Bacteriophages facilitate nasal colonization of Staphylococcus aureus

  • Willem van Wamel, Department of Medical Microbiology and Infectious Diseases, Erasmus MC, Rotterdam, The Netherlands
  • Nelianne Verkaik, Department of Medical Microbiology and Infectious Diseases, Erasmus MC, Rotterdam, The Netherlands
  • Hèléne Boelens, Department of Medical Microbiology and Infectious Diseases, Erasmus MC, Rotterdam, The Netherlands
  • Susan Snijders, Department of Medical Microbiology and Infectious Diseases, Erasmus MC, Rotterdam, The Netherlands
  • Damian Mellis, Department of Medical Microbiology and Infectious Diseases, Erasmus MC, Rotterdam, The Netherlands
  • Willem van Leeuwen, Department of Medical Microbiology and Infectious Diseases, Erasmus MC, Rotterdam, The Netherlands
  • Alex van Belkum, Department of Medical Microbiology and Infectious Diseases, Erasmus MC, Rotterdam, The Netherlands
  • Background: The genes encoding for the inhibitory protein of Staphylococcus aureus (S. aureus) (chp), staphylococcal complement inhibitor (scn), staphylokinase (sak) and enterotoxin A (sea), cluster on the conserved 3’ end of β-hemolysin (hlb) converting bacteriophages (βC-Φ’s) forming an innate immune evasion cluster (IEC). In humans 90% of the S. aureus isolates carry a βC-Φ, whereas only 5,5% of the S. aureus strains isolated from cows are positive for an IEC. Objective: Do bacteriophages carrying an IEC play a role in nasal colonization of S. aureus in humans but not in animals? Methods: The distribution and stability of βC-Φ’s carrying an IEC in S. aureus strains isolated from the nose of 50 individuals (68% women and 32% men; age range 21-60 years; mean 39 years) was studied. Five nasal swabs were taken longitudinally. The first three swabs were taken with time intervals of 2 weeks, the last two with intervals of 4 weeks. Of every culture, 3 S. aureus colonies of each morphotype (based on colony morphology and haemolytic criteria), were stored. Stains were characterized by PFGE and spa-PCR. Further PCRs were performed using specific primers for chp, sak, sea, sep, scn, and hlb. Moreover, the prevalence of IEC carrying βC-Φ’s was studied in 77 earlier described S. aureus strains isolated from different animal species (24 of these strains are typical animal isolates and 53 are typical human isolates) and from 73 genetically related human isolates. Results: Of the 50 volunteers 42% are persistent S. aureus carriers, 10% intermittent and 48% are non carriers. 90% of the persistent carriers are colonized with the same IEC carrying S. aureus over a period of time; every carrier carries a different type of S. aureus strain though. In some cases IEC positive and IEC negative strains can be isolated from one nose, but the IEC negative stains -in compare to the IEC positive stains- are present in lower amount.
    Among typical animal strains isolated from animals 12.5% (3/24) are IEC positive.
    Further more typical human strains isolated from animals 43.4% (23/53) are IEC positive. Finally 83.6% (61/73) of the typical human strains isolated from humans sharing similar genetic backgrounds as the animal isolates that are typical human are IEC positive.

    Conclusion: Bacteriophages carrying IEC encoded immune modulators play a role in human nose colonization.