Competitive advantage of oral streptococci for colonization of the middle ear mucosa

Abstract

The identification of a diverse microbiome in otic secretions from healthy young adults challenged the entrenched dogma of middle ear sterility and underscored previously unknown roles for oral commensals in the seeding of otic biofilms. We gained insights into the selective forces that enrich for specific groups of oral migrants in the middle ear mucosa by investigating the phylogeny and physiology of 19 strains isolated previously from otic secretions and representing otic commensals (Streptococcus) or transient migrants (Staphylococcus, Neisseria and actinobacterial Micrococcus and Corynebacterium). Phylogenetic analyses of full length 16S rRNA sequences recovered from partially sequenced genomes resolved close relationships between the isolates and (peri)oral commensals. Physiological functions that facilitate mucosal colonization (swarming motility, surfactant production) and nutrition (mucin and protein degradation) were also widespread among the cultivars, as was their ability to grow in the presence or absence of oxygen. Yet, streptococci stood out for their enhanced biofilm-forming abilities under oxic and anoxic conditions and ability to ferment host-derived mucosal substrates into lactate, a key metabolic intermediate in the otic trophic webs. Additionally, the otic streptococci inhibited the growth of common otopathogens, an antagonistic interaction that could exclude competitors and protect the middle ear mucosa from infections. These adaptive traits allow streptococcal migrants to colonize the otic mucosa and grow microcolonies with syntrophic anaerobic partners, establishing trophic interactions with other commensals that mirror those formed by the oral ancestors in buccal biofilms.