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Volume 160, Issue 2

Surface proteins of group G in different phases of growth: patterns of production and implications for the host–bacteria relationship Free

Abstract

Group G (GGS) is a human bacterial pathogen expressing surface proteins FOG and protein G (PG) which interact with several host defence systems, including the complement and contact systems. Selected reaction monitoring mass spectrometry, electron microscopy and protein binding assays were used to track the amounts of FOG and PG intracellularly and on the bacterial surface during different phases of growth. Large and increasing amounts of PG were present on the surface in the stationary growth phase, and this was due to production. In contrast, the amount of FOG did not change substantially during this phase. Apart from PG, a number of housekeeping proteins also increased in abundance in the stationary phase. These results show that GGS protein production is active during the stationary phase and that the bacteria actively remodel their surface and enter a less pro-inflammatory state in this phase.

  • Received:
  • Accepted:
  • Published Online:
Funding
This study was supported by the:
  • Swedish Research Council (Award 996, 2010:, 2008:3356 and 7480)
  • Swedish Government Funds for Clinical Research
  • Swedish Foundation
  • for Strategic Research (Award FFL4)
  • European Research Council (Award ERC-2012-StG-309831)
  • Crafoord Foundation (Award 20100892 and 20090802)
  • Knut and
  • Alice Wallenberg Foundation
  • Alfred Österlund Foundation
  • Greta and Johan Kock
  • Foundation
  • Hansa Medical AB
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2014-02-01
2024-04-26
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References

  1. Barer M. R. ( 2007). Bacterial growth, physiology and death. Medical Microbiology, 17th edn.38–51 Greenwood D., Slack R., Peutherer J., Barer M. Edinburgh: Elsevier;
     [Google Scholar]
  2. Björck L., Kronvall G. ( 1984). Purification and some properties of streptococcal protein G, a novel IgG-binding reagent. J Immunol 133:969–974[PubMed]
     [Google Scholar]
  3. Björck L., Kastern W., Lindahl G., Widebäck K. ( 1987). Streptococcal protein G, expressed by streptococci or by Escherichia coli, has separate binding sites for human albumin and IgG. Mol Immunol 24:1113–1122 [View Article][PubMed]
     [Google Scholar]
  4. Bober M., Enochsson C., Collin M., Mörgelin M. ( 2010). Collagen VI is a subepithelial adhesive target for human respiratory tract pathogens. J Innate Immun 2:160–166 [View Article][PubMed]
     [Google Scholar]
  5. Bramhachari P. V., Kaul S. Y., McMillan D. J., Shaila M. S., Karmarkar M. G., Sriprakash K. S. ( 2010). Disease burden due to Streptococcus dysgalactiae subsp. equisimilis (group G and C streptococcus) is higher than that due to Streptococcus pyogenes among Mumbai school children. J Med Microbiol 59:220–223 [View Article][PubMed]
     [Google Scholar]
  6. Brandt C. M., Spellerberg B. ( 2009). Human infections due to Streptococcus dysgalactiae subspecies equisimilis. Clin Infect Dis 49:766–772 [View Article][PubMed]
     [Google Scholar]
  7. Chen Z., Itzek A., Malke H., Ferretti J. J., Kreth J. ( 2012). Dynamics of speB mRNA transcripts in Streptococcus pyogenes. J Bacteriol 194:1417–1426 [View Article][PubMed]
     [Google Scholar]
  8. de Château M., Holst E., Björck L. ( 1996). Protein PAB, an albumin-binding bacterial surface protein promoting growth and virulence. J Biol Chem 271:26609–26615 [View Article][PubMed]
     [Google Scholar]
  9. Dinkla K., Nitsche-Schmitz D. P., Barroso V., Reissmann S., Johansson H. M., Frick I.-M., Rohde M., Chhatwal G. S. ( 2007). Identification of a streptococcal octapeptide motif involved in acute rheumatic fever. J Biol Chem 282:18686–18693 [View Article][PubMed]
     [Google Scholar]
  10. Egesten A., Eliasson M., Johansson H. M., Olin A. I., Mörgelin M., Mueller A., Pease J. E., Frick I.-M., Bjorck L. ( 2007). The CXC chemokine MIG/CXCL9 is important in innate immunity against Streptococcus pyogenes. J Infect Dis 195:684–693 [View Article][PubMed]
     [Google Scholar]
  11. Egesten A., Frick I.-M., Mörgelin M., Olin A. I., Björck L. ( 2011). Binding of albumin promotes bacterial survival at the epithelial surface. J Biol Chem 286:2469–2476 [View Article][PubMed]
     [Google Scholar]
  12. Frick I.-M., Åkesson P., Herwald H., Mörgelin M., Malmsten M., Nägler D. K., Björck L. ( 2006). The contact system – a novel branch of innate immunity generating antibacterial peptides. EMBO J 25:5569–5578 [View Article][PubMed]
     [Google Scholar]
  13. Guss B., Eliasson M., Olsson A., Uhlén M., Frej A. K., Jörnvall H., Flock J. I., Lindberg M. ( 1986). Structure of the IgG-binding regions of streptococcal protein G. EMBO J 5:1567–1575[PubMed]
     [Google Scholar]
  14. Herwald H., Cramer H., Mörgelin M., Russell W., Sollenberg U., Norrby-Teglund A., Flodgaard H., Lindbom L., Björck L. ( 2004). M protein, a classical bacterial virulence determinant, forms complexes with fibrinogen that induce vascular leakage. Cell 116:367–379 [View Article][PubMed]
     [Google Scholar]
  15. Johansson H. M., Mörgelin M., Frick I.-M. ( 2004). Protein FOG – a streptococcal inhibitor of neutrophil function. Microbiology 150:4211–4221 [View Article][PubMed]
     [Google Scholar]
  16. Karlsson C., Malmström L., Aebersold R., Malmström J. ( 2012). Proteome-wide selected reaction monitoring assays for the human pathogen Streptococcus pyogenes. Nature Commun 3:1301 [View Article][PubMed]
     [Google Scholar]
  17. Lei B., Mackie S., Lukomski S., Musser J. M. ( 2000). Identification and immunogenicity of group A Streptococcus culture supernatant proteins. Infect Immun 68:6807–6818 [View Article][PubMed]
     [Google Scholar]
  18. Loughman J. A., Caparon M. ( 2006). Regulation of SpeB in Streptococcus pyogenes by pH and NaCl: a model for in vivo gene expression. J Bacteriol 188:399–408 [View Article][PubMed]
     [Google Scholar]
  19. Malmström L., Marko-Varga G., Westergren-Thorsson G., Laurell T., Malmström J. ( 2006). 2DDB – a bioinformatics solution for analysis of quantitative proteomics data. BMC Bioinformatics 7:158 [View Article][PubMed]
     [Google Scholar]
  20. Malmström J., Karlsson C., Nordenfelt P., Ossola R., Weisser H., Quandt A., Hansson K., Aebersold R., Malmström L., Björck L. ( 2012a). Streptococcus pyogenes in human plasma: adaptive mechanisms analyzed by mass spectrometry-based proteomics. J Biol Chem 287:1415–1425 [View Article][PubMed]
     [Google Scholar]
  21. Malmström L., Malmström J., Selevsek N., Rosenberger G., Aebersold R. ( 2012b). Automated Workflow for large-scale selected reaction monitoring experiments. J Proteome Res 11:1644–1653 [View Article][PubMed]
     [Google Scholar]
  22. Nature Methods Editors ( 2013). Method of the year 2012. Nature Methods 10:1–1 [View Article]
     [Google Scholar]
  23. Nitsche-Schmitz D. P., Johansson H. M., Sastalla I., Reissmann S., Frick I.-M., Chhatwal G. S. ( 2007). Group G streptococcal IgG binding molecules FOG and protein G have different impacts on opsonization by C1q. J Biol Chem 282:17530–17536 [View Article][PubMed]
     [Google Scholar]
  24. Nordahl E. A., Rydengård V., Nyberg P., Nitsche D. P., Mörgelin M., Malmsten M., Björck L., Schmidtchen A. ( 2004). Activation of the complement system generates antibacterial peptides. Proc Natl Acad Sci U S A 101:16879–16884 [View Article][PubMed]
     [Google Scholar]
  25. Picotti P., Aebersold R. ( 2012). Selected reaction monitoring-based proteomics: workflows, potential, pitfalls and future directions. Nat Methods 9:555–566 [View Article][PubMed]
     [Google Scholar]
  26. Rasmussen M., Björck L. ( 2002). Proteolysis and its regulation at the surface of Streptococcus pyogenes. Mol Microbiol 43:537–544 [View Article][PubMed]
     [Google Scholar]
  27. Reis K. J., Ayoub E. M., Boyle M. D. ( 1984). Streptococcal Fc receptors. I. Isolation and partial characterization of the receptor from a group C streptococcus. J Immunol 132:3091–3097[PubMed]
     [Google Scholar]
  28. Severin A., Nickbarg E., Wooters J., Quazi S. A., Matsuka Y. V., Murphy E., Moutsatsos I. K., Zagursky R. J., Olmsted S. B. ( 2007). Proteomic analysis and identification of Streptococcus pyogenes surface-associated proteins. J Bacteriol 189:1514–1522 [View Article][PubMed]
     [Google Scholar]
  29. Sjöbring U., Falkenberg C., Nielsen E., Akerström B., Björck L. ( 1988). Isolation and characterization of a 14-kDa albumin-binding fragment of streptococcal protein G. J Immunol 140:1595–1599[PubMed]
     [Google Scholar]
  30. Solis N., Larsen M. R., Cordwell S. J. ( 2010). Improved accuracy of cell surface shaving proteomics in Staphylococcus aureus using a false-positive control. Proteomics 10:2037–2049 [View Article][PubMed]
     [Google Scholar]
  31. Takahashi T., Ubukata K., Watanabe H. ( 2011). Invasive infection caused by Streptococcus dysgalactiae subsp. equisimilis: characteristics of strains and clinical features. J Infection Chemother 17:1–10 [View Article][PubMed]
     [Google Scholar]
  32. Wollein Waldetoft K., Svensson L., Mörgelin M., Olin A. I., Nitsche-Schmitz D. P., Björck L., Frick I.-M. ( 2012). Streptococcal surface proteins activate the contact system and control its antibacterial activity. J Biol Chem 287:25010–25018 [View Article][PubMed]
     [Google Scholar]
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Surface proteins of group G Streptococcus in different phases of growth: patterns of production and implications for the host–bacteria relationship
Microbiology 160, 279 (2014); https://doi.org/10.1099/mic.0.071332-0
/content/journal/micro/10.1099/mic.0.071332-0
/content/journal/micro/10.1099/mic.0.071332-0
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