Site-specialization of human oral Gemella species

ABSTRACT

Gemella species are core members of the human oral microbiome in healthy subjects and are regarded as commensals, although they can cause opportunistic infections.

Our objective was to evaluate the site-specialization of Gemella species among various habitats within the mouth by combining pangenomics and metagenomics. With pangenomics, we identified genome relationships and categorized genes as core and accessory to each species. With metagenomics, we identified the primary oral habitat of individual genomes. Our results establish that the genomes of three species, G. haemolysans, G. sanguinis and G. morbillorum, are abundant and prevalent in human mouths at different oral sites: G. haemolysans on buccal mucosa and keratinized gingiva; G. sanguinis on tongue dorsum, throat, and tonsils; and G. morbillorum in dental plaque.

The gene-level basis of site-specificity was investigated by identifying genes that were core to Gemella genomes at a specific oral site but absent from other Gemella genomes. The riboflavin biosynthesis pathway was present in G. haemolysans genomes associated with buccal mucosa but absent from the rest of the genomes. Overall, metapangenomics show that Gemella species have clear ecological preferences in the oral cavity of healthy humans and provides an approach to identifying gene-level drivers of site specificity.

KEYWORDS:

• oral
• microbiome
• Gemella
• pangenome
• metagenome
• metapangenome

Acknowledgments

This work was supported by the NIH under Grants DE 030136 and DE 022586 and under Forsyth collaborative pilot project grant FSI_CP04. We thank Anthony McLean for critical insights in the analysis and Tabita Ramirez-Puebla for reading the manuscript. We thank A. Murat Eren and the anvi’o team for their assistance, consultations, and support in the use of anvi’o.

Disclosure statement

No potential conflict of interest was reported by the authors.

Author contributions

J.T.M., J.M.W., F.E.D., and G.G.B. designed the study; J.T.M. acquired the data and performed the analysis; G.G.B., J.T.M., and J.M.W. wrote the manuscript. All authors reviewed the manuscript and approved the final version.

Supplementary material

Supplemental data for this article can be accessed online at https://doi.org/10.1080/20002297.2023.2225261

Additional information

Funding

The work was supported by the National Institute of Dental and Craniofacial Research [Grant DE 022586]; National Institute of Dental and Craniofacial Research [Grant DE 030136]; Forsyth collaborative pilot project [Grant FSI_CP04]