA 1997; 277:38–43 [View Article] [PubMed]
     [Google Scholar]
  55. Musser JM, Kapur V, Peters JE, Hendrix CW, Drehner D et al. Real-time molecular epidemiologic analysis of an outbreak of Streptococcus pyogenes invasive disease in US Air Force trainees. Arch Pathol Lab Med 1994; 118:128–133 [PubMed]
     [Google Scholar]
  56. Muotiala A, Seppälä H, Huovinen P, Vuopio-Varkila J. Molecular comparison of group A streptococci of T1M1 serotype from invasive and noninvasive infections in Finland. J Infect Dis 1997; 175:392–399 [View Article] [PubMed]
     [Google Scholar]
  57. Teatero S, McGeer A, Tyrrell GJ, Hoang L, Smadi H et al. Canada-wide epidemic of emm74 group A Streptococcus invasive disease. Open Forum Infect Dis 2018; 5:ofy085 [View Article]
     [Google Scholar]
  58. Fittipaldi N, Tyrrell GJ, Low DE, Martin I, Lin D et al. Integrated whole-genome sequencing and temporospatial analysis of a continuing group A Streptococcus epidemic. Emerg Microbes Infect 2013; 2:1–8 [View Article] [PubMed]
     [Google Scholar]
  59. Athey TBT, Teatero S, Sieswerda LE, Gubbay JB, Marchand-Austin A et al. High incidence of invasive group A Streptococcus disease caused by strains of uncommon emm types in Thunder Bay, Ontario, Canada. J Clin Microbiol 2016; 54:83–92 [View Article] [PubMed]
     [Google Scholar]
  60. Mosites E, Frick A, Gounder P, Castrodale L, Li Y et al. Outbreak of invasive infections from subtype emm26.3 group A Streptococcus among homeless adults – Anchorage, Alaska, 2016–2017. Clin Infect Dis 2017; 66:1068–1074 [View Article] [PubMed]
     [Google Scholar]
  61. Hammond-Collins K, Strauss B, Barnes K, Demczuk W, Domingo M-C et al. Group A Streptococcus outbreak in a Canadian armed forces training facility. Mil Med 2019; 184:e197–e204 [View Article] [PubMed]
     [Google Scholar]
  62. Chalker VJ, Smith A, Al-Shahib A, Botchway S, Macdonald E et al. Integration of genomic and other epidemiologic data to investigate and control a cross-institutional outbreak of Streptococcus pyogenes. Emerg Infect Dis 2016; 22:973–980 [View Article] [PubMed]
     [Google Scholar]
  63. Fittipaldi N, Olsen RJ, Beres SB, Van Beneden C, Musser JM. Genomic analysis of emm59 group A Streptococcus invasive strains, United States. Emerg Infect Dis 2012; 18:650–652 [View Article] [PubMed]
     [Google Scholar]
  64. Cordery R, Purba AK, Begum L, Mills E, Mosavie M et al. Frequency of transmission, asymptomatic shedding, and airborne spread of Streptococcus pyogenes in schoolchildren exposed to scarlet fever: a prospective, longitudinal, multicohort, molecular epidemiological, contact-tracing study in England, UK. Lancet Microbe 2022; 3:e366–e375 [View Article] [PubMed]
     [Google Scholar]
  65. Lacey JA. Evaluating the role of asymptomatic throat carriage of Streptococcus pyogenes in impetigo transmission in remote Aboriginal communities in Northern territory, Australia: a retrospective genomic analysis. Lancet Microbe 2023; 4:e524–e533 [View Article]
     [Google Scholar]
  66. Davies MR, Keller N, Brouwer S, Jespersen MG, Cork AJ et al. Detection of Streptococcus pyogenes M1UK in Australia and characterization of the mutation driving enhanced expression of superantigen SpeA. Nat Commun 2023; 14:1051 [View Article] [PubMed]
     [Google Scholar]
  67. Kasper KJ, Zeppa JJ, Wakabayashi AT, Xu SX, Mazzuca DM et al. Bacterial superantigens promote acute nasopharyngeal infection by Streptococcus pyogenes in a human MHC class II-dependent manner. PLoS Pathog 2014; 10:e1004155 [View Article] [PubMed]
     [Google Scholar]
  68. Zhi X, Li HK, Li H, Loboda Z, Charles S et al. Emerging invasive group A Streptococcus M1(UK) lineage detected by allele-specific PCR, England, 2020. Emerg Infect Dis 2023; 29:1007–1010 [View Article]
     [Google Scholar]
  69. Vekemans J, Gouvea-Reis F, Kim JH, Excler J-L, Smeesters PR et al. The path to group A Streptococcus vaccines: World Health Organization research and development technology roadmap and preferred product characteristics. Clin Infect Dis 2019; 69:877–883 [View Article] [PubMed]
     [Google Scholar]
  70. Dale JB, Penfound TA, Chiang EY, Walton WJ. New 30-valent M protein-based vaccine evokes cross-opsonic antibodies against non-vaccine serotypes of group A streptococci. Vaccine 2011; 29:8175–8178 [View Article] [PubMed]
     [Google Scholar]
  71. Walkinshaw DR, Wright MEE, Mullin AE, Excler J-L, Kim JH et al. The Streptococcus pyogenes vaccine landscape. NPJ Vaccines 2023; 8:16 [View Article] [PubMed]
     [Google Scholar]
  72. Dale JB, Penfound TA, Tamboura B, Sow SO, Nataro JP et al. Potential coverage of a multivalent M protein-based group A streptococcal vaccine. Vaccine 2013; 31:1576–1581 [View Article] [PubMed]
     [Google Scholar]
/content/journal/mgen/10.1099/mgen.0.001152
Loading
Insights gained from sequencing Australian non-invasive and invasive Streptococcus pyogenes isolates
M Gen 10, 001152 (2024); https://doi.org/10.1099/mgen.0.001152
/content/journal/mgen/10.1099/mgen.0.001152
/content/journal/mgen/10.1099/mgen.0.001152
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