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The rise of diversity in metabolic platforms across the Candidate Phyla Radiation.

ABSTRACT: BACKGROUND:A unifying feature of the bacterial Candidate Phyla Radiation (CPR) is a limited and highly variable repertoire of biosynthetic capabilities. However, the distribution of metabolic traits across the CPR and the evolutionary processes underlying them are incompletely resolved. RESULTS:Here, we selected ~?1000 genomes of CPR bacteria from diverse environments to construct a robust internal phylogeny that was consistent across two unlinked marker sets. Mapping of glycolysis, the pentose phosphate pathway, and pyruvate metabolism onto the tree showed that some components of these pathways are sparsely distributed and that similarity between metabolic platforms is only partially predicted by phylogenetic relationships. To evaluate the extent to which gene loss and lateral gene transfer have shaped trait distribution, we analyzed the patchiness of gene presence in a phylogenetic context, examined the phylogenetic depth of clades with shared traits, and compared the reference tree topology with those of specific metabolic proteins. While the central glycolytic pathway in CPR is widely conserved and has likely been shaped primarily by vertical transmission, there is evidence for both gene loss and transfer especially in steps that convert glucose into fructose 1,6-bisphosphate and glycerate 3P into pyruvate. Additionally, the distribution of Group 3 and Group 4-related NiFe hydrogenases is patchy and suggests multiple events of ancient gene transfer. CONCLUSIONS:We infer that patterns of gene gain and loss in CPR, including acquisition of accessory traits in independent transfer events, could have been driven by shifts in host-derived resources and led to sparse but varied genetic inventories.

SUBMITTER: Jaffe AL

PROVIDER: S-EPMC7304191 | biostudies-literature | 2020 Jun

REPOSITORIES: biostudies-literature

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The rise of diversity in metabolic platforms across the Candidate Phyla Radiation.

Jaffe Alexander L AL Castelle Cindy J CJ Matheus Carnevali Paula B PB Gribaldo Simonetta S Banfield Jillian F JF

BMC biology 20200619 1

<h4>Background</h4>A unifying feature of the bacterial Candidate Phyla Radiation (CPR) is a limited and highly variable repertoire of biosynthetic capabilities. However, the distribution of metabolic traits across the CPR and the evolutionary processes underlying them are incompletely resolved.<h4>Results</h4>Here, we selected ~ 1000 genomes of CPR bacteria from diverse environments to construct a robust internal phylogeny that was consistent across two unlinked marker sets. Mapping of glycolysi ...[more]

PMID: 32560683

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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.

Dataset Information

The rise of diversity in metabolic platforms across the Candidate Phyla Radiation.

Publications

The rise of diversity in metabolic platforms across the Candidate Phyla Radiation.

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