1887

Microbiology Society logo

Volume 169, Issue 1

Promiscuous evolution of Group A Streptococcal M and M-like proteins Open Access

Abstract

Group A (GAS) M and M-like proteins are essential virulence factors and represent the primary epidemiological marker of this pathogen. Protein sequences encoding 1054 M, Mrp and Enn proteins, from 1668 GAS genomes, were analysed by SplitsTree4, partitioning around medoids and co-occurrence. The splits network and groups-based analysis of all M and M-like proteins revealed four large protein groupings, with multiple evolutionary histories as represented by multiple edges for most splits, leading to ‘M-family-groups’ (FG) of protein sequences: FG I, Mrp; FG II, M protein and Protein H; FG III, Enn; and FG IV, M protein. M and Enn proteins formed two groups with nine sub-groups and Mrp proteins formed four groups with ten sub-groups. Discrete co-occurrence of M and M-like proteins were identified suggesting that while dynamic, evolution may be constrained by a combination of functional and virulence attributes. At a granular level, four distinct family-groups of M, Enn and Mrp proteins are observable, with Mrp representing the most genetically distinct of the family-group of proteins. While M and Enn protein families generally group into three distinct family-groups, horizontal and vertical gene flow between distinct GAS strains is ongoing.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): MGA regular , Streptococcus pyogenes , Surface protein , Typing , Vaccine and Virulence
Funding
This study was supported by the:
  • Fonds De La Recherche Scientifique - FNRS (Award PDR T.0255.16 and CDR J.0019.17)
    • Principle Award Recipient: PierreR Smeesters
© 2023 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.001280
2023-01-17
2024-05-17
Loading full text...

Full text loading...

/deliver/fulltext/micro/169/1/mic001280.html?itemId=/content/journal/micro/10.1099/mic.0.001280&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. 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]
  3. Steer AC, Law I, Matatolu L, Beall BW, Carapetis JR. Global emm type distribution of group a Streptococci: systematic review and implications for vaccine development. Lancet Infect Dis 2009; 9:611–616 [View Article]
     [Google Scholar]
  4. Dale JB, Walker MJ. Update on group A streptococcal vaccine development. Curr Opin Infect Dis 2020; 33:244–250 [View Article] [PubMed]
     [Google Scholar]
  5. Athey TBT, Teatero S, Li A, Marchand-Austin A, Beall BW et al. Deriving group a Streptococcus typing information from short-read whole-genome sequencing data. J Clin Microbiol 2014; 52:1871–1876 [View Article]
     [Google Scholar]
  6. Facklam R, Beall B, Efstratiou A, Fischetti V, Johnson D. emm typing and validation of provisional M types for group A streptococci. Emerg Infect Dis 1999; 5:247–253 [View Article]
     [Google Scholar]
  7. Bessen DE, Fischetti VA. Nucleotide sequences of two adjacent M or M-like protein genes of group A streptococci: different RNA transcript levels and identification of A unique immunoglobulin A-binding protein. Infect Immun 1992; 60:124–135 [View Article]
     [Google Scholar]
  8. Hollingshead SK, Readdy TL, Yung DL, Bessen DE. Structural heterogeneity of the emm gene cluster in group A streptococci. Mol Microbiol 1993; 8:707–717 [View Article] [PubMed]
     [Google Scholar]
  9. 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]
  10. Falugi F, Zingaretti C, Pinto V, Mariani M, Amodeo L et al. Sequence variation in group a Streptococcus pili and association of pilus backbone types with lancefield T serotypes. J Infect Dis 2008; 198:1834–1841 [View Article]
     [Google Scholar]
  11. Steemson JD, Moreland NJ, Williamson D, Morgan J, Carter PE. Survey of the bp/tee genes from clinical group A Streptococcus isolates in New Zealand - implications for vaccine development. J Med Microbiol 2014; 63:1670–1678 [View Article]
     [Google Scholar]
  12. Enright MC, Spratt BG, Kalia A, Cross JH, Bessen DE. Multilocus sequence typing of Streptococcus pyogenes and the relationships between emm type and clone. Infect Immun 2001; 69:2416–2427 [View Article] [PubMed]
     [Google Scholar]
  13. 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]
     [Google Scholar]
  14. Smeesters PR, McMillan DJ, Sriprakash KS. The streptococcal M protein: a highly versatile molecule. Trends Microbiol 2010; 18:275–282 [View Article] [PubMed]
     [Google Scholar]
  15. Frost HR, Laho D, Sanderson-Smith ML, Licciardi P, Donath S et al. Immune cross-opsonization within emm clusters following group A Streptococcus skin infection: broadening the scope of type-specific immunity. Clin Infect Dis 2017; 65:1523–1531 [View Article]
     [Google Scholar]
  16. 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]
     [Google Scholar]
  17. Frost HR, Sanderson-Smith M, Walker M, Botteaux A, Smeesters PR. Group A streptococcal M-like proteins: From pathogenesis to vaccine potential. FEMS Microbiol Rev 2018; 42:193–204 [View Article] [PubMed]
     [Google Scholar]
  18. Ermert D, Weckel A, Magda M, Mörgelin M, Shaughnessy J et al. Human IgG Increases Virulence of Streptococcus pyogenes through Complement Evasion. J Immunol 2018; 200:3495–3505 [View Article] [PubMed]
     [Google Scholar]
  19. Ermert D, Laabei M, Weckel A, Mörgelin M, Lundqvist M et al. The molecular basis of human IgG-mediated enhancement of C4b-Binding protein recruitment to group A Streptococcus. Front Immunol 2019; 10:1230 [View Article]
     [Google Scholar]
  20. DebRoy S, Li X, Kalia A, Galloway-Pena J, Shah BJ et al. Identification of A chimeric emm gene and novel emm pattern in currently circulating strains of emm4 Group A Streptococcus. Microb Genom 2018; 4:11 [View Article] [PubMed]
     [Google Scholar]
  21. Bao Y, Liang Z, Booyjzsen C, Mayfield JA, Li Y et al. Unique genomic arrangements in an invasive serotype M23 strain of Streptococcus pyogenes identify genes that induce hypervirulence. J Bacteriol 2014; 196:4089–4102 [View Article] [PubMed]
     [Google Scholar]
  22. McNeilly CL, McMillan DJ. Horizontal gene transfer and recombination in Streptococcus dysgalactiae subsp. equisimilis. Front Microbiol 2014; 5:676 [View Article] [PubMed]
     [Google Scholar]
  23. Almagro Armenteros JJ, Tsirigos KD, Sønderby CK, Petersen TN, Winther O et al. SignalP 5.0 improves signal peptide predictions using deep neural networks. Nat Biotechnol 2019; 37:420–423 [View Article] [PubMed]
     [Google Scholar]
  24. Katoh K, Kuma K, Toh H, Miyata T. MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res 2005; 33:511–518 [View Article] [PubMed]
     [Google Scholar]
  25. Huson DH, Bryant D. Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 2006; 23:254–267 [View Article] [PubMed]
     [Google Scholar]
  26. Csardi G, Nepusz T. The igraph software package for complex network research. InterJournal 2006Complex Systems:1695
     [Google Scholar]
  27. Team R RStudio: Integrated Development Environment for R. Boston, MA: RStudio, Inc; 2015
  28. Yang Z, Algesheimer R, Tessone CJ. A comparative analysis of community detection algorithms on Artificial Networks. Sci Rep 2016; 6:30750 [View Article]
     [Google Scholar]
  29. Hollingshead SK, Arnold J, Readdy TL, Bessen DE. Molecular evolution of A multigene family in group A streptococci. Mol Biol Evol 1994; 11:208–219 [View Article] [PubMed]
     [Google Scholar]
  30. Frick IM, Akesson P, Cooney J, Sjöbring U, Schmidt KH et al. Protein H--a surface protein of Streptococcus pyogenes with separate binding sites for IgG and albumin. Mol Microbiol 1994; 12:143–151 [View Article] [PubMed]
     [Google Scholar]
  31. Frick IM, Crossin KL, Edelman GM, Björck L. Protein H--a bacterial surface protein with affinity for both immunoglobulin and fibronectin type III domains. EMBO J 1995; 14:1674–1679 [View Article] [PubMed]
     [Google Scholar]
  32. Rouchon CN, Ly AT, Noto JP, Luo F, Lizano S et al. Incremental contributions of FbaA and other impetigo-associated surface proteins to fitness and virulence of a classical group a Streptococcal skin strain. Infect Immun 2017; 85:11 [View Article]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.001280
Loading
Promiscuous evolution of Group A Streptococcal M and M-like proteins
Microbiology 169, 001280 (2023); https://doi.org/10.1099/mic.0.001280
/content/journal/micro/10.1099/mic.0.001280
/content/journal/micro/10.1099/mic.0.001280
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