Human skin commensals augment Staphylococcus aureus pathogenesis

Nat Microbiol. 2018 Aug;3(8):881-890. doi: 10.1038/s41564-018-0198-3. Epub 2018 Jul 16.

Abstract

All bacterial infections occur within a polymicrobial environment, from which a pathogen population emerges to establish disease within a host. Emphasis has been placed on prevention of pathogen dominance by competing microflora acting as probiotics1. Here we show that the virulence of the human pathogen Staphylococcus aureus is augmented by native, polymicrobial, commensal skin flora and individual species acting as 'proinfectious agents'. The outcome is pathogen proliferation, but not commensal. Pathogenesis augmentation can be mediated by particulate cell wall peptidoglycan, reducing the S. aureus infectious dose by over 1,000-fold. This phenomenon occurs using a range of S. aureus strains and infection models and is not mediated by established receptor-mediated pathways including Nod1, Nod2, Myd88 and the NLPR3 inflammasome. During mouse sepsis, augmentation depends on liver-resident macrophages (Kupffer cells) that capture and internalize both the pathogen and the proinfectious agent, leading to reduced production of reactive oxygen species, pathogen survival and subsequent multiple liver abscess formation. The augmented infection model more closely resembles the natural situation and establishes the role of resident environmental microflora in the initiation of disease by an invading pathogen. As the human microflora is ubiquitous2, its role in increasing susceptibility to infection by S. aureus highlights potential strategies for disease prevention.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Bacteria / metabolism*
  • Disease Models, Animal
  • Humans
  • Inflammasomes / metabolism
  • Kupffer Cells / cytology
  • Kupffer Cells / immunology
  • Macrophages / metabolism
  • Mice
  • Microbiota
  • Peptidoglycan / metabolism
  • Peptidoglycan / pharmacology*
  • Reactive Oxygen Species / metabolism
  • Sepsis / immunology
  • Sepsis / microbiology*
  • Skin / microbiology*
  • Staphylococcal Infections / immunology
  • Staphylococcal Infections / microbiology*
  • Staphylococcus aureus / growth & development
  • Staphylococcus aureus / pathogenicity*
  • Symbiosis
  • Virulence

Substances

  • Inflammasomes
  • Peptidoglycan
  • Reactive Oxygen Species