The ability of Staphylococcus aureus to proliferate within nasal communities is strain-specific and dependent on resource availability

Introduction

The asymptomatic nasal colonization of Staphylococcus aureus increases the risk of infection and concerns approximatively 30% of the population. The underlying molecular principles and especially the role of the endogenous microbiota in this carriage pattern are poorly understood. We hypothesize that, depending on their composition and origin, nasal bacterial communities can promote or inhibit the proliferation of S. aureus within nares.

Goals

Characterize how S. aureus interacts with nasal commensals and communities from different volunteers.

Methods

Three nasal communities of different composition and S. aureus carriage level were reconstituted by isolating the nasal bacterial species of healthy volunteers. Using these communities and the corresponding resident strains of S. aureus, in addition to a reference S. aureus strain, we performed (i) pairwise interactions experiments between individual strains, (ii) in vitro co-cultivations between S. aureus and synthetic communities and (iii) in vivo nasal co-colonization assays in gnotobiotic mice. Bacterial proliferation, community structure and metabolomics profiles were monitored.

Results

Two of the tested communities showed predominantly negative pairwise interactions in vitro and inhibited all S. aureus strains regardless of their origin. Instead, the last community was dominated by cooperative interactions, and the corresponding synthetic consortia promoted the survival of S. aureus. This effect appeared to be specific to the S. aureus nasal strain that was co-isolated with the community and promoted in poor medium, suggesting the existence of co-adaptation mechanisms for resource acquisition. First in vivo experiments indicate that, as observed in vitro, this cooperative community does not interfere with nasal colonization of the reference S. aureus strain.

Conclusions

Nasal communities display different interaction patterns that can either support or hinder S. aureus proliferation. The strain-specific nature of these interactions could explain why certain communities are invaded by this pathogen, and could inform strategies for preventing nasal colonization by S. aureus.