Dewhirst
Floyd E.
Dewhirst
Floyd E.
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ArticleSite specialization of human oral veillonella species(American Society for Microbiology, 2023-01-25) Giacomini, Jonathan J. ; Torres-Morales, Julian ; Dewhirst, Floyd E. ; Borisy, Gary G. ; Mark Welch, Jessica L.Veillonella species are abundant members of the human oral microbiome with multiple interspecies commensal relationships. Examining the distribution patterns ofspecies across the oral cavity is fundamental to understanding their oral ecology. In this study, we used a combination of pangenomic analysis and oral metagenomic information to clarifytaxonomy and to test the site specialist hypothesis for thegenus, which contends that most oral bacterial species are adapted to live at specific oral sites. Using isolate genome sequences combined with shotgun metagenomic sequence data, we showed thatspecies have clear, differential site specificity: Veillonella parvula showed strong preference for supra- and subgingival plaque, while closely related V. dispar, as well as more distantly related V. atypica, preferred the tongue dorsum, tonsils, throat, and hard palate. In addition, the provisionally namedsp. Human Microbial Taxon 780 showed strong site specificity for keratinized gingiva. Using comparative genomic analysis, we identified genes associated with thiamine biosynthesis and the reductive pentose phosphate cycle that may enablespecies to occupy their respective habitats.Understanding the microbial ecology of the mouth is fundamental for understanding human physiology. In this study, metapangenomics demonstrated that differentspecies have clear ecological preferences in the oral cavity of healthy humans, validating the site specialist hypothesis. Furthermore, the gene pool of differentspecies was found to be reflective of their ecology, illuminating the potential role of vitamins and carbohydrates in determiningdistribution patterns and interspecies interactions.
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ArticleSite-specialization of human oral Gemella species(Taylor and Francis Group, 2023-06-22) Torres-Morales, Julian ; Mark Welch, Jessica L. ; Dewhirst, Floyd E. ; Borisy, Gary G.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.
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ArticleSpatial ecology of Haemophilus and Aggregatibacter in the human oral cavity(American Society for Microbiology, 2024-03-15) Giacomini, Jonathan J. ; Torres-Morales, Julian ; Tang, Jonathan ; Dewhirst, Floyd E. ; Borisy, Gary G. ; Mark Welch, Jessica L.Haemophilus and Aggregatibacter are two of the most common bacterial genera in the human oral cavity, encompassing both commensals and pathogens of substantial ecological and medical significance. In this study, we conducted a metapangenomic analysis of oral Haemophilus and Aggregatibacter species to uncover genomic diversity, phylogenetic relationships, and habitat specialization within the human oral cavity. Using three metrics—pangenomic gene content, phylogenomics, and average nucleotide identity (ANI)—we first identified distinct species and sub-species groups among these genera. Mapping of metagenomic reads then revealed clear patterns of habitat specialization, such as Aggregatibacter species predominantly in dental plaque, a distinctive Haemophilus parainfluenzae sub-species group on the tongue dorsum, and H. sp. HMT-036 predominantly in keratinized gingiva and buccal mucosa. In addition, we found that supragingival plaque samples contained predominantly only one out of the three taxa, H. parainfluenzae, Aggregatibacter aphrophilus, and A. sp. HMT-458, suggesting independent niches or a competitive relationship. Functional analyses revealed the presence of key metabolic genes, such as oxaloacetate decarboxylase, correlated with habitat specialization, suggesting metabolic versatility as a driving force. Additionally, heme synthesis distinguishes H. sp. HMT-036 from closely related Haemophilus haemolyticus, suggesting that the availability of micronutrients, particularly iron, was important in the evolutionary ecology of these species. Overall, our study exemplifies the power of metapangenomics to identify factors that may affect ecological interactions within microbial communities, including genomic diversity, habitat specialization, and metabolic versatility.