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

Abstract

Introduction Microbial residents of the human oral cavity have long been a major focus of microbiology due to their influence on host health and intriguing patterns of site specificity amidst the lack of dispersal limitation. However, the determinants of niche partitioning in this habitat are yet to be fully understood, especially among taxa that belong to recently discovered branches of microbial life. Results Here, we assemble metagenomes from tongue and dental plaque samples from multiple individuals and reconstruct 790 non-redundant genomes, 43 of which resolve to TM7, a member of the Candidate Phyla Radiation, forming six monophyletic clades that distinctly associate with either plaque or tongue. Both pangenomic and phylogenomic analyses group tongue-specific clades with other host-associated TM7 genomes. In contrast, plaque-specific TM7 group with environmental TM7 genomes. Besides offering deeper insights into the ecology, evolution, and mobilome of 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 microbes. Additionally, we report that prophages are widespread among oral-associated TM7, while absent from environmental TM7, suggesting that prophages may have played a role in adaptation of TM7 to the host environment. Conclusions Our data illuminate niche partitioning of enigmatic members of the oral cavity, including TM7, SR1, and GN02, and provide genomes for poorly characterized yet prevalent members of this biome, such as uncultivated Flavobacteriaceae.

Complete genomes of clade G6 Saccharibacteria suggest a divergent ecological niche and lifestyle

“…Taken together, these analyses indicate that Saccharibacteria clade G6 is highly divergent from clade G1, and may have a different lifestyle, host, and host-dependencies. This is in line with the recent hypothesis that G6 reside on the tongue (G6 are referred to as 'T2' in reference 9) and have a long history of association with animal hosts, while G1 reside in dental plaque and were a much more recent acquisition from the environment (8,9). Interestingly, the species-level clade containing JB002 (the most reduced Saccharibacteria genome, with only 615 genes) was the only Saccharibacteria group that resided both on the tongue and in dental plaque (9).…”

“…Although it is not known how Saccharibacteria obtain needed metabolites from the host, a type IV pilus-like system is generally well-conserved across the group, has been proposed as a candidate mechanism (8,9), and was present in the G6 genomes here. The species-level clade that included JB001 and JB003 encoded a ~10,000bp putative prophage element, which was flanked by homologs to the PinE invertase and contained a T4SS VirD4 homolog and 4 hypothetical proteins, all with ~95% homology to a similar region in Streptococcus salivarius.…”

“…While 97% of the pan-Saccharibacteria Core Genes and 89% of the G1 Core Genes had known COG functions and pathways, only 50% of the G6 Core Genes had known COG functions and pathways (Figure 2A), highlighting the enigmatic nature of this clade. The likely reason for the lower number of G1 core genes is the larger amount of known diversity within the G1 clade and the genomes analyzed here (8,9), leading to less conservation across the G1 pangenome. A larger pangenome analysis, examining all 11 G6 genomes and 14 diverse G1 genomes is available in Figure S2 and Table S4.…”

“…Saccharibacteria contains at least 6 distinct clades (G1-G6) (7,8), however all currently available human-associated complete genomes and cultured isolates belong to clade G1, leaving clades G2-G6 quite poorly understood. Several recent publications have provided the first draft genomes from clades G3, G5, and G6 (4,(8)(9)(10)(11). Obtaining complete genomes is of particular importance for Saccharibacteria, because they lack many of the "essential" single-copy core genes that are typically used to estimate genome completion, as well as complete reference genomes outside of the G1 clade.…”

The economical lifestyle of CPR bacteria in groundwater allows little preference for environmental drivers

“…The values and bp as well as and 10000 bp were used as -min and -max parameters to calculate 4-mer frequencies for Abawaca and ESOM (the script esomWrapper.pl, https://github.com/tetramerFreqs/Binning), and both the 40 and 107 marker gene sets were utilized in Maxbin2. DASTool v1.1 [14] was used to determine the best bins among these approaches. Bins were further refined manually inside the Anvi'o workflow v6.1 [35,36].…”