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Members of the Candidate Phyla Radiation are functionally differentiated by carbon- and nitrogen-cycling capabilities.

ABSTRACT: 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.

SUBMITTER: Danczak RE

PROVIDER: S-EPMC5581439 | biostudies-literature | 2017 Sep

REPOSITORIES: biostudies-literature

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Members of the Candidate Phyla Radiation are functionally differentiated by carbon- and nitrogen-cycling capabilities.

Danczak R E RE Johnston M D MD Kenah C C Slattery M M Wrighton K C KC Wilkins M J MJ

Microbiome 20170902 1

<h4>Background</h4>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, co ...[more]

PMID: 28865481

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Project description:The growing application of metagenomics to different ecological and microbiome niches in recent years has enhanced our knowledge of global microbial biodiversity. Among these abundant and widespread microbes, the candidate phyla radiation (CPR) group has been recognized as representing a large proportion of the microbial kingdom (>26%). CPR are characterized by their obligate symbiotic or exoparasitic activity with other microbial hosts, mainly bacteria. Currently, isolating CPR is still considered challenging for microbiologists. The idea of this study was to develop an adapted protocol for the coculture of CPR with a suitable bacterial host. Based on various sputum samples, we tried to enrich CPR (Saccharibacteria members) and to cocultivate them with pure hosts (Schaalia odontolytica). This protocol was monitored by TaqMan real-time quantitative PCR (qPCR) using a system specific for Saccharibacteria designed in this study, as well as by electron microscopy and sequencing. We succeeded in coculturing and sequencing the complete genomes of two new Saccharibacteria species, "Candidatus Minimicrobia naudis" and "Candidatus Minimicrobia vallesae." In addition, we noticed a decrease in the CT values of Saccharibacteria and a significant multiplication through their physical association with Schaalia odontolytica strains in the enriched medium that we developed. This work may help bridge gaps in the genomic database by providing new CPR members, and in the future, their currently unknown characteristics may be revealed. IMPORTANCE In this study, the first TaqMan real-time quantitative PCR (qPCR) system, targeting Saccharibacteria phylum, has been developed. This technique can specifically quantify Saccharibacteria members in any sample of interest in order to investigate their prevalence. In addition, another easy, specific, and sensitive protocol has been developed to maintain the viability of Saccharibacteria cells in an enriched medium with their bacterial host. The use of this protocol facilitates subsequent studies of the phenotypic characteristics of CPR and their physical interactions with bacterial species, as well as the sequencing of new genomes to improve the current database.

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

Members of the Candidate Phyla Radiation are functionally differentiated by carbon- and nitrogen-cycling capabilities.

Publications

Members of the Candidate Phyla Radiation are functionally differentiated by carbon- and nitrogen-cycling capabilities.

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