Functional and genetic markers of niche partitioning among enigmatic members of the human oral microbiome

Abstract

30Microbial residents of the human oral cavity have long been a major focus of microbiology due to their influence on host health and their intriguing patterns of site specificity amidst the lack of dispersal limitation. Yet, the determinants of niche partitioning in this habitat are yet to be fully understood, especially among the taxa that belong to recently discovered branches of microbial life. Here we assembled metagenomes from daily 35 tongue and dental plaque samples from multiple individuals and reconstructed 790 nonredundant genomes, 43 of which resolved to TM7 that formed six monophyletic clades distinctly associated either with plaque or with tongue. Both pangenomic and phylogenomic analyses grouped tongue-specific TM7 clades with other host-associated TM7 genomes. In contrast, plaque-specific TM7 grouped together with environmental 40 TM7 genomes. Besides offering deeper insights into the ecology, evolution, and the mobilome of the cryptic members of the oral microbiome, our study reveals an intriguing resemblance between dental plaque and non-host environments indicated by the TM7 evolution, suggesting that plaque may have served as a stepping stone for environmental microbes to adapt to host environments for some clades of human associated microbes. 45Additionally, we report that prophages are widespread amongst oral-associated TM7, while absent from environmental TM7, suggesting that prophages may have played a role in adaptation of TM7 to the host environment.

Metapangenomics of the oral microbiome provides insights into habitat adaptation and cultivar diversity

“…Only a small set of genes were present in all genomes of the TD group of H. parainfluenzae and not in any of the other isolate genomes; these genes are marked by a dark blue wedge labeled "TD group core" on the figure. We carried out a functional enrichment analysis, as described in Shaiber et al (2020), to compare the prevalence of predicted functions among TD genomes to their prevalence among non-TD genomes revealed by the metapangenome. This analysis identified exactly three functions in three gene clusters altogether encoding the three subunits of a sodium-dependent oxaloacetate decarboxylase enzyme exclusive to the TD group (Additional File 7).…”

“…The Baas-Becking hypothesis that "everything is everywhere, but the environment selects" (Baas-Becking, 1934) suggests that the isolation of a single cell does not necessarily imply the existence of a population. The mapping of metagenomic data to a cultivar genome, by contrast, does indicate the overall abundance of an isolate in a habitat (Kraal et al, 2014;Shaiber et al, 2020), and the depth of coverage provided by different samples can indicate that the location of highest abundance of a resident population may not be its original site of isolation. For example, the obligate bacterial symbiont TM7x was first isolated from a salivary sample in association with an Actinomyces odontolyticus strain (He et al, 2015).…”

“…However, as saliva is a transient mixture of bacteria shed from other oral sites, the ultimate source of TM7x remained ambiguous until metagenomic mapping was used to identify dental plaque as its native habitat (Shaiber et al 2020). Many of the genomes we used in this study came from strains isolated from sputum and non-oral sources such as blood, gallbladder, and skin (Additional File 3).…”

“…Functional enrichment analyses were carried out following the pipeline described in Shaiber et al (2020).…”

“…To investigate functional enrichment in one set of genomes compared to another, we recorded the proportion of genomes containing each TIGRFAM function. From this proportional data, the enrichment of each function in each group was determined using a logistic regression by the method of Shaiber et al (2020). The full enrichment data is presented in Additional File 7 for each gene.…”