Competitive advantage of oral streptococci for colonization of the middle ear mucosa
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 s...
| Main Authors: | , |
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| Format: | Article |
| Language: | English |
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Elsevier
2022-12-01
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| Series: | Biofilm |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S2590207522000016 |
| _version_ | 1811294438719225856 |
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| author | Kristin M. Jacob Gemma Reguera |
| author_facet | Kristin M. Jacob Gemma Reguera |
| author_sort | Kristin M. Jacob |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-04-13T05:17:24Z |
| format | Article |
| id | doaj.art-5cf4a421cb4741b7a0437685ab07c3e3 |
| institution | Directory Open Access Journal |
| issn | 2590-2075 |
| language | English |
| last_indexed | 2024-04-13T05:17:24Z |
| publishDate | 2022-12-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Biofilm |
| spelling | doaj.art-5cf4a421cb4741b7a0437685ab07c3e32022-12-22T03:00:51ZengElsevierBiofilm2590-20752022-12-014100067Competitive advantage of oral streptococci for colonization of the middle ear mucosaKristin M. Jacob0Gemma Reguera1Department of Microbiology and Molecular Genetics, Michigan State University, East Lansing, MI, USACorresponding author. 567 Wilson Rd., Rm, 6190 Biomedical & Physical Sciences building East Lansing, MI, 48824, USA.; Department of Microbiology and Molecular Genetics, Michigan State University, East Lansing, MI, USAThe 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.http://www.sciencedirect.com/science/article/pii/S2590207522000016Middle earEustachian tubeBiofilmsOtic microbiomeOral cavityOtopathogen |
| spellingShingle | Kristin M. Jacob Gemma Reguera Competitive advantage of oral streptococci for colonization of the middle ear mucosa Biofilm Middle ear Eustachian tube Biofilms Otic microbiome Oral cavity Otopathogen |
| title | Competitive advantage of oral streptococci for colonization of the middle ear mucosa |
| title_full | Competitive advantage of oral streptococci for colonization of the middle ear mucosa |
| title_fullStr | Competitive advantage of oral streptococci for colonization of the middle ear mucosa |
| title_full_unstemmed | Competitive advantage of oral streptococci for colonization of the middle ear mucosa |
| title_short | Competitive advantage of oral streptococci for colonization of the middle ear mucosa |
| title_sort | competitive advantage of oral streptococci for colonization of the middle ear mucosa |
| topic | Middle ear Eustachian tube Biofilms Otic microbiome Oral cavity Otopathogen |
| url | http://www.sciencedirect.com/science/article/pii/S2590207522000016 |
| work_keys_str_mv | AT kristinmjacob competitiveadvantageoforalstreptococciforcolonizationofthemiddleearmucosa AT gemmareguera competitiveadvantageoforalstreptococciforcolonizationofthemiddleearmucosa |