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Patterns of Gene Content and Co-occurrence Constrain the Evolutionary Path toward Animal Association in Candidate Phyla Radiation Bacteria.

ABSTRACT: Candidate Phyla Radiation (CPR) bacteria 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 among 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 overlaying phylogeny with habitat information, we show that bacteria from these three lineages have undergone multiple transitions from environmental habitats into animal microbiomes. Based on co-occurrence analyses of 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 animal-associated Saccharibacteria have 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 rhodopsin. For protein families exhibiting the clearest patterns of differential habitat distribution, we compared protein and species phylogenies to estimate the incidence of lateral gene transfer and genomic loss occurring 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. IMPORTANCE Studying the genetic differences between related microorganisms from different environment types can indicate factors associated with their movement among habitats. This is particularly interesting for bacteria from the Candidate Phyla Radiation because their minimal metabolic capabilities require associations with microbial hosts. We found that shifts of Absconditabacteria, Gracilibacteria, and Saccharibacteria between environmental ecosystems and mammalian mouths/guts probably did not involve major episodes of gene gain and loss; rather, gradual genomic change likely followed habitat migration. The results inform our understanding of how little-known microorganisms establish in the human microbiota where they may ultimately impact health.

SUBMITTER: Jaffe AL

PROVIDER: S-EPMC8406219 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:The Candidate Phyla Radiation (CPR) is a recently described expansion of the tree of life that represents more than 15% of all bacterial diversity and potentially contains over 70 different phyla. Despite this broad phylogenetic variation, these microorganisms appear to feature little functional diversity, with members generally characterized as obligate fermenters. Additionally, much of the data describing CPR phyla has been generated from a limited number of environments, constraining our knowledge of their functional roles and biogeographical distribution. To expand our understanding of subsurface CPR microorganisms, we sampled four separate groundwater wells over 2 years across three Ohio counties.Samples were analyzed using 16S rRNA gene amplicon and shotgun metagenomic sequencing. Amplicon results indicated that CPR members comprised between 2 and 20% of the microbial communities with relative abundances stable through time in Athens and Greene samples but dynamic in Licking groundwater. Shotgun metagenomic analyses generated 71 putative CPR genomes, representing roughly 32 known phyla and 2 putative new phyla, Candidatus Brownbacteria and Candidatus Hugbacteria. While these genomes largely mirrored metabolic characteristics of known CPR members, some features were previously uncharacterized. For instance, nitrite reductase, encoded by nirK, was found in four of our Parcubacteria genomes and multiple CPR genomes from other studies, indicating a potentially undescribed role for these microorganisms in denitrification. Additionally, glycoside hydrolase (GH) family profiles for our 71 genomes and over 2000 other CPR genomes were analyzed to characterize their carbon-processing potential. Although common trends were present throughout the radiation, differences highlighted potential mechanisms that could allow microorganisms across the CPR to occupy various subsurface niches. For example, members of the Microgenomates superphylum appear to potentially degrade a wider range of carbon substrates than other CPR phyla.CPR members are present across a range of environments and often constitute a significant fraction of the microbial population in groundwater systems, particularly. Further sampling of such environments will resolve this portion of the tree of life at finer taxonomic levels, which is essential to solidify functional differences between members that populate this phylogenetically broad region of the tree of life.

Project description:Microbes belonging to Candidate Phyla Radiation (CPR) have joined the tree of life as a new branch, thanks to the intensive application of metagenomics and sequencing technologies. CPR have been eventually identified by 16S rRNA analysis, and they represent more than 26% of microbial diversity. Despite their ultrasmall size, reduced genome, and metabolic pathways which mainly depend on exosymbiotic or exoparasitic relationships with the bacterial host, CPR microbes were found to be abundant in almost all environments. They can be considered survivors in highly competitive circumstances within microbial communities. However, their defense mechanisms and phenotypic characteristic remain poorly explored. Here, we conducted a thorough in silico analysis on 4,062 CPR genomes to search for antibiotic resistance (AR)-like enzymes using BLASTp and functional domain predictions against an exhaustive consensus AR database and conserved domain database (CDD), respectively. Our findings showed that a rich reservoir of divergent AR-like genes (n = 30,545 hits, mean = 7.5 hits/genome [0 to 41]) were distributed across the 13 CPR superphyla. These AR-like genes encode 89 different enzymes that are associated with 14 different chemical classes of antimicrobials. Most hits found (93.6%) were linked to glycopeptide, beta-lactam, macrolide-lincosamide-streptogramin (MLS), tetracycline, and aminoglycoside resistance. Moreover, two AR profiles were discerned for the Microgenomates group and "Candidatus Parcubacteria," which were distinct between them and differed from all other CPR superphyla. CPR cells seem to be active players during microbial competitive interactions; they are well equipped for microbial combat in different habitats, which ensures their natural survival and continued existence. IMPORTANCE To our knowledge, this study is one of the few studies that characterize the defense systems in the CPR group and describes the first repertoire of antibiotic resistance (AR) genes. The use of a BLAST approach with lenient criteria followed by a careful examination of the functional domains has yielded a variety of enzymes that mainly give three different mechanisms of action of resistance. Our genome analysis showed the existence of a rich reservoir of CPR resistome, which is associated with different antibiotic families. Moreover, this analysis revealed the hidden face of the reduced-genome CPR, particularly their weaponry with AR genes. These data suggest that CPR are competitive players in the microbial war, and they can be distinguished by specific AR profiles.

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Patterns of Gene Content and Co-occurrence Constrain the Evolutionary Path toward Animal Association in Candidate Phyla Radiation Bacteria.

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