Staphylococcus aureus Colonization of the Human Nose and Interaction with Other Microbiome Members

Abstract

Staphylococcus aureus is usually regarded as a bacterial pathogen due to its ability to cause multiple types of invasive infections. Nevertheless, S. aureus colonizes about 30% of the human population asymptomatically in the nares, either transiently or persistently, and can therefore be regarded a human commensal as well, although carriage increases the risk of infection. Whereas many facets of the infection processes have been studied intensively, little is known about the commensal lifestyle of S. aureus. Recent studies highlight the major role of the composition of the highly variable nasal microbiota in promoting or inhibiting S. aureus colonization. Competition for limited nutrients, trace elements, and epithelial attachment sites, different susceptibilities to host defense molecules and the production of antimicrobial molecules by bacterial competitors may determine whether nasal bacteria outcompete each other. This chapter summarizes our knowledge about mechanisms that are used by S. aureus for efficient nasal colonization and strategies used by other nasal bacteria to interfere with its colonization. An improved understanding of naturally evolved mechanisms might enable us to develop new strategies for pathogen eradication.

FIGURE 1

Attachment mechanisms of S. aureus in the human nasal cavity. The anterior and posterior parts of the human nose are lined by different types of epithelial cell, which require alternative bacterial adhesion mechanisms. For the keratinized stratified squamous epithelium in the anterior nasal cavity, S. aureus predominantly uses cell wall-attached surface proteins (MSCRAMMs) (2, 41). In contrast, the primary attachment in the posterior area, composed of a pseudostratified columnar ciliated epithelium, is mediated by specific interaction of the cell-wall linked wall teichoic acid (WTA) with the scavenger receptor class F member 1 (SREC1) (41, 46). The corneocytes (desquamated epithelial cells) in the anterior nasal cavity contain high levels of the proteins loricrin, cytokeratin 10, and involucrin (55). S. aureus can express a variety of cell wall proteins, which bind to these matrix proteins. The S. aureus adhesin clumping factor B (ClfB) binds to cytokeratin 10 and loricrin (48, 52), whereas the iron-regulated surface determinant A (IsdA) can also interact with involucrin (55). In addition, the S. aureus serine-aspartate repeat-containing protein D (SdrD) mediates adhesion to human squamous epithelial cells by binding to desmoglein 1 (56). Some S. epidermidis isolates secrete an extracellular serine protease (Esp), which inhibits S. aureus colonization by degradation of the surface proteins IsdA and SdrD and host receptors (77, 78). In addition, S. lugdunensis can prevent nasal colonization of S. aureus by producing the cyclic thiazolidine-containing peptide antibiotic lugdunin (35).

FIGURE 2

Established interactions between nasal bacteria. C. accolens and Propionibacterium spp. can promote the colonization by S. aureus (green boxes) by modulation of its adhesive capacities (20, 85) (blue arrows), while specific clones of S. epidermidis, S. lugdunensis, and Streptococcus spp. can lead to S. aureus growth inhibition (orange boxes). Some S. epidermidis isolates secrete high levels of extracellular serine protease (Esp), which inhibits S. aureus nasal colonization (77) (yellow arrow). In addition, S. epidermidis and S. lugdunensis can impede S. aureus colonization by producing antimicrobial molecules (35, 64) (black arrows). S. pneumoniae can release hydrogen peroxide, which leads to prophage activation in S. aureus along with phage-mediated lysis of S. aureus cells (80, 81) (red arrow).