Dataset Information

Lysogeny is prevalent and widely distributed in the murine gut microbiota.

ABSTRACT: Bacteriophages are central members and potential modulators of the gut microbiome; however, the ecological and evolutionary relationships of gut bacteria and phages are poorly understood. Here we investigated the abundance and diversity of lysogenic bacteria (lysogens) in the bacterial community of C57BL/6J mice by detecting integrated prophages in genomes reconstructed from the metagenome of commensal bacteria. For the activities of lysogens and prophages, we compared the prophage genomes with the metagenome of free phages. The majority of commensal bacteria in different taxa were identified as lysogens. More lysogens were found among Firmicutes and Proteobacteria, than among Bacteroidetes and Actinobacteria. The prophage genomes shared high sequence similarity with the metagenome of free phages, indicating that most lysogens appeared to be active, and that prophages are spontaneously induced as active phages; dietary interventions changed the composition of the induced prophages. By contrast, CRISPR-Cas systems were present in few commensal bacteria, and were rarely active against gut phages. The structure of the bacteria-phage infection networks was "nested-modular", with modularity emerging across taxonomic scales, indicating that temperate phage features have developed over a long phylogenetic timescale. We concluded that phage generalists contribute to the prevalence of lysogeny in the gut ecosystem.

SUBMITTER: Kim MS

PROVIDER: S-EPMC5864201 | biostudies-literature | 2018 Apr

REPOSITORIES: biostudies-literature

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Lysogeny is prevalent and widely distributed in the murine gut microbiota.

Kim Min-Soo MS Bae Jin-Woo JW

The ISME journal 20180207 4

Bacteriophages are central members and potential modulators of the gut microbiome; however, the ecological and evolutionary relationships of gut bacteria and phages are poorly understood. Here we investigated the abundance and diversity of lysogenic bacteria (lysogens) in the bacterial community of C57BL/6J mice by detecting integrated prophages in genomes reconstructed from the metagenome of commensal bacteria. For the activities of lysogens and prophages, we compared the prophage genomes with ...[more]

PMID: 29416123

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Project description:BackgroundAccumulating evidence indicates interactions between human milk composition, particularly sugars (human milk oligosaccharides or HMO), the gut microbiota of human infants, and behavioral effects. Some HMO secreted in human milk are unable to be endogenously digested by the human infant but are able to be metabolized by certain species of gut microbiota, including Bifidobacterium longum subsp. infantis (B. infantis), a species sensitive to host stress (Bailey & Coe, 2004). Exposure to gut bacteria like B. infantisduring critical neurodevelopment windows in early life appears to have behavioral consequences; however, environmental, physical, and social stress during this period can also have behavioral and microbial consequences. While rodent models are a useful method for determining causal relationships between HMO, gut microbiota, and behavior, murine studies of gut microbiota usually employ oral gavage, a technique stressful to the mouse. Our aim was to develop a less-invasive technique for HMO administration to remove the potential confound of gavage stress. Under the hypothesis that stress affects gut microbiota, particularly B. infantis, we predicted the pups receiving a prebiotic solution in a less-invasive manner would have the highest amount of Bifidobacteria in their gut.MethodsThis study was designed to test two methods, active and passive, of solution administration to mice and the effects on their gut microbiome. Neonatal C57BL/6J mice housed in a specific-pathogen free facility received increasing doses of fructooligosaccharide (FOS) solution or deionized, distilled water. Gastrointestinal (GI) tracts were collected from five dams, six sires, and 41 pups over four time points. Seven fecal pellets from unhandled pups and two pellets from unhandled dams were also collected. Qualitative real-time polymerase chain reaction (qRT-PCR) was used to quantify and compare the amount of Bifidobacterium, Bacteroides, Bacteroidetes, and Firmicutes.ResultsOur results demonstrate a significant difference between the amount of Firmicutes in pups receiving water passively and those receiving FOS actively (p-value = 0.009). Additionally, we found significant differences between the fecal microbiota from handled and non-handled mouse pups.DiscussionFrom our results, we conclude even handling pups for experimental purposes, without gavage, may induce enough stress to alter the murine gut microbiota profile. We suggest further studies to examine potential stress effects on gut microbiota caused by experimental techniques. Stress from experimental techniques may need to be accounted for in future gut microbiota studies.

Project description:UNLABELLED:Elucidation of the molecular mechanisms underlying the human gut microbiota's effects on health and disease has been complicated by difficulties in linking metabolic functions associated with the gut community as a whole to individual microorganisms and activities. Anaerobic microbial choline metabolism, a disease-associated metabolic pathway, exemplifies this challenge, as the specific human gut microorganisms responsible for this transformation have not yet been clearly identified. In this study, we established the link between a bacterial gene cluster, the choline utilization (cut) cluster, and anaerobic choline metabolism in human gut isolates by combining transcriptional, biochemical, bioinformatic, and cultivation-based approaches. Quantitative reverse transcription-PCR analysis and in vitro biochemical characterization of two cut gene products linked the entire cluster to growth on choline and supported a model for this pathway. Analyses of sequenced bacterial genomes revealed that the cut cluster is present in many human gut bacteria, is predictive of choline utilization in sequenced isolates, and is widely but discontinuously distributed across multiple bacterial phyla. Given that bacterial phylogeny is a poor marker for choline utilization, we were prompted to develop a degenerate PCR-based method for detecting the key functional gene choline TMA-lyase (cutC) in genomic and metagenomic DNA. Using this tool, we found that new choline-metabolizing gut isolates universally possessed cutC. We also demonstrated that this gene is widespread in stool metagenomic data sets. Overall, this work represents a crucial step toward understanding anaerobic choline metabolism in the human gut microbiota and underscores the importance of examining this microbial community from a function-oriented perspective. IMPORTANCE:Anaerobic choline utilization is a bacterial metabolic activity that occurs in the human gut and is linked to multiple diseases. While bacterial genes responsible for choline fermentation (the cut gene cluster) have been recently identified, there has been no characterization of these genes in human gut isolates and microbial communities. In this work, we use multiple approaches to demonstrate that the pathway encoded by the cut genes is present and functional in a diverse range of human gut bacteria and is also widespread in stool metagenomes. We also developed a PCR-based strategy to detect a key functional gene (cutC) involved in this pathway and applied it to characterize newly isolated choline-utilizing strains. Both our analyses of the cut gene cluster and this molecular tool will aid efforts to further understand the role of choline metabolism in the human gut microbiota and its link to disease.

Dataset Information

Lysogeny is prevalent and widely distributed in the murine gut microbiota.

Publications

Lysogeny is prevalent and widely distributed in the murine gut microbiota.

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