Skip to content
1887

Abstract

Human skin is our primary physical barrier and largest immune organ, and it also hosts a protective microbiota. Staphylococci are prominent members of the skin microbiota, including the ubiquitous coagulase-negative staphylococci (CoNS). The coagulase-positive is found as part of the microbiota, but it poses clinical concern due to its potential pathogenicity and antibiotic resistance. Recently, a CoNS, , has been shown to inhibit growth via the production of a novel antibiotic, lugdunin. In this study, we use human skin models to understand the spatial relationships between the CoNS and with during colonization of human skin. We investigated the attachment patterns of the bacteria, both individually and in competition. Surprisingly, we found that attachment did not always correlate with colonization ability. exhibited significantly reduced attachment to human skin stratum corneum but was an efficient longer-term colonizer. had a distinct attachment pattern on human corneocytes, with no significant overlap, or competitive exclusion, with the other strains. is a potential probiotic strain, with a proven ability to suppress . Before this potential can be realized, however, further research is needed to understand how this strain adheres and interacts with other bacteria in the human skin microenvironment.

Funding
This study was supported by the:
  • Vetenskapsrådet (Award 2019-01460)
    • Principal Award Recipient: KeiraMelican
  • Novo Nordisk Fonden (Award NNF22OC0077593)
    • Principal Award Recipient: KeiraMelican
  • Karolinska Institutet (Award FUS-2019:0003)
    • Principal Award Recipient: KeiraMelican
  • Vetenskapsrådet (Award 2020–01790)
    • Principal Award Recipient: KeiraMelican
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.001522
2025-01-31
2025-11-11

Metrics

Loading full text...

Full text loading...

/deliver/fulltext/micro/171/1/mic001522.html?itemId=/content/journal/micro/10.1099/mic.0.001522&mimeType=html&fmt=ahah

References

  1. Byrd AL, Belkaid Y, Segre JA. The human skin microbiome. Nat Rev Microbiol 2018; 16:143–155 [View Article] [PubMed]
    [Google Scholar]
  2. Grice EA, Segre JA. The skin microbiome. Nat Rev Microbiol 2011; 9:244–253 [View Article] [PubMed]
    [Google Scholar]
  3. Grice EA, Kong HH, Conlan S, Deming CB, Davis J et al. Topographical and temporal diversity of the human skin microbiome. Science 2009; 324:1190–1192 [View Article] [PubMed]
    [Google Scholar]
  4. Kabashima K, Honda T, Ginhoux F, Egawa G. The immunological anatomy of the skin. Nat Rev Immunol 2019; 19:19–30 [View Article] [PubMed]
    [Google Scholar]
  5. Elias PM. Stratum corneum defensive functions: an integrated view. J Invest Dermatol 2005; 125:183–200 [View Article] [PubMed]
    [Google Scholar]
  6. Otto M. Staphylococci in the human microbiome: the role of host and interbacterial interactions. Curr Opin Microbiol 2020; 53:71–77 [View Article] [PubMed]
    [Google Scholar]
  7. Byrd AL, Belkaid Y, Segre JA. The human skin microbiome. Nat Rev Microbiol 2018; 16:143–155 [View Article] [PubMed]
    [Google Scholar]
  8. Jochum L, Stecher B. Label or concept - What Is a Pathobiont?. Trends Microbiol 2020; 28:789–792 [View Article] [PubMed]
    [Google Scholar]
  9. Mrochen DM, Fernandes de Oliveira LM, Raafat D, Holtfreter S. Staphylococcus aureus host tropism and its implications for murine infection models. Int J Mol Sci 2020; 21:7061 [View Article] [PubMed]
    [Google Scholar]
  10. Schulz A, Jiang L, de Vor L, Ehrström M, Wermeling F et al. Neutrophil Recruitment to Noninvasive MRSA at the stratum corneum of human skin mediates transient colonization. Cell Rep 2019; 29:1074–1081 [View Article] [PubMed]
    [Google Scholar]
  11. Lang JC, Brutscher A, Ehrström M, Melican K. Tissue resident cells differentiate S. aureus from S. epidermidis via IL-1β following barrier disruption in healthy human skin. PLOS Pathog 2024; 20:e1012056 [View Article] [PubMed]
    [Google Scholar]
  12. Mills KB, Roy P, Kwiecinski JM, Fey PD, Horswill AR. Staphylococcal corneocyte adhesion: assay optimization and roles of Aap and SasG adhesins in the establishment of healthy skin colonization. Microbiol Spectr 2022; 10:e0246922 [View Article] [PubMed]
    [Google Scholar]
  13. Mills KB, Roy P, Kwiecinski JM, Fey PD, Horswill AR. Staphylococcal corneocyte adhesion: assay optimization and roles of Aap and SasG adhesins in the establishment of healthy skin colonization. Microbiol Spectr 2022; 10:e0246922 [View Article] [PubMed]
    [Google Scholar]
  14. Roy P, Horswill AR, Fey PD. Glycan-dependent corneocyte adherence of Staphylococcus epidermidis mediated by the lectin subdomain of Aap. mBio 2021; 12: [View Article]
    [Google Scholar]
  15. Fleury OM, McAleer MA, Feuillie C, Formosa-Dague C, Sansevere E et al. Clumping factor B promotes adherence of Staphylococcus aureus to corneocytes in atopic dermatitis. Infect Immun 2017; 85:e00994-16 [View Article] [PubMed]
    [Google Scholar]
  16. Towell AM, Feuillie C, Vitry P, Da Costa TM, Mathelié-Guinlet M et al. Staphylococcus aureus binds to the N-terminal region of corneodesmosin to adhere to the stratum corneum in atopic dermatitis. Proc Natl Acad Sci U S A 2021; 118:e2014444118 [View Article] [PubMed]
    [Google Scholar]
  17. Feuillie C, Vitry P, McAleer MA, Kezic S, Irvine AD et al. Adhesion of Staphylococcus aureus to Corneocytes from Atopic Dermatitis Patients Is Controlled by Natural Moisturizing Factor Levels. mBio 2018; 9: [View Article]
    [Google Scholar]
  18. Zipperer A, Konnerth MC, Laux C, Berscheid A, Janek D et al. Human commensals producing a novel antibiotic impair pathogen colonization. Nature 2016; 535:511–516 [View Article] [PubMed]
    [Google Scholar]
  19. Heilbronner S, Foster TJ. Staphylococcus lugdunensis: a skin commensal with invasive pathogenic potential. Clin Microbiol Rev 2021; 34:e00205-20 [View Article] [PubMed]
    [Google Scholar]
  20. Liu P-Y, Huang Y-F, Tang C-W, Chen Y-Y, Hsieh K-S et al. Staphylococcus lugdunensis infective endocarditis: a literature review and analysis of risk factors. J Microbiol Immunol Infect 2010; 43:478–484 [View Article] [PubMed]
    [Google Scholar]
  21. Heilbronner S, Foster TJ. Staphylococcus lugdunensis: a skin commensal with invasive pathogenic potential. Clin Microbiol Rev 2021; 34:e00205-20 [View Article] [PubMed]
    [Google Scholar]
  22. Hussain M, Steinbacher T, Peters G, Heilmann C, Becker K. The adhesive properties of the Staphylococcus lugdunensis multifunctional autolysin AtlL and its role in biofilm formation and internalization. Int J Med Microbiol 2015; 305:129–139 [View Article] [PubMed]
    [Google Scholar]
  23. Heilbronner S, Holden MTG, van Tonder A, Geoghegan JA, Foster TJ et al. Genome sequence of Staphylococcus lugdunensis N920143 allows identification of putative colonization and virulence factors. FEMS Microbiol Lett 2011; 322:60–67 [View Article] [PubMed]
    [Google Scholar]
  24. Macintosh RL, Brittan JL, Bhattacharya R, Jenkinson HF, Derrick J et al. The terminal A domain of the fibrillar accumulation-associated protein (Aap) of Staphylococcus epidermidis mediates adhesion to human corneocytes. J Bacteriol 2009; 191:7007–7016 [View Article] [PubMed]
    [Google Scholar]
  25. Mills KB, Roy P, Kwiecinski JM, Fey PD, Horswill AR. Staphylococcal corneocyte adhesion: assay optimization and roles of Aap and SasG adhesins in the establishment of healthy skin colonization. Microbiol Spectr 2022; 10:e0246922 [View Article] [PubMed]
    [Google Scholar]
  26. Roy P, Horswill AR, Fey PD. Glycan-dependent corneocyte adherence of Staphylococcus epidermidis mediated by the lectin subdomain of Aap. mBio 2021; 12: [View Article]
    [Google Scholar]
  27. Lang JC, Brutscher A, Ehrstrom M, Melican K. Tissue resident cells differentiate S. aureus from S. epidermidis via IL-1beta following barrier disruption in healthy human skin disruption in healthy human skin. Microbiology 2024; 2024 [View Article]
    [Google Scholar]
  28. Flannagan RS, Brozyna JR, Kumar B, Adolf LA, Power JJ et al. In vivo growth of Staphylococcus lugdunensis is facilitated by the concerted function of heme and non-heme iron acquisition mechanisms. J Biol Chem 2022; 298:101823 [View Article] [PubMed]
    [Google Scholar]
  29. Brozyna JR, Sheldon JR, Heinrichs DE. Growth promotion of the opportunistic human pathogen, Staphylococcus lugdunensis, by heme, hemoglobin, and coculture with Staphylococcus aureus. Microbiologyopen 2014; 3:182–195 [View Article] [PubMed]
    [Google Scholar]
  30. Rosenstein R, Salazar BOT, Sauer C et al. Siderophore piracy enables the nasal commensal Staphylococcus lugdunensis to antagonize the pathogen Staphylococcus aureus. bioRxiv 2024 [View Article]
    [Google Scholar]
  31. Ibberson CB, Parlet CP, Kwiecinski J, Crosby HA, Meyerholz DK et al. Hyaluronan modulation impacts Staphylococcus aureus biofilm infection. Infect Immun 2016; 84:1917–1929 [View Article] [PubMed]
    [Google Scholar]
  32. Mack D, Siemssen N, Laufs R. Parallel induction by glucose of adherence and a polysaccharide antigen specific for plastic-adherent Staphylococcus epidermidis: evidence for functional relation to intercellular adhesion. Infect Immun 1992; 60:2048–2057 [View Article] [PubMed]
    [Google Scholar]
/content/journal/micro/10.1099/mic.0.001522
Loading
/content/journal/micro/10.1099/mic.0.001522
Loading

Data & Media loading...

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