Nutritional Interactions between Bacterial Species Colonising the Human Nasal Cavity: Current Knowledge and Future Prospects

Abstract

The human nasal microbiome can be a reservoir for several pathogens, including Staphylococcus aureus. However, certain harmless nasal commensals can interfere with pathogen colonisation, an ability that could be exploited to prevent infection. Although attractive as a prophylactic strategy, manipulation of nasal microbiomes to prevent pathogen colonisation requires a better understanding of the molecular mechanisms of interaction that occur between nasal commensals as well as between commensals and pathogens. Our knowledge concerning the mechanisms of pathogen exclusion and how stable community structures are established is patchy and incomplete. Nutrients are scarce in nasal cavities, which makes competitive or mutualistic traits in nutrient acquisition very likely. In this review, we focus on nutritional interactions that have been shown to or might occur between nasal microbiome members. We summarise concepts of nutrient release from complex host molecules and host cells as well as of intracommunity exchange of energy-rich fermentation products and siderophores. Finally, we discuss the potential of genome-based metabolic models to predict complex nutritional interactions between members of the nasal microbiome.

Keywords: Staphylococcus aureus; bacterial interaction; nasal microbiome; nutritional interaction.

Figure 1

Production and consumption of small molecules. Bacteria can secrete fermentation products such as acetoin and 2,3-butanediol, which might support growth of another cohabitant bacterium. Siderophores bind iron (Fe³⁺) and can be taken up not only by the producing bacterium but also by other bacteria with a matching receptor and transporter. Oxygen consumption by one species can relieve growth inhibition of anaerobic species. This figure was created with BioRender.com.

Figure 2

Release of nutrients from host macromolecules. Bacteria can release nutrients from different human macromolecules by secretion of degradative enzymes. Mucins (peptide chain with sugar side chains is shown) can be degraded by mucinases and sulphatases to release carbon and sulphate. Sialic acid is released from sialylated glycans (proteins modified with carbohydrates; here: blue square—N-acetylglucosamine, green circle—mannose, yellow circle—galactose, pink diamond—sialic acid) by the action of sialidases. Fatty acids, phosphate, carbon and nitrogen are released from lipoproteins, triacylglycerols, phospholipids and phosphocholine, respectively, by secretion of lipases and esterases. Lysis of red blood cells (RBCs) by haemolysins can release haemoglobin (hb). Not only the bacteria secreting the enzymes (here shown in red) but also other bacteria colonising the same niche might benefit from these nutrient sources, enhancing proliferation of the entire community. This figure was created with BioRender.com.

Figure 3

Microbiome members as a source of nutrients for other bacteria. Bacteria can degrade surface-exposed molecules of other bacteria and use them as nutrient sources. e.g., wall teichoic acids (WTA) can be degraded releasing glycerol-3-phosphate. Sialic acid (sia) can be acquired by degrading sialylated glycans. This figure was created with BioRender.com.

Figure 4

Metabolic models for prediction of bacterial interactions. Using metabolic models, primary metabolite interactions in bacterial communities can be modeled (blue box). Secondary metabolites such as siderophores and bacteriocins should also be regarded in predicting interactions (orange box) as well as public goods released from human host macromolecules (green box). This figure was created with BioRender.com.