Patterns of gene content and co-occurrence constrain the evolutionary path toward animal association in CPR bacteria

Abstract

Bacteria from the Candidate Phyla Radiation (CPR) are small, likely episymbiotic organisms found across Earth's ecosystems. Despite their prevalence, the distribution of CPR lineages across habitats and the genomic signatures of transitions amongst these habitats remain unclear. Here, we expand the genome inventory for Absconditabacteria (SR1), Gracilibacteria, and Saccharibacteria (TM7), CPR bacteria known to occur in both animal-associated and environmental microbiomes, and investigate variation in gene content with habitat of origin. By combining phylogeny and habitat information, we show that bacteria from these three lineages have undergone multiple transitions from environmental habitats into animal microbiomes. Using computational co-occurrence analyses based on hundreds of metagenomes, we extend the prior suggestion that certain Saccharibacteria have broad bacterial host ranges and constrain possible host relationships for Absconditabacteria and Gracilibacteria. Full-proteome analyses show that Saccharibacteria from animal-associated microbiomes have, on average, smaller gene repertoires than their environmental counterparts and are enriched in numerous protein families, including those likely functioning in amino acid metabolism, phage defense, and detoxification of peroxide. In contrast, some freshwater Saccharibacteria encode a putative bacteriorhodopsin. For protein families that exhibited the clearest patterns of differential habitat distribution, we compared protein and species phylogenies to estimate the incidence of lateral gene transfer and genomic loss that occurred over the species tree. These analyses suggest that habitat transitions were likely not accompanied by large transfer or loss events, but rather were associated with continuous proteome remodeling. Thus, we speculate that CPR habitat transitions were driven largely by availability of suitable host taxa, and were reinforced by acquisition and loss of some capacities.

Acquisition of the arginine deiminase system benefits epiparasitic Saccharibacteria and their host bacteria in a mammalian niche environment

“…T he recent discovery of the Candidate Phyla Radiation (CPR), a large monophyletic radiation of phyla and superphyla that includes the group currently referred to as Patescibacteria (1) and accounts for over 26% of microbial diversity, has greatly expanded the bacterial tree of life (2)(3)(4). Among the CPR (>73 phyla), Saccharibacteria (formerly known as TM7) represents one of the only three phyla, the other two being uncultivated Candidatus Absconditabacteria and Candidatus Gracilibacteria, whose members are detected in mammalian microbiomes in addition to diverse environmental niches (5,6). Analyses suggest multiple acquisition events (transfer of bacteria from the environment to mammals that results in stable incorporation into the mammalian microbiome) in the past led to the current wide diversity, with convergent evolution of key functions allowing Saccharibacteria from the environment with already extremely reduced genomes to adapt to mammals (7).…”

Ecogenomics Sheds Light On Diverse Lifestyle Strategies In Freshwater CPR

“…A total of 1326 CPR genomes (1032 GTDB representative genomes, 282 freshwater CPR assembles in this study, 12 MAGs obtained by Jaffe et al [79]) were screened for the presence of rhodopsins. We were able to detect 115 rhodopsin sequences in 86 genomes, out of which 17 were predicted to be protonpumping rhodopsins while the rest had a reverse orientation (N-terminal in the inside, C-terminal in the outside of the membrane [80]) and were therefore inferred to be heliorhodopsins (HeRs).…”

“…Type I rhodopsin [100] can generate a PMF or ion gradient, which could be used for energy production. As some Saccharimonadia MAGs obtained from freshwater lake samples in Sweden and Finland, as well as from glacial surface ice in Greenland [79] encoded genes annotated with low con dence as bacteriorhodopsin, it was hypothesized that they might encode protein pumping rhodopsins (Supplementary Table S15). Bins that were investigated by Jaffe et al [79] form a freshwater cluster in our rhodopsin phylogeny in between Sensory Rhodopsin I (SRI) and II (SRII) (Figure 7), but we were unable to nd any of the proteins involved in the signal transduction from SRI/II in the near genome context [101,102] (Supplementary Figure S17).…”

Adapted protocol for Saccharibacteria co-cultivation: two new members join the club of Candidate Phyla radiation

“…Recent studies on microbial diversity in human and environmental samples based on whole metagenomics analyses has made it possible to identify a new group of microorganisms that are not well recognised by the 16S rRNA gene, and which continue to be resistant to culture: the Saccharibacteria or TM7, is the most studied CPR phylum and was named due to its sugar metabolism (17). Sequences belonging to this phylum have been systematically detected in several environmental and ecological samples, including soil, freshwater lakes, dolphin teeth, and termite guts (18,19). In addition, metagenomics studies have shown that members of TM7 are also present in the human microbiome, including the intestinal, oral, urinary, cutaneous, blood and vaginal microbiota (11,17,(20)(21)(22).…”

“…Saccharibacteria or TM7, is the most studied CPR phylum and was named due to its sugar metabolism (17). Sequences belonging to this phylum have been systematically detected in several environmental and ecological samples, including soil, freshwater lakes, dolphin teeth, and termite guts (18,19). In addition, metagenomics studies have shown that members of TM7 are also present in the human microbiome, including the intestinal, oral, urinary, cutaneous, blood and vaginal microbiota (11,17,(20)(21)(22).…”